The Evolutionary Consequences of Interspecific Competition

The Evolutionary Consequences of Interspecific Competition WALLACE ARTHUR I. Introduction . . . . . . . . . . . . . . . . I1. Proposed Patterns of Competitively-induced Evolution . . . . . A . Character Displacement . . . . . . . . . . . . B. Character Convergence . . . . . . . . . . . . C. Character Release . . . . . . . . . . . . . D . Evolution of Competitive Ability. . . . . . . . . . E . Genetic Feedback . . . . . . . . . . . . . F. Effects of Competition on Polymorphic Loci . . . . . . . I11. Some Coevolutionary Models . . . . . . . . . . . A . Introduction . . . . . . . . . . . . . . . B. The Models . . . . . . . . . . . . . . . IV . Criteria for Demonstrating Competitive Selection . . . . . . A . Criteria for Conclusive Demonstration of Character Displacement in Natural Populations . . . . . . . . . . . . . B. Criteria for Conclusive Demonstration of the Evolution of Interspecific . . . . . Competitive Ability in Experimental Populations V . The Evidence . . . . . . . . . . . . . . . . . . . . A . Changes in the Mean of Quantitative Characters B . Changes in the Variance of Quantitative Characters . . . . . C. Changes in Heterozygosity and Gene-frequency . . . . . . VI . Conclusions . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . .

i27 129 129 131 131 132 133 134 136 136 137 145 145 149 150 150 173 174 181 182 182

.

I INTRODUCTION When populations of two different species compete with each other. both will suffer increased mortality and/or decreased natality . However. such effects are unlikely to be spread evenly across the various members of either population . If the two species concerned are cross-fertilizing plants or animals. then their populations will be genetically heterogeneous and indeed are likely to exhibit polymorphism at a large proportion of their genetic loci. (For a

128

WALLACE ARTHUR

review of the extent and nature of genetic variation in natural populations see Lewontin, 1974.) It is still not clear whether the majority of these polymorphisms affect fitness, but intensive studies on some loci have shown that in at least some polymorphisms, the different variants differ in their fitness under certain environmental conditions (see Clarke, 1975). It is likely that some of the polymorphisms affecting fitness influence the interspecific competitive ability. If this is so, then the competing populations may each evolve as a result of their competitive interaction. This will apply equally to chromosomal polymorphism and to heritable variation in quantitative characters, where these also affect competitive ability. Early models of interspecific competition did not take into account the possibility that different genetic variants within each population might differ in their ability to compete (for example Volterra, 1926). Nevertheless, such variation in competitive ability has now been shown to exist in a number of cases (see Section V). More recent models of competition, such as that of Lawlor and Maynard Smith (1976), have included provision for genetic variation. Whether competitively-induced evolutionary change will actually be effective in natural populations depends partly on the competitive population dynamics. If one species is rapidly excluded by a superior competitor it will have little time in which to exhibit an evolutionary response. Given a state of stable coexistence, however, or a very slow trends towards competitive exclusion, a similar selective differential within one (or both) species will have a much longer time in which to take effect. The main aim of this article is to assess the degree to which genetic changes in mixed species populations can be ascribed to natural selection resulting from interspecific competition. In order to achieve this aim, I will proceed through a number of steps. Firstly, the main postulated patterns of competitively-induced evolution will be outlined. Secondly, the relevant theoretical models will be briefly discussed. A series of criteria will then be developed which should be satisfied before an instance of variation in some character can be conclusively attributed to selection stemming from interspecific competition. Finally, experimental and observational case-studies on a wide range of species will be reviewed in the light of these criteria. It is necessary at the outset to give the definition of interspecific competition which will be adopted, since several alternative definitions are available. The populations of two species are considered to be in competition here if each exerts an inhibitory effect on the growth-rate or equilibrium size of the other. This corresponds to the (-, -) population-interaction described by Odum (1971) and elaborated by Williamson (1972). The mutual inhibitory effect can be achieved in two rather different ways; directly, for example, by the secretion of substances which harm the other species, in which case we have interference competition; or indirectly, through depletion of a common

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

129

limiting resource, which may be described as exploitative competition. It should be stressed that if only one population suffers in the interaction, while the other is unaffected, then this falls outside the definition of competition adopted, and this asymmetrical type of interaction is referred to as amensalism. For further discussion of the relationships between competition and other sorts of population-interaction, see Odum (1971; p. 21 1). For verbal economy I will often use the words competition, competitor and competitive in this review without a qualifying adjective. In all such cases the interspecific sense should be inferred. Finally, most of the discussion is centred on Competition between two species, since until this simplest case is understood it seems unlikely that discussion of the simultaneous coevolution of many competing species will be fruitful.

11. PROPOSED PATTERNS OF

COMPETITIVELY-INDUCED EVOLUTION Several different forms of evolutionary change, resulting from interspecific competition, have been proposed. These include character displacement (Brown and Wilson, 1956),character convergence (see Cody, 1973),alteration of the variance of morphological characters (Van Valen, 1965), evolution of competitive ability (Moore, 1952b) and genetic feedback (Pimentel et al., 1965). The aim of this section is to consider what is meant by such terms; and to discuss their relationships to, and differences from, each other. These discussions will serve two purposes. Firstly, they will reveal in some detail, and at an early stage, what the alternative possible modes of competitivelyinduced evolution are; and secondly, they will lead to the remainder of the review being left relatively free of controversy over terminology.

A. Character Displacement It has long been held that a common evolutionary consequence ofcompetition between two species is divergence of the species, in some character, in areas of sympatry. The character concerned may be ecological, behavioural, morphological or physiological, though the last of these possibilities has received little attention. This sort of divergence was termed character displacement by Brown and Wilson (1956), a term which has gained general acceptance. These authors also distinguished between reproductive and competitive character displacement. The former is an evolutionary response to the selective disadvantage of producing interspecific hybrids and is thus

130

WALLACE ARTHUR

synonymous with the Wallace Effect (see V. Grant, 1966 and review by Murray, 1972). Competitive character displacement, on the other hand, is an evolutionary response to interspecific competition. In the present article, I will be concerned only with competitive character displacement. Grant (1972), in a critical review of the subject, redefined character displacement, and some of his points deserve brief mention here. Firstly, in their original definition, Brown and Wilson (1956) referred specifically to animals; Grant extended the definition to include plants. In this respect, Grant’s definition seems preferable. There is some evidence for reproductive character displacement in plants (see Levin, 1970) though as yet there appears to be no botanical evidence for competitive displacement of non-reproductive characters. (Levin has suggested, though, that plants may diverge in reproductive characters for competitive reasons-for example, floral structure of angiosperms may diverge in sympatry to avoid competition for a limited supply of pollinators.) Secondly, Grant (1972) has restricted the term character displacement to include only changes in morphological characters. This is desirable on two grounds: because most studies of character displacement have in fact been morphologically orientated; and because the problem of unknown, possibly low heritabilities (discussed at some length later in connection with morphological characters) is even more acute with nonmorphological characters. Indeed it is likely, though by no means certain, that many ecological/behavioural changes associated with interspecific competition, such as Schoener’s (1975) “habitat shift”, may be nonevolutionary responses. The third of Grant’s (1972) modifications to the definition of character displacement will not be accepted here. Grant has argued that both convergence and divergence of a character in sympatry should be included under the overall heading of “character displacement”. Thus there would be convergent character displacement and divergent character displacement. This seems unnecessarily cumbersome and so I will treat convergence as a totally separate category from displacement. In a fourth modification, Grant (1972) distinguished between cases where allopatry preceded sympatry temporally and those where the reverse was true, considering only the former cases to be describable as character displacement. This distinction, which I will not make here, seems unhelpful since the timesequence of allopatry and sympatry is usually unknown. Finally Grant (1972) has distinguished between unilateral and bilateral displacement depending on whether one or both species displace in sympatry. This seems a useful distinction and I will retain it here. Mayr (1963) uses the term character divergence in preference to character displacement, apparently on the basis that Darwin (1 859) devoted much discussion to “divergence of character”. However, Darwin (1 859) used his “divergence of character” in a different, and much broader sense than Brown and Wilson (1956) used their term of

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

13 1

character displacement. Thus I will adhere to Brown and Wilson’s term. Throughout this article, then, competitive character displacement will refer to: the process by which the mean values of a morphological character, in two competing species, displace away from each other in areas of sympatry, or converge towards each other in allopatry, because of the presence in sympatric populations, but not in allopatric ones, of a selective pressure stemming from interspecific competition.

B. Character Convergence When two species become more similar in some character in sympatry, this may be termed character convergence-competitive character convergence where the selection producing the convergence emanates from competition. A theoretical argument suggesting that competition might lead to character convergence was put forward by MacArthur and Levins (1967), though this argument has been disputed by Lawlor and Maynard Smith (1976). Details of that dispute will be given in Section 111. The evidence for competitive convergence, as opposed to competitive displacement of characters is more restricted and is mostly related to interspecific territoriality in birds (see Cody, 1973). As with character displacement, the discussion of case-studies will be restricted to morphological characters, and only competitive convergence will be treated, though the difficulties of separating this from other sorts of sympatric convergence will form a major part of the discussion.

C. Character Release Both of the processes described above represent alterations in the mean value of a character. However, it has also been proposed that, as a result of competition, a change in the variance of a character may occur. Basically, an expansion of the feeding habits or the numbers of microsites occupied is thought to take place when a population moves to a relatively competitorfree environment such as, for example, an island. This phenomenon has been termed ecological release (Wilson, 1961). Note that the related term competitive release has been used by Yeaton and Cody (1974) in the slightly different sense of an increase in population density in competitor-free areas. An increased variability in ecological habits may lead to an increased variance of morphological characters (Van Valen, 1965) and I will refer to this as character release, in order to stress its relation to ecological and competitive release. (It should be noted that this usage of the term character release differs from Grant’s (1972) usage.) The process concerned is an example of

132

WALLACE ARTHUR

disruptive selection if migration is from a species-rich to a species-poor area, or stabilizing selection if migration is in the reverse direction. Since disruptive/ stabilizing selection and directional selection may occur simultaneously on the same character, release of a morphological character is not necessarily an alternative to displacement/convergence of the same character; the two processes may occur together.

D. Evolution of Competitive Ability Much of the evidence for and discussion of competitive character displacement, convergence and release has come from field-workers studying populations of vertebrates. However, considerable experimental work on interspecific competition has been conducted on laboratory populations of insects, notably Drosophila and Tribolium, as well as plants, and it is largely from this work that the concept of the evolution of competitive ability has arisen. A frequent observation in an experiment in which two species of insect are in competition for some food-medium, is that at some stage in the experiment the species-frequency trajectory in one cage suddenly alters from a gradual march towards competitive exclusion of one species to an increase in the frequency of that same species. In other words there is a reversal of competitive dominance, despite the environmental conditions being kept relatively constant. This sort of observation has been made on a number of occasions (for example, Ayala, 1966, 1969) and has often been interpreted as an evolutionary increase in the competitive ability of the species whose frequency has increased after first declining. Several points need to be made here. If competitive ability is to be measured, the variable by which it is measured should be independent of the species-frequency (i.e. the number of individuals of one species as a fraction, or percentage, of the combined numbers). It is thus dubious, at least in comparing competitive abilities between cages with different species-frequencies, to use the change in species-frequency itself (i.e. the equivalent of the geneticist’s Aq) as a measure of competitive ability. In fact the differential in competitive abilities that will produce an increase in the frequency of species 1 (say) of 17% in one generation of competition starting with equal numbers of both species will only produce a 9% alteration in species-frequency in an experiment started at 80% of species 1. Thus it is desirable to have a different measure of competitive ability, and one which has no inherent relationship with the species-frequency. One possible measure is the cross-product-ratio or C P R (see Cook, 1971 and Arthur, 1980a, b) or its natural log, which has been used as a measure of fitness in studies of polymorphism (for example Muggleton, 1979). The CPR measuring the competitive ability of species 1 relative to species 2

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

133

where N is the population size in the ith generation, subscripts refer to species, and N ‘ is the population size in the (i + l)Ih generation. In some situations, such as comparison of competitive abilities in cages started at the same species-frequency, or where the alteration in competitive ability is very marked (such as a “reversal”), the change in species-frequency itself may be a good enough estimator of competitive ability. If competitive ability is seen to alter during the course of an experiment (with reversals of dominance being an extreme case), and if this change can be attributed to selection, then there are two possible selective explanations. (1) The species which has increased in competitive ability has done so because it has become more efficient at inhibiting the other species or more efficient at obtaining or converting the resource it was already using. (2) The relative patterns of resource-utilization may have altered; for example, the species which has increased in competitive ability may have evolved so that it can utilize a greater, and/or shifted range of resources than before. The first of these explanations is often assumed to be correct because a single food-medium is generally used in the sort of experiment concerned. However, even a single food-medium may be chemically heterogeneous; some experiments in which competitive ability putatively evolved have provided more than one resource (for example, three in the experiments of Pimentel et al., 1965);and even a resource that is chemically homogeneous may require differing strategies to utilize different portions of it, for example, different layers within a resource-bottle. Thus the second explanation given above cannot be eliminated on a priori grounds alone, and so the relationship between character displacement (or its behavioural equivalent) and the evolution of competitive ability remains obscure. If explanation (1) is correct, the two processes are very different; if (2) is correct, they may not be.

E. Genetic Feedback This concept was advanced in conjunction with the results of an experiment by Pimentel et al. (1965) and will be described in detail along with those experimental results in Section V.A. Briefly, the hypothesis of genetic feedback is an extension of the idea that competitive abilities may evolve, whereby: (a) selection for increased interspecific competitive ability is stronger on the rarer species which thus evolves faster and eventually becomes competitively superior; (b) the process is then reversed; and (c) a series of evolutionary and

134

WALLACE ARTHUR

dynamic oscillations thus results, leading eventually to the stable coexistence of the two species.

F. Effects of Competition on Polymorphic Loci So far, I have discussed only the evolution of quantitative characters in response to competition between species. Although variation in such characters is contributed to by polymorphic variation at a large number of loci, the effects of most loci on their own are small. However, several studies have now been conducted in which the effect of selection on one polymorphic locus, or on a small group of such loci, has provided the focus of attention (Murphy (1976), Arthur (1978, 1980c), Powell and Wistrand (1978), Clark (1979) and Gosling (1980)). These studies will be described in Section V.C, but I will briefly state here the possible results of competitive selection at this level using, for illustrative purposes, the simplified situation of a biallelic locus, in each of two competing species (with alleles A 1 , A2 in species A ; B1,B2 in species B), which in some way affects competition. First of all, considering each of the species in turn, there are two possibilities: (1) If one homozygote is a superior competitor to the other, and there is complete, partial or no dominance, then the favoured allele will eventually become fixed in the population. (2) If the heterozygote is the most able interspecific competitor, the polymorphism will be balanced by competition, and will thus persist in the population with an equilibrium gene-frequency determined by the relative competitive abilities of the two homozygotes. It should be noted that these two possibilities exist when any selective agent is operating; here, they have merely been stated in such a way as to refer specifically to the situation where the selection stems from competition. However, when competition is the selective agent, both species may evolve. Thus their coevolution needs to be considered. Several combinations of the results described above are possible, since selection will operate separately in the two species, and there is no necessity for the ranking of genotypes by competitive ability to be the same in both. I wish in particular to distinguish between three forms of coevolution, which are as follows: (1) The selective differential within each species may depend on the genefrequency in the other (an extension of the concept of frequency-dependent selection (Clarke and O’Donald, 1964) to a two-species situation) such that single-locus equivalents of displacement and convergence are possible. Thus the species might displace or converge in gene-frequency in sympatric regions. (2) The selective differential within each species may be independent of the gene-frequency in the other. This would happen if one genotype, in each species, is simply a superior interspecific competitor to other genotypes. The

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

135

result of this situation would be a parallel change in sympatry (p(A1 ) increases in species A and p(B1) increases in species B) or an antithetical change (p(Al) increases but p(B1) decreases). If the polymorphisms are not analogous, then of course it would not be possible to say whether the coevolutionary changes were parallel or antithetical, but it would still be possible to distinguish these two possibilities, taken together, from the situation described under (1). (3) It is important to stress that, especially if species compete by interference rather than exploitation, the genetic bases of susceptibility and antagonistic ability may be separate. In such cases, limit cycles in gene-frequency may result. If, instead of one locus in each species we now consider two-an “attack” and a “defence” locus, then two limit cycles may be set up if one of species A’s “attack” genotypes is more effective on one of species B’s “defence” genotypes, and the same holds for species B “attacking” species A. This possibility has received little attention, though a simpler sort of limit-cycling behaviour in parasite-host coevolution has been dealt with by Clarke (1976). To summarize, then, there are several possible patterns of competitivelyinduced evolutionary change. Some of these, such as character displacement and character convergence, are mutually exclusive. Others, such as character displacement and character release, are not. Also, some relationships such as that between character displacement and the evolution of competitive ability, are obscure. Thus for any pair of competing species in a natural community, many possibilities are open, ranging from a complete lack of coevolution because (for example) of rapid competitive exclusion of one species, to the simultaneous occurrence of two or more of the processes described in this section. It is now necessary to enquire: (1) For which of these evolutionary patterns is there clear evidence from at least one species-pair? (2) How taxonomically and geographically widespread are the various patterns described, both in absolute terms and relative to each other? In order to answer these questions, it is necessary to consider the evidence from individual case-studies, and this will be done in Section V. First, though, some coevolutionary models which expand on some of the proposals of this section will be briefly discussed (Section III), and some criteria will be developed (Section IV) that case-studies should satisfy if they are to be regarded as providing conclusive evidence in favour of a particular coevolutionary pattern.

136

WALLACE ARTHUR

111. SOME COEVOLUTIONARY MODELS A. Introduction Initially, the models of population genetics assumed fixed selective coefficients, suggesting an unrealistic insensitivity of selection to population density, frequency of different phenotypes within the population, and the relative frequencies of the species concerned and those with which it interacted, such as competitors and parasites. Early ecological models, as already stressed, often assumed the equally unrealistic situation of genetically homogeneous populations. However, a substantial collection of models, treating both genetic and ecological factors as variables has now been built up; these are known as coevolutionary models, and have recently been reviewed by Slatkin and Maynard Smith (1979). Two somewhat separate questions have been asked in relation to the coevolution of interacting species: (1) What effects do the population dynamics of the interaction have on the extent and nature of evolutionary change in the interacting populations? (2) What are the effects of the genetic structure and evolution of the populations concerned on the outcome of their numerical interactions? These questions may be applied equally, of course, to predation and parasitism as well as interspecific competition. Also, with some rewording, they may be applied to a joint study of the evolution and dynamics of a single-species population. In the present article, I will be concerned only with a very restricted section of the field of coevolution. Firstly, only situations of interspecific competition will be considered. Secondly, since the article is concerned with “the evolutionary consequences of interspecific competition”, the emphasis will be on question (1) rather than question ( 2 ) . Finally, I will deal for the most part with two-species, as opposed to multi-species models, since the latter remain to be developed. Those readers wishing a more comprehensive review of coevolutionary models should consult Slatkin and Maynard Smith’s (1979) paper. The theoretical approach to the coevolution of competing species was pioneered by MacArthur and Levins (1964, 1967), and subsequent models have been provided by Levin (1969a, 1971), Leon (1974), Bulmer (1974), Crozier (1974), Lawlor and Maynard Smith ( 1 976), Roughgarden ( 1976), Fenchel and Christiansen (1977) and Slatkin (1980). These various models differ in some important ways and, as a result, arrive at sometimes different conclusions. The emphasis of the models at the outset may be different, some being predominantly concerned with directional evolutionary changes resulting from interspecific competition (for example Crozier, 1974), while

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

137

others (such as Llon, 1974) have been more preoccupied with the role of competition in maintaining genetic variability within the competing populations. Also, some models have dealt with continuously-variable characters, others with discrete variation. The models will now be briefly outlined, with emphasis on their assumptions and their predictions.

B. The Models MacArthur and Levins (1967) developed a graphical analysis of evolutionary change in competitors, following on from their earlier (1964)largely ecological study. These authors considered the evolution of a continuously variable character of unspecified inheritance, namely “niche position” (not breadth). A situation was described in which two species were already present in a community and a third, immigrant species subsequently appeared. Given sufficient genetic variation, the immigrant will evolve to a point of minimum combined competitive inhibition from the two resident species (i.e. minimum

a

@

Fig. 1. Graphical illustration of evolutionary change in niche-location, 4) represents phenotype, defined as the midpoint of the niche along some environmental axis. a1 and a2 are the values of the competition coefficients of the two (resident) competing species:(a) niche-separation; (b) “niche-convergence”.See text for further details. From MacArthur and Levins (1967).

138

WALLACE ARTHUR

a1 + a2). This results in a divergence of the immigrant away from either of the other two species to the point Q in cases where the two species are themselves sufficiently distant from each other that a1 + a2 is at a minimum between the separate modal a-values of species 1 and 2 (see Fig. la). However, when the a1 and a2 curves are closer (Fig. lb), there is no “intermediate minimum” and the immigrant converges, in niche-location, towards point P , which corresponds to the modal a-value of the less severe competitor. MacArthur and Levins point out that this convergence will only occur if “there is a large linear array of competing species”. This qualification is necessary since, if there is not such an array, the immigrant species may evolve past point P and hence ultimately diverge from both of the others. Lawlor and Maynard Smith (1976) dispute MacArthur and Levins’ second prediction, namely convergence, claiming that convergence would also occur in the absence of competition and so cannot be regarded as an evolutionary outcome of it. It is certainly clear from Fig. Ib that the convergence of the immigrant towards species 2 would occur in the absence of species 2 due simply to the immigrant’s divergence from species 1. (Whether the immigrant would move past point P in this case would depend on the amount of genetic variability present and on the presence or absence of further competitors.) A more detailed model has been developed by Levin (1969a, 1971) and is based on the Lotka-Volterra equation: dNi dt

~

= riNi

(Ki - N-,

ctNj

where N is the population size, r the intrinsic rate of increase, K the carrying capacity, a the competition coefficient; and i, j = 1, 2 for the simplified case of 2-species competition. Levin introduced variation into the parameters r, K and r so that the model becomes:

where h refers to genotypes within species i (there are gi of them); k refers to genotypes within speciesj; and ( i j h k is the inhibitory effect of an individual of genotype-k within speciesj on the growth of the genotype4 subgroup of species i. Using various numerical values for the parameters, Levin ran simulations to determine the result of competition and to examine the evolutionary changes within the competing populations. Some of his main conclusions are as follows. Variation in r has little effect on the outcome of competition, as would be expected from the well-known conditions for coexistence of the

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

139

Lotka-Volterra model, which do not involve r. Selection on K leads simply to the maximization of K, and this can have implications for the population dynamics, as can selection on the competition coefficients. In particular, if selection leads to a situation where each species inhibits itself more than the alternative species, and this was not the case prior to selection, then selection results in stable coexistence of the two species. However, Levin points out that the possible results of selection on variable competition coefficients are too numerous to yield a simple conclusion. In the restricted situation where one genotype of each species has a minimum sensitivity to competitive inhibition from all genotypes in both species, then selection will favour this genotype. One interpretation of this last result is that selection will favour genotypes within each species that are least similar to the alternative species. However, in addition to the fact that Levin only considered a restricted case, there are several assumptions built into his model. The model relates to a pair of asexual haploid species, each of which has an array of discrete genotypes. Time-lags (for example in competitive inhibition) are excluded from the model, as indeed they are in most similar ones. Also, for the most part, Levin considered selection on r, K and u separately. Thus the model’s predictions must be considered against this background. Leon (1974) has provided a model that is complementary to the previous one in that it deals with a pair of diploid sexual species. In each species there is assumed to be a biallelic locus (with alleles A1, A Z in species A; B1, BZ in species B ) which affects competition in some way. It is further assumed that no other polymorphic loci are involved and that while genotypes (at the A, B loci) vary in their sensitivity to competition, they do not vary in their ability to inhibit their competitors. For this situation, Leon’s equations (in discrete-time form) for changes in population density and allele-frequency respectively are:

+ 1) = F ( t ) N A ( t ) N B ( t + 1) = V ( t ) N B ( t )

NA(t

where N represents the population size, and pi the frequency of the iIh allele. Wi and Vi are estimates of the fitness of allele i in species A, B respectively, based on the genotypic adaptive values and gene-frequencies as follows:

1 40

WALLACE ARTHUR

wi(t)= C ~ 4 (wij(t) t) j

vi(t)= C p ? ( t ) vij(t). j

The genotypic adaptive values (Wij and Vij) are highest for those genotypes least affected by competition. Using this model, Leon investigated the evolution of the two species, and concentrated on establishing the conditions under which both will remain stably polymorphic. These conditions turn out to be heterozygous advantage in K and/or competitive sensitivity. That is, heterozygotes must have either the highest K-value or the lowest sensitivity to competition or both. Levin (1971) and Leon ( 1 974) gave special consideration to the possibility of genetic feedback (see Section V and Pimentel et al., 1965) and they reached a similar conclusion: evolutionarily-induced oscillations in numerical dominance of competing species can only occur if there is an inverse relationship between interspecific and intraspecific competitive abilities. Levin (1971) considered this unlikely to be a common occurrence, though he does point out that it could occur if the different components of competitive ability were improved by different alleles at the same locus. Levin concludes that a genetic mechanism for reversals of competitive dominance is not likely to be common and that “such reversals are not important to either evolutionary or ecological theory”. In contrast with Leon (1974), who was largely concerned with conditions for stable polymorphisms, Crozier (1974) investigated directional change in gene-frequency and phenotype-frequency in a similar system-two diploid species each with a biallelic locus affecting competition. Crozier considered a situation in which a resource-array, consisting of five discrete resources, was utilized by both species, with different genotypes within each species differing in their optimal resource, as shown below: Resource subunit Genotype of species A for which each resource is optimal Genotype of species B for which each resource is optimal

]

1

2

3

AA

AU

aa

BB

4

5

Bb

bb

The fitness of each genotype falls off to each side of its optimal resource and is given by:

where Fij is the fitness of genotype i on resource j ; Vi is the “utilization

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

141

phenotype” of genotype i (which is designated a value of optimal subunit +2); Vj is the optimal utilization phenotype for resourcej; and x is a constant (10 in the simulations performed by Crozier). A result of the above equation is that the fitness ofany genotype on its optimal resource is 1.0 and its fitness on any other resource is between 0 and 1. The survival ofeach genotype is given by the product ofits fitness (as defined above) and a crowding parameter. The results of the model are in fact predictable, at least in direction, from the allocation of optimal resources given in the table above. In particular, it is apparent from this table that only one genotype in each species shares an optimal resource with any members of the other species-namely, aa and BB. Thus it would be expected that these genotypes, and the corresponding phenotypes, would decline in frequency in sympatric populations. This indeed occurred in Crozier’s (1974) simulations. Various simulations, each with a different distribution of quantities of resource between the five subunits, showed qualitatively similar (but quantitatively different) patterns. Interspecific divergence in phenotype was universal but the exact pattern of divergence depended on the resource-distribution. This model shows, more vividly than most, the dependence of a model’s predictions on the assumptions built into it-in particular on the relative patterns of resource-utilization that are assigned to different genotypes. If the table of resource allocation had been constructed differently in this case, a completely different pattern of coevolutionary change could have been produced. The problem lies in deciding exactly what genotype/utilization relationship is most realistic, and as yet there are few data on which to base this decision. Bulmer (1974) approached the problem of competitively-induced evoiution in a different manner. He based his model on a continuously variable character, which affected competition, with individuals having similar values of this character competing more severely than those with different values. Unlike MacArthur and Levins (1967), Bulmer’s character had an explicit genetic basis, The character’s phenotypic value (y) was considered to be the result of the action of n loci, each with equal effect and without dominance, combined with an environmental component that was taken to be normally distributed. For each locus, then, we have: Genotypes With effects

CICl

+a

ClC2 0

C2C2 -a

on y.

Bulmer first extended the concept of density-dependent selection (see Clarke, 1972) to the case of metric characters, and then considered the effect of a second, competing species on the evolution of the character, y (in both species). He found that when, in addition to optimizing selection, of environmental origin, on y, there is also selection resulting from interspecific

142

WALLACE ARTHUR

competition, divergence of the two species will occur, but to a very limited extent. In fact, divergence will stop when the difference between the mean y-values, in the two species, ( M i - M 2 ) = 1,850,

which will not yield a bimodal distribution of the character concerned, since the condition for bimodality is (M1-

M2)

> 20,

where the two curves have equal values of 0. The small degree of difference between the two species that would result under the model would be insufficient to account for most purported examples of character displacement (Bulmer, 1974). The model can only predict a higher degree of displacement if the optimizing selection on y is largely a result of the genetic, rather than the external, environment. In this case, as selection proceeds, the “target value” of the optimizing selection changes simultaneously. A model by Lawlor and Maynard Smith (1976) has introduced, into the study of coevolving competitors, the concept of the evolutionarily stable strategy (or ESS). This is the strategy such that, when it is adopted, the population is resistant to invasion by mutant individuals with alternative strategies, (but subject to the same constraints as the other members of the population). The coevolutionary model of Lawlor and Maynard Smith is based on the following ecological model (from MacArthur, 1972; see also Stewart and Levin, 1973): 1 Xi

dX1 dt

-~

where

=~

+

I I W I R a12w2R2 I - TI

are the population sizes of consumer species I , 2; are the population sizes of resource species 1, 2; T1.2 are the threshold food requirements for the consumers to maintain themselves; ai, is the probability of capturing and consuming a unit of resource j per unit time (for an individual of species i); w, is the value of a unit of resource j to the consumer.

X1.2

R1.z

(Equations for the rate of change of the resource populations are also given by Lawlor and Maynard Smith, 1976.) The parameters chosen as the evolutionary variables were the aij’s. Importantly, a constraint was built into the model such that, within either

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFICCOMPETITION

143

species, phenotypes with improved ail suffered a decreased value of a i 2 .This was expressed in the form of two constraint equations: and a 2 2 = h2(a21) where the (declining) functions h~ and h2 may or may not be equal. As stated in the discussion of Crozier’s (1974) work, this sort of assumption is crucial to the predictions a model makes. It is pertinent to ask if the above relations between ail and ai2 are realistic. If the two resources were very different (e.g. worms and snails) then it would seem reasonable that as ail increases, ui2 should fall. However, if the resources were very similar (e.g. two closely related species of worm) then it would seem more likely that as ail increases, ai2 will also increase, though of course there must be some limit to their increase. The predictions of the model are that, although the ESSs for each species in the absence of competition would be generalist strategies, the coevolutionary ESSs are for the two species to evolve as specialists on different resources. In a coarse-grained environment, specialization will be complete, but in a fine-grained environment, specialization may only be partial. No cases of evolutionary convergence in patterns of resource-utilization were found. Lawlor and Maynard Smith (1976) state explicitly that no form of group selection is entailed in the coevolutionary process-the interspecific divergence towards complementary patterns of resource-utilization is achieved entirely by natural selection acting at the level of the individual in both species. Roughgarden (1976), in addition to developing some general coevolutionary models, dealt specifically with cases of competition in twospecies and three-species systems, where evolution of niche-location, but not niche-breadth, was permitted. The Lotka-Volterra equations (as described earlier in this section) formed the basis of the model, with Ks and as being genetically variable. The variation in both of these parameters, in Roughgarden’s model, derives from the variation in niche-location. Since nichebreadth is constant, the competition coefficients for two species are functions of the distance between their niche-locations. In addition, it is assumed that as niche-location moves along the spectrum of available resources, the resultant carrying capacity also varies. In this model, interspecific displacement in niche-location evolves, though Roughgarden shows that selection does not result in the species adopting niche-locations that maximize their population sizes. Also, the degree of displacement between “consecutive” species is higher in the two-species than in the three-species system. An interesting point made by Roughgarden (1976) is that natural selection will not necessarily favour increased ability, within one species, to competia12

= hl(al1)

1 44

WALLACE ARTHUR

tively inhibit the other species. This is despite the fact that if the more inhibitory type were fixed in a population, it would lead to a higher overall population size for that species. Indeed it may often be the case, as Roughgarden suggests, that “interspecific nastiness is selectively neutral”. However, it should be noted that this will not always be so. In particular, selection might well favour “nasty” genotypes in sedentary populations where the individuals concerned, and possibly their offspring, will reap the benefits of a localized inhibition of competitors. This difference in the action of selection on such traits in mobile and sedentary species may explain the commonness of allelopathic inhibition in plants (see Muller, 1970) and its relative rarity in animals. Like Roughgarden’s model, that of Fenchel and Christiansen (1977) involves systems of two and three species whose competitive interactions are described in terms of the Lotka-Volterra equations. Competition coefficients ( a ) are determined by the extent of overlap in patterns of utilization of a 1 -dimensional resource spectrum. Genetic variation is assumed to exist in only one species and takes the form of a biallelic locus, with the three genotypes differing in their competition coefficients. In the simplest situation, where only two species compete, where the resource spectrum is considered to be infinite, and where intraspecific competition is ignored, an evolutionary decrease in competition coefficients occurs. If niche breadth is fixed and the genetic variants differ only in niche position, then the decrease in the value of the competition coefficients takes the form of ecological displacement. If a third species is added to the system such that the genetically variable species has a utilization function intermediate between the other two, then Fenchel and Christiansen (1977) show that the variable species will evolve towards the midpoint between the utilization functions of the other two species. They also show that where effects of intraspecific competition are included, the prediction of displacement still applies. In a recent model put forward by Slatkin (1980),two species with discrete, non-overlapping generations compete for a limiting resource, with their competition being mediated by a continuously-variable character (designated z) which is normally distributed and under polygenic control. At any time t , we have a number Ni(t) of each species, whose mean character-value is .2i(t), with variance (ri2(t). Fitness values Wi(z) for individuals with each particular value of z are determined jointly by intra- and inter-specific competition. Slatkin (1980) used his model to explore the evolutionary consequences of competition in a number of different situations. The results are complex and suggest that displacement will occur under certain conditions but not under others. In particular, Slatkin shows that the existence of constraints on the genetic and phenotypic variance of the character, and the

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

145

nature of such constraints, has a considerable influence on the predictions. Constraints may arise due to pleiotropic effects of the genes contributing to the character (z) or because of selection on characters correlated with z. If, for some such reason, the variance in each species is constrained so that it is held below its single-species equilibrium value, displacement (divergence between 21 and 2 2 ) evolves rapidly. However, if the variance is held above its equilibrium, Z1 and Zz will converge towards each other. If there are no constraints on the variance, then permanent displacement will only occur if the two species have different patterns of resource-utilization in the absence of interspecific competition. The evolution of displacement in this case is essentially an equivalent, for quantitative characters, of the evolution of displacement at a single locus described by Crozier (1974) where correspondence between genotypes and resource-subunits differed between the two species.

IV. CRITERIA FOR DEMONSTRATING COMPETITIVE SELECTION Before considering the evidence from particular case-studies for evolutionary change in competing populations, it is desirable to consider what criteria a study should satisfy in order to provide an unambiguous conclusion. I will deal in particular with two sorts of study: first, studies of natural populations where variation in the mean value of a morphological character is attributed to character displacement; and second, experimental studies where a demonstration of the evolution of interspecific competitive ability is attempted. These have been chosen since they are the commonest sorts of study attempted in this field. However, many of the comments made are of general relevance.

A. Criteria for Conclusive Demonstration of Character Displacement in Natural Populations Studies falling under this heading typically involve the monitoring of a character along a transect which crosses from an allopatric to a sympatric region. If the mean values of the character, in the two species, diverge (either unilaterally or bilaterally) at the border between allopatry and sympatry, then it is often proposed that character displacement is the process responsible for this shift. However, a number of problems may arise in attempting to draw this conclusion. These will now be discussed in some detail, along with possible ways of avoiding them.

I46

WALLACE ARTHUR

1. The alteration in the mean value ofthe character at the allopatrylsympatry border should not be predictable from variation within either of these areas This point has been stressed by Grant (1972) and so requires less explanation than the others. Briefly, the argument is that, along a transect over a number of sampling sites, many characters will exhibit clinal variation. If the “displacement” of a character (in either species) could be merely an extension of a cline which started somewhere within (say) the allopatric region, then it is unnecessary to invoke a special explanation for the simple continuation of the cline. If, on the other hand, there is an abrupt change in the character’s mean value at the border between allopatry and sympatry, considerably steeper than any clinal gradient elsewhere on the transect, there may be a need for a special explanation. To distinguish which of the above two situations pertains, it is clearly necessary to take sufficient samples to get a good idea of the nature of variation within allopatry and within sympatry. A further complication here is that stepwise changes in genetically-based characters can occur even in the absence of stepwise environmental changes (see Clarke, 1966).

2. Sampling should be conducted along several geographically separate transects from allopatry to sympatry, each preferably located in an area whose habitat differs from that of the others The existence of an abrupt change in the mean value of a character, as described above, may, if it only occurs on a single transect, have a specific local explanation. However, if displacement occurs on many or all of a number of transects then some general explanation is required. Of course, it is very difficult to rule out the possibility that some environmental factor always associated with (and perhaps giving rise to) the border between allopatry and sympatry is itself the selective agent causing displacement. Indeed, it might be expected that allopatry/sympatry borders would occur at the position of steps in one or more environmental variables. However, this sort of explanation can at least be rendered less likely by taking transects (from allopatry to sympatry) in different places with different habitats.

3. Heritability must be estimated because if the characterdifference under study has a low or unknown heritability then an evolutionary explanation such as character displacement is suspect Heritability has not received nearly enough attention in studies of character displacement. By heritability, I mean the ratio of additive genetic variance

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

147

in a character to its total phenotypic variance, as described by Falconer (1960-quivalent to the “narrow heritability” of Mather and Jinks (1977). There are, however, several problems involved in the estimation and interpretation of this parameter. Firstly, the heritability of variation within and between populations may differ. Secondly, either of these two types of heritability may vary from place to place. Thirdly, there are complications in estimating heritability caused by interactions between genotype and environment (see Falconer, 1960). Finally, breeding experiments and rearing of the F1 generation in the laboratory may artificially reduce the environmental component of the variance and hence lead to an overestimate of the heritability. Despite these problems, estimates of heritability have been obtained in species which were the subject of evolutionary investigations other than character displacement, even some whose generation-time is fairly long (for example, shell size in land-snails with a 2-3 year generation time: Cook, 1965, 1967). There is no reason why similar studies should not be undertaken in species which have been the subject of investigations of character displacement, and their continued rarity in this field (with some notable exceptions such as the study by Boag and Grant, 1978) is unfortunate. If the heritability of a character is low or unknown then not only is there a serious gap in the argument for character displacement, but there is indeed a possible non-evolutionary explanation for frequent divergence in character between two species in sympatry, which is as follows. A commonly observed effect of crowding in single-species cultures is a decrease in the size of individuals. This has been noted in a wide range of organisms including Drosophila melanogaster (Bakker, 196l), the land-snail Cepaea nemoralis (Williamson et al., 1976), the seaweed fly Coelopa frigida (Collins, 1978) and the pond snail Lymnaea palustris (Forbes and Crampton, 1942).When populations of two competing species meet, a frequent result is an increase in the total density with a concomitant decrease in the densities of both individual species. In such situations, the effect of the different components of density on the size of individuals in each species has not been thoroughly studied. One possible outcome, however, is that the larger competitor will respond mainly to its own density, while the smaller species will respond to the overall density (see Wilson (1975) for a possible reason for this). Thus in sympatry the larger species would become larger, the smaller one smaller. Taking any morphological character that is positively correlated with size-and most are-then this too will exhibit sympatric divergence unless it is expressed as a fraction of total body size. Here, then, we have a possible non-genetic “mimic” of character displacement. In species where there is no clear distinction between juveniles and adults, there is the added problem that changes in age structure will affect the mean value of a character, assuming

148

WALLACE ARTHUR

that all individuals, or those above some arbitrary cut-off point are measured. This problem is discussed further in Section V.

4. selection resulting from interspeciJic competition is proposed, then it is desirable that there should be evidence that the species are indeed competing, and that the character investigated has some bearing on the competitive process The number of cases in which experimental evidence for interspecific competition is available is limited, and where such evidence exists it is incomplete (see Williamson, 1972 and Pianka, 1976). This is no doubt due in part to the practical difficulties involved in conducting the required “reciprocal explant” experiment, with sufficient replicates, in the field. Evidence for competition may also be difficult to obtain since, if character displacement has indeed occurred in a particular case, then the amount of competition still taking place may be considerably reduced. Circumstantial evidence for competition is more widely available but is of much more variable quality. If, in a particular case-study, there is little or no evidence that interspecific competition is occurring, then the case for competition being the selective agent, as in character displacement, is weak. If competition is occurring, a character would only be expected to exhibit displacement if it is involved in obtaining the limiting resource, whether it be food or space, and if the relationship between the patterns of resourceutilization of the two species is such that selection will favour those members of each species least like the other. (Correlated characters would also be expected to show some degree of displacement.) To maximize the likelihood of this being the case most studies of character displacement have monitored the size or shape of feeding apparatus (such as beak dimensions in birds); but the exact relationship between character-variation and the obtaining of resources has rarely been determined in studies of character displacement, a notable exception being the study of Fenchel(1975a, b), described in Section V. The conclusiveness of a particular study of character displacement will depend on the degree to which the above four criteria are satisfied for the populations studied. Individual case studies will be discussed in Section V.A. Also, it should be noted that while the preceding discussion was couched in terms of character displacement, much of what has been said is relevant also to studies of character convergence and character release.

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

149

B. Criteria for Conclusive Demonstration of the Evolution of Interspecific Competitive Ability in Experimental Populations The results of competition experiments are often presented as graphs of the species-frequency (i.e. the numbers of one species as a fraction of the total numbers) against time. The species-frequency trajectories sometimes show a steady change towards an equilibrium, whether trivial or non-trivial: see Arthur (1980a) for examples of the former. However, on other occasions (for example, Ayala, 1966) one or more cages show a more or less sudden change in the direction of the trajectory at some stage during the experiment. One interpretation of this occurrence is that one of the competing populations has evolved an increased interspecific competitive ability. In fact, there are at least three possible explanations for this sort of observation, which are described in Sections 1, 2 and 3 below. An outline of an experiment to distinguish between the different explanations is given in Section 3.

1. Changes in Environmental Conditions It is clear from the work of Park (1948, 1954) and others that the relative competitive abilities of two species can be markedly altered by environmental conditions such as temperature and humidity. It is equally clear that such variables can only be controlled within certain limits in a typical laboratory incubator or culture-room. It is common, in experiments with Drosophila for example, to keep the temperature at 25 & 1°C. However, even a 2°C shift in temperature can have a dramatic effect on the outcome of interspecific competition (see Ayala, 1971).It is therefore highly desirable that continuous records of temperature and indeed of as many other variables as possible be kept throughout all experiments. Screening for parasites is also desirable since parasitic infection can cause a change in relative competitive abilities. An example of this is given by Park (1948) for infection of Tribolium cultures with the parasite Adelina.

2. In traspecijic Competitive Selection If many environmental variables have been monitored, and none exhibit any marked change when a reversal of competitive superiority occurs, then it is likely that one of the species has evolved an increased interspecific competitive ability. However, such an evolutionary change need not have arisen through selection resulting from interspecific competition. It may, rather, have occurred as an evolutionary response to extremely high density-in which case it might also have occurred in single-species culture. In other words, though the effects of the selection may include increased interspecific

I50

WALLACE ARTHUR

competitive ability, the cause of the selection need not have been interspecific competition. It may be, of course, that a particular investigator is only concerned to show that an evolutionary change has occurred, in which case it is not necessary to distinguish this explanation from the next one (3). However, if a distinction between these two is required, as indeed it is in the context of this review, then it should be possible to contrast the effects of single- and mixed-species cultures as described in the next section.

3. Interspecijic Competitive Selection The proposal that a change in competitive ability is a direct result of selection originating from interspecific competition can be tested as follows. A sample of the population, in which a change in competitive ability has been observed, along with a sample from its parent population which has not undergone interspecific competition, and a third sample which has undergone intense intraspecific competition, should be transferred to new containers and cultured in standardized conditions. Their offspring should then be allowed to compete for one generation with a standard stock of species 2. This sort of test of course needs to be replicated many times, as single-generation experiments on competition are subject to considerable heterogeneity between replicates. If the CPR-values (or equivalent) measuring the competitive ability of the stock which had previously undergone interspecific competition are significantly higher than those for the other stocks of the same species, then it is clear that selection stemming from interspecific competition has modified the competitive ability. It is still desirable to have continuous recordings of environmental conditions, though, so that it can be seen whether the evolutionary change is likely to have been wholly, or only partially responsible for the observed alteration in competitive ability.

V. THE EVIDENCE A. Changes in the Mean of Quantitative Characters The majority of case-studies on the evolutionary consequences of interspecific competition fall into this category, including purported cases of character displacement, character convergence and the evolution of competitive ability. The inclusion of the last of these three categories in this section is somewhat arbitrary though, since the underlying character may have changed in mean and/or variance. It is important to stress that competitive ability, as measured by change in species-frequency or preferably, the CPR or some equivalent, is a result, and what is causing this result usually remains obscure. An increase

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

15 1

in the mean efficiency of resource-conversion could cause an increase in competitive ability, but so also could an increase in the variance of resources utilized.

I . Character Displacement Since the concept of character displacement was put forward by Brown and Wilson (1956), a large number of surveys has been conducted on field populations in an attempt to obtain evidence for displacement in sympatry. These studies have dealt with a wide range of taxonomic groups, and have usually taken the form of a comparison of a morphological character in allopatric and sympatric samples of two closely-related species. The earlier studies have been critically reviewed by Grant (1972), and there is thus little point in discussing them in detail here. Grant’s conclusion, with which I fully agree, was that “the evidence for the ecological aspect (i.e. competitive as opposed to reproductive) of morphological character displacement is weak”. Thus after a brief consideration of two of the case-studies covered by Grant, on which there have been developments since 1972, I will move on to the more recent evidence for character displacement. (a) Sitta neumayer and Sitta tephronota These two species of rock nuthatch provide what has become known as the classical case of character displacement (see Grant, 1975). This case stemmed originally from studies by Vaurie (1951), was used by Brown and Wilson (1956) to provide an example ofcharacter displacement, and was subsequently reviewed (Grant, 1972) and exhaustively re-analysed (Grant, 1975) by Grant. Two main areas of uncertainty in this study, which are of general relevance, have been partially clarified by Grant (1972, 1975). Firstly, to what extent would character-values in sympatry have been predicted from the pattern of variation in allopatry? Grant has shown that for the characters most likely to be directly related to competition for food-beak dimensions-clinal variation in allopatry “predicts” the variation in sympatry in S. tephronota. (The data on variation of S. neumayer in allopatry were insufficient to perform a similar analysis.) Thus there is no necessity to invoke competitive character displacement in beak-size. Secondly, to what extent is variation in individual characters simply a result of changes in body-size, and the correlation of these characters with size? Grant (1975) did find some evidence for sympatric displacement in eye-stripes, which relate to mate-recognition, but argued that this was partially a result of variation in body-size-though the data on the latter were too limited to warrant a firm conclusion. Thus although there is some evidence for displacement in a reproductive character in Sitta, there is no clear evidence for competitive character displacement. In addition, there was only one transect from allopatry to sympatry; heritability estimates for

152

WALLACE ARTHUR

the relevant characters were not made; and there was no firm evidence of competition. Thus none of points 1 to 4 (see Section 1V.A) are fully satisfied by this study. ( b ) Geospiza fortis and Geospiza fuliginosa Among the many evolutionary inferences that have been drawn from data on Darwin’s finches (see Lack, 1947) is that of character displacement in beak-depth between the medium and small ground-finch. These two species are found together on most of the Galapagos Islands. However, each is found allopatrically on small islets. On Daphne, where the larger species G . fortis occurs alone, its beak-depth is considerably smaller (and thus closer to values of the same character in G.fuliginosa) than the beak-depth of the G . fortis individuals coexisting with G.fuliginosa. Similarly, when G .fuliginosa is found alone (on the Crossman islets), its beak-depth is considerably larger than when this species is found sympatrically with G .fortis. Data on beak-depths in these two species are shown in Fig. 2. The interpretation of these data made by Lack (1947) was, although he did not use the phrase, character displacement. Both Lack (1947) and Grant (1972) have pointed out that migration was probably from the larger to the smaller islands and thus the allopatric populations on Daphne and Crossman are probably derived from sympatric populations on the main islands. This led Grant (1972), because of his definition of character displacement, to exclude Geospiza as an example of it. However, under the definition adopted here, the time-sequence of allopatry and sympatry does not occupy a central role, and so the Geospiza example cannot be excluded as an example of character displacement for this reason. It is clear from Fig. 2 that the allopatric/sympatric difference in beak-depth is very marked in both species. While it would clearly be desirable to have measurements on several additional allopatric populations, the number of these is of course strictly limited since the species concerned are entirely restricted to the Galapagos, and because this example concerns island populations, it is not open to the transect approach described in point 2 of Section 1V.A. As regards heritability, estimates have recently been made (Boag and Grant, 1978) for a number of morphological characters in G . fortis (but not G . fuliginosa), and all characters studied showed a high heritability. These included beak-depth (0.82), beak-width (0.95) and beak-length (0.62). The figures given here are those derived from midparent-offspring regression, with other estimating techniques giving slightly higher values for all three characters. It should be stressed, though, that all the above figures relate to variation of G . fortis within Daphne and their relevance to inter-island variation is thus questionable. While bearing this problem in mind, as well as others concerned with the estimation of heritability, it seems likely that the observed variation in beak-depth in Geospiza is largely genetic in origin. The evidence

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

/o '

fortis magnirostris ABINGDON, BINDLOE, JAMES, JERVIS

-

50 /'o

-

30 10

30 10-

fortis

30 -

-

10

fuliginoso

A fortis

CHARLES, CHATHAM

40

-

I o/o

magnirostris

ALBEMARLE ,INDEFATIGABLE

50 o /'

153

Da rw In's mognirostris CHARLES

DAPHNE

20

fuliginosa CROSSMAN I l l r l l l l r l l r l l l l l l l r l l l l l l l l l l l l l l l r

7

8

9 10 11 12 13 14 15 16 17 18 19 20 21 22 23

Fig. 2. Distributions of beak-depth in G. fortis and G. fuliginosa on islands where these species occur together and apart. (Data on G. magnirostris are also given.) From Lack (1947).

for competition is less satisfactory in that it is based largely on observed dietary overlaps (Snodgrass, 1902; Lack, 1947) but if competition for food does occur, then clearly beak-depth is a potentially relevant character. Lack (1947) suggests, though not from quantitative data, that there is a correlation between the size of food eaten and the size of the beak in Galapagos groundfinches. Abbott et al. (1977) have shown that in the genus Geospiza in general, the overlap in diet between two sympatric species decreases markedly as the ratio of beak-depth in the larger to beak-depth in the smaller species increases. Relating the Geospiza study, then, to the discussion of Section IV, it can be seen that criteria 1 and 3 are largely satisfied, while 2 and 4 are not.

154

WALLACE ARTHUR

(c) Typhlosaurus gariepensis and Typhlosaurus lineatus A case of possible competitive character displacement in these two species of legless subterranean lizards has been reported by Huey and Pianka (1974; see also Huey et al., 1974). This investigation was one of unilateral displacement as there were insufficient allopatric sites of T. gariepensis to examine whether or not this species reacted to the presence of the larger species, T. lineatus. An allopatric/sympatric comparison was possible for the latter species, with eight sympatric samples and a much larger number of allopatric ones. Several morphological characters were measured including snout-ventlength (SVL) and the length and width of the head. In these three characters, individuals of T. lineatus showed significantly higher values in samples sympatric with T. gariepensis than in allopatric samples. Huey and Pianka (1974) state that, for SVL, the shift from allopatric to sympatric values is “step-wise”. However, the pattern of variation in allopatry is not presented clearly and there is considerable lumping of data from geographically separate samples in order to calculate means, which is clearly unsatisfactory. Also, while the variation in males is fairly sharp, at the allopatry/sympatry border, that in females is much less so. Little is known of the heritability of morphological characters in Typhlosaurus, and non-genetic variation in size thus remains a possibility (see Lister and McMurtie, 1976). However, there is some information on the possible relevance of size-variation to competition for food: the larger, sympatric T . lineatus eat significantly larger prey (P < 0.001) than the smaller, allopatric individuals (Huey and Pianka, 1974). In this example, it is apparent that points 1 and 4 are to some extent satisfied, whilst 2 and 3 are not. ( d ) Phacops iowensis and Phacops rana Several purported cases of character displacement in fossils have been discussed by Eldredge (1974) who cites these two species of benthic trilobites as presenting “perhaps the most compelling case of character displacement in the paleontological literature”. Yet this must be a comment on the general difficulties of working with fossils rather than the completeness of this example. Only one sympatric sample was available, and as Eldredge himself points out, only one individual of P. iowensis within this single sample was measurable. Thus while P. iowensis is seen to diverge morphologically from P . rana in sympatry, this “divergence” cannot be taken very seriously, as only one trilobite specimen is “diverging”. More data are available for P . rana, but the results are far from simple: in one character this species diverges from P . iowensis, in others it converges towards the later species, and in still others there is no marked convergence or divergence. This example does not-apart from some circumstantial evidence of competition-satisfy any of the criteria put forward in Section IV.A, and no firm conclusion

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

155

as to whether or not character displacement has occurred in Phacops is possible. (e) Eucyrtidium calvertense and Eucyrtidium matuyamai Another case in which morphological variation in closely-related fossil species -this time two radiolarians-is ascribed to character displacement, is presented by Kellogg (1975). The older species, E. calvertense, is thought to have given rise, possibly by evolutionary divergence of a peripheral population, to the more recent E. matuyamai, which subsequently re-contacted its ancestral species in a phase of “neosympatry” which persisted for about one million years. During this period, the larger species (E. matuyamai) increased greatly in size and E. calvertense became smaller. The character measured was the width, in microns, of the fourth segment. There are, however, several problems in attributing this divergence in size to character displacement. Firstly, since E. calvertense pre-dated and post-dated its congener in the area where the populations were for a time sympatric, only unilateral character displacement of E. calvertense from E. matuyamai can be investigated. Secondly, although the sympatric period saw a steepening of the reduction in size of E. calvertense, this was not sufficiently abrupt to make it clear that the presence of E. matuyamai was responsible. Added to these difficulties is the impossibility of making heritability estimates, though it might be argued that the particular pattern of variation described by Kellogg is unlikely to be of a non-genetic nature. A point noted by both Eldredge (1974) and Kellogg (1975) is that, despite other problems, fossil studies can at least answer the question of whether allopatry preceded sympatry in a particular region. This question must often go unanswered in studies of contemporary species. (f) Hydrobia ulvae and Hydrobia ventrosa The most detailed case of character displacement is provided by Fenchel’s (1975a, b) study of populations of mud-snails from Northern Jutland. The main study-area comprised 57 sampling sites; in all, about 130oO animals were collected; the lengths of approximately 100 snails were measured, to the nearest 0.25 mm, in each population. In addition to H. ulvae and H. ventrosa, two further species of mud-snail were collected: H . neglecta and Potamopyrgusjenkinsi. However, the latter was not considered to be in strong competition with any of the Hydrobia species, while the data for H. neglecta were patchy and, according to Fenchel, difficult to interpret. The data on H. ulvae and H. ventrosa showed consistent divergence between these two species in sympatry: see Fig. 3. Histograms illustrating the variation within typical allopatric and sympatric samples are shown in Fig. 4. The numbers in both of these figures refer to sampling sites. It can be seen from Fig. 3 that the variations between samples within sympatry and within allopatry

156

WALLACE A R T H U R

‘1

7

6

12 23A

5758636965 23 2

9

10

10A

1

19

3766 7 0 A 7OE

U

lU IF Y

GW 700

GI

‘I 1

Fig. 3. Average lengths of H . uluae (open circles) and H . ventrow (closed circles) from localities where the two species coexist (a) and where they occur alone (b). Vertical bars indicate one standard deviation. From Fenchel (1975b).

is slight, for both species, compared with the clear difference between allopatric and sympatric samples of each. Furthermore, sympatric samples from different localities show similar divergences. Having established that H. ulvae and H . ventrosa did indeed exhibit consistent sympatric divergence, Fenchel (1975b) proceeded to determine what effect shell-size had on the size of particles ingested. (These snails ingest particles of substrate and assimilate attached micro-organisms and detritus.) A positive association was found between the mean diameter of ingested particles and the shell-size (see Fig. 5); though for any particular size of shell, Potarnopyrgus snails ingested larger particles than did Hydrobia. Considering the ingestion-patterns of typical allopatric and sympatric samples of H . ulvae and H . ventrosa, then, it can be seen (Fig. 6) that divergence in size leads to

"i

6

20

H venfrosa

I0

0

L

H ulwe

10

0

2

3

5

4

6mm

010 I

43

i

4

i

4

imm

Fig. 4. Length-frequency distributions of the shells of H . uluae and H. uentrosa from a locality where they coexist (above) and from two localities where they occur allopatrically (below). From Fenchel (1975b).

I

I

2

3

I

I

I 1 1 1 1

4 5 678910 Shell length (mm)

Fig. 5. Relationship between size of shell and size of food particles in Hydrobia and Potamopyrgus. From Fenchel(1975b).

158

WALLACE ARTHUR 6

O/O

40 60

-

20

-

-

060

-

40

-

2

-

20 -

-

0 40

43

-

-

20

4

8 16 32 64lhBi56k12 Diameter ( p m )

Fig. 6. Distributions of the size of food-particles (expressed as volume %) for populations of H . uluae (open circles) and H . uentrosa (closed circles) from sympatric (top) and allopatric localities. From Fenchel (1975b).

divergence in the size of particles ingested, in other words, partial partitioning of resources. When this case-study is considered in relation to the criteria put forward in Section IV.A, it can be seen that points 1, 2 and 4 are reasonably well satisfied. The divergence on moving into sympatry is sharp and would not be predicted from a knowledge of the variation between samples within allopatry; many geographically separate comparisons show similar divergence; there is some circumstantial evidence for competition in Hydrobia (Fenchel, 1975a); and the importance of shell-size to the selection of foodparticles has been experimentally demonstrated. The only serious gap in the evidence provided by this study is the lack of information on the heritability of the observed differences in size. It is particularly important that this information should be obtained, not only because the rest of the data are so clear, but also because coexistence has an effect on the timing of reproduction (Fenchel, 1975b),and hence on the age-distribution of the population,

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

159

which will no doubt affect the distribution of shell-size. The effect of coexistence on age-distribution varies from place to place but in general there appears to be a shortening of the reproductive period in sympatric areas. Thus point 3 is not yet satisfied for this case-study, but despite this Hydrobia provides probably the clearest evidence yet obtained for character displacement. (9)Raja erinacea and Raja ocellata A study of several morphological characters in these two species of skates has been carried out by McEachran and Martin (1977). In one area, the Gulf of St Lawrence, R. ocellata occurs allopatrically, while other populations of this species are sympatric with R. erinacea. The possibility of unilateral displacement (of R. ocellata) was investigated here. While some characters were very similar in allopatric and sympatric samples of R. ocellata, one showed significant divergence in sympatry and one significant convergence. The former character was the number of toothrows in the upper jaw, and the latter was the number of pre-caudal vertebrae. There was also considerable sympatric divergence in total body-length. However, only three samples were measured in all-one of R. erinacea and two (one allopatric plus one sympatric) of R. ocellata. No data on heritability for any of the characters studied are given by the authors. Some information on feeding habits is given, but evidence for competition is lacking. Thus none of criteria 1 to 4 are fully satisfied in this study, and it is difficult to draw any firm conclusion. (h) Poecilozonites circumjirrnatus and Poecilozonites discrepans Schindel and Gould (1977) measured five morphological characters in these fossil landsnails, and derived two further characters (ratios relating to shellshape). They then considered the overall (multivariate) pattern of variation between habitats, which were determined by the substrate from which the fossils were removed, and between allopatry and sympatry. The effect of a congener was found to be greater than the effect of habitat, and was in such a direction that the species were more different in sympatry than in allopatry. The displacement was greater in P. discrepans than in P. circumjirmatus. The characters contributing most to the overall displacement were spire-height and shell-shape, the latter measured as the ratio of width to height. There is a problem as regards the choice of individuals to measure in Poecilozonites because neither species exhibits a recognizable adult stage (Schindel and Gould, 1977).These authors state that they measured “between ten and thirty of the larger specimens of each species for each locality”. This is obviously less satisfactory than the measurement of a clearly-defined adult group, where such exists. Also, there is the problem of unmeasurable heritability. The allopatric/sympatric difference is repeatable in different places and is not likely to be a result of habitat since, as has already been

160

WALLACE ARTHUR

noted, habitats were separated out in this study and had less effect on morphology than the presence or absence of a congener. Whether the two species competed, and what relation the size and shape of the shells had to any competition remains obscure. Thus criteria 1 and 2 are satisfied while 3 and 4 are not. ( i ) Catostomus discobolus and Catostomus platyrhynchus The study by Dunham et al. (1979) on these two species of freshwater fish (and some other congeners) stands out from most other studies of character displacement in its attempt to dissociate competitive effects on morphological variation from effects due to other environmental factors. Dunham et al. (1979) studied two morphological characters-the number of gill rakers in the anterior row on the first anterior gill arch, and the number of vertebrae. The first of these characters relates to the sieving of food particles to be ingested and so has an obvious potential relation to competition for food; the second character is unlikely to be of direct relevance to competition. A stepwise multiple regression technique was used to separate the effects of a number of environmental factors on the two dependent variables. These environmental factors were elevation, mean and minimum water discharge rates, latitude, longitude and gradient. In addition, two variables were constructed in an attempt to quantify the degree of interspecific competition. Firstly, as regards competition between C . discobolus and C . platyrhynchus, the intensity of interspecific competition experienced by each of these was estimated by the species-frequency of the other + 1 for sympatric areas (which were thus on a scale from 1 to 2), with allopatric areas being allocated a value of 0. Secondly, the degree of intersubgeneric competition was estimated as the relative frequency of the alternative subgenus (i.e. alternative to the subgenus Pantosteus in which the above two species are placed) + I , with areas where the alternative subgenus was absent being allocated a value of 0. Multiple regression was then used to calculate the partial correlation coefficients representing the effects of the different environmental variables on the number of gill rakers and number of vertebrae. This analysis showed that both of the competitive indices (and many of the other environmental variables) had significant effects on morphological variation. C . discobolus and C . platyrhynchus showed significant displacement in the numbers of both gill rakers and vertebrae. The species with higher values of these characters ( C . discobolus) showed increases in both with increased intensity of competition from C . platyrhynchus, and the latter species showed significant declines in both morphological variables with increased frequency of C . discobolus. (Competition from the other subgenus also had significant effects on both species.) The main problem with this study, as with Fenchel’s (1975a, b) study of Hydrobia, is the lack of information on heritability, but otherwise it satisfies

EVOLUTIONARY CONSEQUENCESOF INTERSPECIFIC COMPETITION

161

the criteria of Section 1V.A fairly well. One cautionary comment should perhaps be added though-the results of a multiple regression analysis are very sensitive to exactly which independent variables are included in it. In addition to case-studies on particular pairs or groups of related species, many general studies which are of relevance to character displacement have been undertaken. I will not attempt to review these, since many studies are relevant to character displacement in one way or another, but one article in particular deserves mention. Wilson (1975) questioned whether selection would indeed favour smaller individuals of the already-smaller species, and consequently whether a pattern of displacement in sympatry was realistic. His argument was based on a considerable amount of data on the relationship between the size of predators and the size of their prey, which suggested that larger predators might have a greater variance in prey-size as well as a larger mean prey-size. Thus the prey of smaller individuals would be included in the distribution of prey eaten by larger individuals and so there would be what Wilson called a competitive gradient, rather than resource-partitioning. The data from one experiment are shown in Fig. 7. This pattern gives a rather different impression from the patterns of ingestion of particles in relation to size in Hydrobia (Figs 5 and 6) though the difference may be partly due to different presentations of the data. The relative commonness of different relationships between

a

55 45

c

.U 25

-a

5 u 45

55

65

75

85

95

105

Animal length (rnrn)

Fig. 7. Prey size as a function of predator size. Data from an experiment where different stages of the copepod Acartia tonsa were fed with plastic beads. The data points are the maximum and minimum 5% ingested. From Wilson (1975).

162

WALLACE ARTHUR

the size of a consumer and its choice of food clearly needs to be established. In summary, it is by no means clear at this stage whether the lack of conclusive evidence for character displacement means that the process is rare, or that it is simply a difficult phenomenon to demonstrate, or both.

2. Character Convergence The possibility that evolution might favour convergence of competitors in their patterns of resource-utilization was put forward by MacArthur and Levins (1967). However, this suggestion has been criticized by Lawlor and Maynard Smith (1976) on the basis that the evolutionary shift described as a convergence would also have occurred in the absence of the competitor which was converged towards (see Section 1II.B and Fig. 1). Nevertheless, cases exist in which apparent convergence in sympatry has been attributed to natural selection resulting from interspecific competition, and these cases have been reviewed by Grant (1972) and Cody (1973). These two reviewers reached markedly different conclusions: Grant (1972), as we have seen, concluded that the evidence for competitive “character displacement” was weak, and it should be recalled that Grant defined displacement so as to include convergence. Cody (1973) on the other hand considered that the evidence for character displacement and character convergence was strong. Indeed, Cody stated that character displacement was widely accepted “not withstanding recent doubts of the purity of commonly cited examples” (a reference to Grant’s review). However, the validity of a general theory ultimately relies on the purity of the individual examples on which it is based, so gaps in the evidence provided by particular case-studies cannot be so easily dismissed. This point has already been stressed in relation to character displacement. It is even more important to have a watertight case when postulating competitive character convergence, because there are several highly plausible reasons why two species might converge in sympatry. Firstly, if the species hybridize to any appreciable extent they may exhibit sympatric convergence. Secondly, if there is a conventional mimetic relationship (either Batesian or Mullerian-see Sheppard, 1967) then they might be expected to resemble each other more closely in sympatry than in allopatry. Thirdly, there may be “social mimicry” (Cody, 1973) where increased similarity facilitates gregariousness in mixed-species flocks (but see also Barnard, 1979). Fourthly, there may be other non-competitive selective pressures acting in a convergent manner in sympatry, such as selection for crypsis against a common background. Finally, where behavioural patterns or morphological characters are concerned, non-genetic forces may have considerable influence. As well as there being a variety of possible causes of sympatric convergence, the evidence for competitive convergence is more taxonomically restricted than that for

EVOLUTIONARY CONSEQUENCESOF INTERSPECIFICCOMPETITION

163

displacement, and stems mostly from studies on birds, though some possible instances in other groups are discussed by Cody (1973). The term character convergence is restricted by Cody (1973) to situations where selection favours similar individuals in two or more species so that interspecific territories may be established. Examples of interspecific territoriality are known, for example in wrens (P. R. Grant, 1966). However, in this particular case there is no evidence for character convergence (Grant, 1972). In other cases, such as the meadowlarks Sturnella magna and S. neglecta, interspecific territoriality has been observed (Lanyon, 1956) and characters associated with display have converged in sympatry (Rohwer, 1973). However, it has not been possible to demonstrate that selection acts through competition and associated interspecific territoriality rather than through some other route, or indeed that the variation observed is a result of selection at all, though the nature of some of the characters (pigmentation patterns) suggest that a non-genetic explanation is unlikely. A case of very marked similarity in floral structure and colour of nine species of hummingbird-pollinated plants has been reported by Brown and KodricBrown (1979). Since the nine species represent seven different families, the similarities are presumably due to convergence; and the nature of the common phenotype suggests that it is an evolutionary response to facilitate pollination by hummingbirds. Cases such as this, while demonstrating very marked evolutionary convergence in several characters, leave open the question of whether the agent giving rise to the selection is limiting, in other words whether the convergence is truly a competitively-induced one. There appears to be no single study where there is consistent convergence in sympatry of a heritable character which is clearly not attributable to any of the non-competitive mechanisms listed earlier. Taking this fact together with criticism (Lawlor and Maynard Smith, 1976)of the theory of competitive convergence, it can be seen that the case for this supposed evolutionary process is very weak.

3. The Evolution of Competitive Ability Included in this section are cases where, usually in experimental populations of insects, it appears that one or both of a pair of competing species has undergone an evolutionary increase in its interspecific competitive ability. Although I will not be concerned here with the evolution of intraspecific competitive ability, the relationship between the genetic basis of this, and of interspecific competitive ability is of considerable interest, as has already been pointed out (see also Levin, 1969a, b, 1971). One of the earliest studies in which an experimental population appeared to evolve an increased interspecific competitive ability was that of Moore (1952a, b) using the sibling species Drosophila melanogaster and D. simulans.

164

WALLACE ARTHUR

Out of 20 cages in which these two species competed (Moore, 1952a) D. simulans fared markedly better in one than in the other 19. Moore (1952b) then took a sample of D . simulans from this cage and allowed it to compete with further stocks of D. melanogaster in new containers. This process was repeated three times giving, eventually, an experiment where the D. melanogaster had not experienced competition with D . simulans previously, but the D. simulans had been in competition with D. melanogaster for 500 days. The results of this experiment are shown in Fig. 8. These results were interpreted as a demonstration that interspecific competition gave rise to selection for increased competitive ability. While this interpretation may well be correct, there are a number of points which have not been noted in relation to Moore’s (1952b)experiment. Firstly, it is not clear to what extent the higher competitive ability of the selected D. simulans was due to selection during the experiment as opposed to genetic differences between the original stocks. Secondly, the results of all experiments are presented as graphs of species-frequency over time, and competitive ability inferred from changes in species-frequency. Yet in some experiments (see Fig. 8) controls and experimentals were started at very different species-frequencies and so the results, as presented, are not directly comparable. Thirdly, it is not clear whether the selection, if it occurred, was caused by high density in general or the presence of a second species in particular. Finally, competition involving the selected stock of D. simulans showed a markedly increased heterogeneity of outcome between different generations compared with competition involving unselected D. simulans (Fig. 8), a phenomenon that remains to be explained. Further studies of changes in competitive ability in Drosophila have been

”

1

0

0.

.

I

I

--*-- Cage 24 Cage 25

--o--

I

I

I

100 200 Time in days

I

I

300

Fig. 8. Results of competition between D. melanogaster and D. simulans. Cages 24 and 25 contain “stock” samples of both species. Cages 26 and 27 contain stock D . melanogaster and “pre-competed” D . simulans. From Moore (1952b).

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

165

conducted by Ayala (1966, 1969), Barker (1973), Futuyma (1970), Hedrick (1972), Hoenigsberg (1968) and Tantawy et al. (1970). Some general comments on the subject have been made by Gill (1974) and Sammeta and Levins (1970). The studies of Hoenigsberg (1968) and Tantawy et al. (1970) were field surveys and it is not clear whether evolutionary changes need be invoked. Futuyma’s (1970) study yielded complex results which, according to the author, required an explanation involving qualitatively different changes in different populations. In Ayala’s (1966) experiments, three populations of D. serrata (competing against different species) increased in frequency after first declining; these effects were interpreted as evolutionary changes in interspecific competitive ability. However, none of the three possible causes of the apparent changes in competitive ability, as discussed in Section IV.B, were excluded, and hence a firm conclusion cannot be drawn. In a later study (Ayala, 1969) D. serrata competed with D. nebulosa and the results of competition in two replicate populations are shown in Fig. 9. Ayala pointed to the increase in the frequency of D. serrata in population I starting around week 22 and devised an experiment to test whether this was a result of evolutionary increase in competitive ability in D. serrata. However, it must be pointed out that D. serrata in population I appeared to fare better, from the start of the experiment, than did their counterparts in population 11. Also, there was considerable heterogeneity in the species-frequency between generations in the earlier period of the experi-

1OOC

0

1

3

I

6

I

9

I

12

I

I

15 18 Weeks

I

21

I

24

I

27

I

30

Fig. 9. Per cent D. serrata in two experimental populations (in competition with D. nebulosa). From Ayala (1969).

166

WALLACE ARTHUR

ment for which an evolutionary explanation seems unlikely; so some degree of caution is necessary in interpreting the later results as a consequence of evolutionary change. Ayala (1969)performed a second experiment to test whether the competitive ability of D. serrata had indeed evolved. F1 offspring of samples of this species from populations I and I1 and from the original stocks were made to compete with a standard stock of D. nebulosa. If the competitive ability of D. serrata had evolved in population I then this should of course be reflected in the results of this second experiment. The results do suggest this (Fig. 10) but they are by no means clear and they are fraught with several problems. The difference in the results between the different treatments (i.e. different origins of D.serrata) differed over time. There was considerable heterogeneity between replicates of the same treatment. In addition, the increase in the average performance of D. serrata from population I was roughly equal to the decrease in the average performance of D. serrata from population 11, as compared

Weeks

Fig. 10. Results of competition between D. serrata and stock D. nebulosa. The D.

serrata originated from population I (solid line), population 11 (dashed line) and a

stock cage (dot/dash line). Each line represents the average of the replicates whose identifying numbers are given. From Ayala (1969).

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

167

to the performance of the original stock (see Fig. 10). Yet it seems very unlikely that a population can show an evolutionary decrease in competitive ability during a competition experiment. The only situation in which interspecific competitive ability might indeed decline during a competition experiment would be where it is negatively correlated with intraspecific competitive ability, and selection resulting from intraspecific competition is stronger than that resulting from interspecific competition (see Levin, 1969b). For these various reasons, the results of Ayala’s (1969) experiment are difficult to interpret in a conclusive manner. Hedrick (1972) has shown a clear case of a population of D. melanogaster that had a much higher competitive ability than other populations with ultimately the same origin. The contrast was very marked, though it was present from the start of the competition experiment in which it was observed, and so it would appear not to be a result of selection through interspecific competition (at least in the laboratory) even though the resultant stock is of considerably increased competitive ability. A somewhat complex series of experiments was conducted by Barker (1973) in an attempt to determine whether D. melanogaster and/or D. simulans evolved in relation to interspecific competition. However, the interpretation of the results is impeded due to a number of interruptions of the standardized experimental conditions. In generation 10, the entire experiment was shipped from America to Australia and slightly different medium and containers were employed subsequently. At generation 14 the heating systems failed and “developmental rate was markedly reduced. From generation 55 a different grade of agar was used. Further, although Barker tested for evolutionary change in both species, the stock of D. melanogaster used was a yellow, white strain which had been kept in the laboratory for an unspecified length of time in vials. Thus it is likely that its genetic variation would have been severely depleted prior to its involvement in the competition experiments. The lack of evidence for evolution of competitive ability in this stock is thus hardly surprising. In three of the four D. simulans populations which were subjected to competition with D. melanogaster there was also no evidence for evolution of competitive ability. In the remaining population there was what Barker (1973) calls “presumptive evidence” for selection leading to ecological divergence but there is little basis for this statement in the data. Although much work was clearly put into this experiment, no clear conclusion on the evolutionary effects of competition can be drawn from it. The role of genetic factors in competition between the flour beetles Tribolium castaneum and T. confusum has received considerable attention since Park’s (1948, 1954) classic experiments on these species. It was shown at an early stage that different strains differed in competitive ability (Lerner and

168

WALLACE ARTHUR

Ho, 1961), a fact well known also in Drosophila. Park et al. (1964) showed that different strains of T . castaneum differed more in competitive ability than those of T. confusum. However, Park and Lloyd (1955) considered that natural selection resulting from competition played little part in determining the (dynamic) outcome of competition. This suggestion was supported by negative results of an experiment by Dawson (1973). Recent work by Dawson (1979), however, has demonstrated that evolutionary changes in feeding behaviour can occur in T . castaneum, apparently as a result of exposure to T . confusum. The situation is complex in that T. confusum and T . castaneum compete by eating each other’s eggs, as well as their own. Dawson (1979) showed that the progeny of T. castaneum originating from cultures differing in the relative proportions of T. castaneum and T . confusum differed in their species-preference of eggs eaten in a choice experiment, despite their having had no contact with the cultures from which their parents came. In other words, an inherited preference appears to have evolved. If this result can be confirmed as a general one, it has important implications for the theories of apostatic selection (Clarke, 1962) and predator-switching (Murdoch, 1969) as well as being of relevance to competition. The genetics and evolution of competitive ability in plants has been the subject ofconsiderable study, for example Sakai (1955,1961),Sakai and Gotoh (1955), Turkington (1975) and review by Harper (1977; Chapter 24). Much of this work has centred on intraspecific competitive ability, but some of the results deserve mention nevertheless. In particular, Sakai’s (1961) study led him to the conclusions that intraspecific competitive ability, although it included a genetic component, was of low heritability and was usually unassociated with gross morphological characteristics. The lack of clear evidence for character displacement or rapid evolution of interspecific competitive ability in animals suggests that Sakai’s conclusions may not be restricted to within-species competition or to plants. One study of a plant population which was directly relevant to evolution in mixed-species assemblages was that of Turkington (1975). In this study, samples of the clover species Trifolium repens were removed from vegetation patches dominated by one of four species of grass-Lolium perenne, Agrostis tenuis, Holcus lanatus and Cynosurus cristatus. The clover samples were then cloned and the cloning-products used in an experiment to test their relative performances when each was grown in combination with each of the four species of grass. With one exception, the clover population which had originated from a patch dominated by a particular species of grass fared better against that species than did other populations of clover. A field experiment carried out by Hairston (1980), using two species of salamander, Plethodon jordani and Plethodon glutinosus, has yielded results which are difficult to interpret. Two sites were studied-one in the Great

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFICCOMPETITION

169

Smoky Mountains where the two species show altitudinal segregation with a narrow overlap zone; the other in the Balsam Mountains where the zone of overlap is much wider. Both study-sites were within the zones of overlap. Each site was divided into plots, some of which remained unaltered as controls, the other, experimental, plots having their resident P . jordani replaced with those from the alternative site. If the different widths of overlap zone in the two mountain ranges are a result of evolutionary differences in competitive abilities or patterns of resource utilization between the two areas, then the population sizes of P. glutinosus in the control plots and experimental plots should differ, and moreover the directions of the experimental/control difference should be opposite when the two sorts of transplant are compared. However, while the P. glutinosus in the Smokies showed a significant increase in population size after replacement of the congeners, the P. gfurinosus populations in the Balsams showed no detectable difference between experimentals and controls. Unfortunately Hairston (1980) lumped his data from different plots and presented only mean population sizes. Thus it is not possible to assess the situation further by examining the fate of the populations in individual plots. It seems likely from the various experiments described above that it is sometimes possible for the competitive ability of a population to increase through selection resulting from the competitive process itself-though there are pitfalls in attempting to demonstrate this and few cases of putative evolution of competitive ability can be regarded as conclusive. Two further questions may be asked of those situations in which competitive ability does evolve: (1) Is the rate of such evolution (in either species) dependent on the speciesfrequency? (2) What effect does the evolutionary change have on the dynamics of the mixed-species population? Pimentel et al. (1965) put forward a hypothesis, relating to these questions, known as “genetic feedback”, and proceeded to test it using experimental populations of the housefly, Musca domestica and the blowfly, Phaenicia sericata. I will first outline their general hypothesis, and then review their experimental results in some detail. Pimentel et al. (1965) proposed that: (1) During an experiment in which two species are made to compete, the species that is rarer, at any particular time, will be undergoing more intense selection for improvement of its interspecific competitive ability than the commoner species. (2) The competitive ability of the rarer species will thus increase more quickly than that of its competitor, and will eventually surpass it. (3) The result of this will be a “reversal” in the population dynamics, with the species which was initially rare becoming more common.

170

WALLACE ARTHUR

(4) The differential in selective pressures is now reversed and thus, eventually, the competitive abilities return to their original ranking. (5) The oscillations in species-frequency resulting from “genetic feedback” will be damped and the system will converge towards a state of stable coexistence. To test this scheme, several different experiments were devised. In nine cages, houseflies and blowflies competed in simple, one-cell containers. In a single experiment, the two species competed in a more complex, 16-cell cage, the different cells being connected in a 4 x 4 arrangement by a series of plastic tubes. Finally, as a test of the evolution of competitive ability in the 16-cell experiment, 15 more single-cell cages were set up in which experimental blowflies (sampled from the 16-cell cage after 38 weeks of competition) competed with wild-caught houseflies (5 cages); experimental houseflies competed with wild-caught blowflies (5 cages); and experimentally-derived samples of both houseflies and blowflies competed with each other (5 cages). The results of these experiments varied considerably. Some showed fairly straightforward elimination of one species (see Fig. 11). Some showed a single reversal of competitive dominance, followed by extinction of one species (the 16-cell cage: see Fig. 12). Others showed several reversals of dominance (Fig. 13). In all experiments, one species-though not always the same onewas eliminated. The interpretation of these diverse results is far from easy. It is perhaps simplest to start by stating what the results do not show. They certainly do not show damped oscillations leading to an eventual equilibrium in species-

Weeks

Fig. 11. Results of competition between houseflies and blowflies in one of the singlecell cages. (Solid line-housefly; broken line-blowfly). From Pimentel et d.( 1 965).

Weeks

Fig. 12. Results of competition in the 16-cell cage. (Solid line-housefly; broken line -blowfly). From Pimentel et a/. (1965).

Weeks

Fig. 13. Results of competition between houseflies (-) and blowflies (---) in one of the single-cell cages showing more than one reversal of competitive dominance. From Pimentel et al. (1965).

172

WALLACE ARTHUR

frequency. If anything, the oscillations in species-frequency were divergent, and in all cases led to elimination of one species by the other. This was true of the complex 16-cell environment as well as the single containers, and indeed the period of coexistence in some of the latter was longer than in the former (compare Figs 12 and 13). Thus step 5 of the general scheme proposed by Pimentel et al. was rejected, at least in the prevailing experimental conditions. Step 4 of the scheme did not materialize in the 16-cell experiment, since there was only one reversal before extinction of the housefly population; however, a minority of the single-celled cages showed several reversals, which would be compatible with step 4 (but which might equally be produced by other mechanisms-such as variation in uncontrolled environmental factors). The clearest evidence for the operation of steps 1, 2 and 3 of the scheme appears to derive from the very marked reversal of competitive superiority approximately one year after the start of the 16-cell experiment. This is backed up by an apparently increased competitive ability of the blowflies removed from this experiment after 38 weeks (they won 5 / 5 contests with wild houseflies, whereas wild blowflies won in only 3/9 similar contests). However, on closer examination, the method of maintenance of the 16-cell cage reveals an alternative reason for this increase in blowfly competitive ability. Samples of wild-caught blowflies (and houseflies) were added to the cage at irregular intervals during the course of the experiment “to prevent any possible significant loss of genes due to inbreeding”. Of the origin of these flies we are told only that the “housefly and blowfly used were collected in the Ithaca area”. Such additions were made, amongst other times, in weeks 15, 22, 23 and 25 of the experiment. If some of these flies originated from a different panmictic unit than the original experimental flies, then the high competitive ability at week 38 may have been due, not to selection operating within the original population, but to a selective differential between different blowfly populations within the experimental cage-a point the authors themselves mentioned. It is apparent, then, that while some of the experimental results give some support to parts of the general hypothesis put forward, none of the proposed steps are confirmed by all the experiments, and the scheme in its entirety is supported by none. Also, there are some remaining problems in the interpretation of the results. It is not clear, for example, why very short-term fluctuations in the numbers of both species occurred. In addition, the cages contained three resources-an agar-based medium, portions of liver and sugar-lumps; yet the possible role of heterogeneous resources in any evolutionary change of competitive ability was not investigated. No subsequent experiments have conclusively demonstrated the “genetic feedback” model of Pimentel et al. (1965) for any competitive system, nor even clearly shown that selection for increased competitive ability is depen-

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

173

dent on the species-frequency; though a related phenomenon has been described by Dawson (1979) as discussed earlier. Thus these must for the moment remain as intriguing possibilities.

B. Changes in the Variance of Quantitative Characters It has sometimes been proposed that, where a population exists in the absence of interspecific competitors, the members of that population are found in a wider range of habitats, or utilize a greater variety of resources than do other populations (of the same species) which exist alongside competitors. This phenomenon has been given a number of names, and which of these has been used in particular cases has depended partly on the time-sequence of allopatry and sympatry. Where the former is thought to have arisen by migration of one species out of a sympatric area, the phenomenon has been referred to as ecological release (Wilson, 1961) and niche-expansion (for example, Lister, 1976a, b). Where sympatric colonies are thought to follow allopatric ones (temporally), the phenomenon has been referred to as ecological compression, and the idea that compression of habitats, but not resources, occurs in sympatry has been termed the “compression hypothesis” (see MacArthur and Levins, 1967; Schoener et al., 1979). All such changes in the variance of ecological characteristics in a population may be due to within-phenotype and/or between-phenotype effects, as described by Roughgarden (1972). In either case, the change in the variance of the population may be an evolutionary change, or merely an uninherited behavioural response to the absence of competitors. As Schoener el al. (1979) have pointed out, changes in the variance of ecological characters associated with sympatry have often been considered to be non-evolutionary, behavioural processes, though these authors have begun to explore an explicitly evolutionary model. Van Valen (1965) centred his discussion on morphological characters, which are likely to have a higher heritability than behavioural ones, and has proposed an evolutionary hypothesis (sometimes referred to as the “nichevariation hypothesis”). Basically, Van Valen argued that increased intraspecific morphological variation was found in allopatric island populations; and that this was due to an increased between-phenotype component of the niche, with different phenotypes filling slightly different ecological roles. Selander (1966) made a similar proposal, but a more specific one in that the phenotypes thought to adopt different ecological roles were the two sexes. Van Valen (1965) based his argument on bill measurements of six species of birds. Of the six, five showed a greater variability in bill-size on islands than on the mainland, the difference being statistically significant, for at least one sex, in four out of these five. In the sixth species, populations on the

174

WALLACE ARTHUR

Azores were significantly more variable than mainland populations, but populations from the Canaries were less variable-though not significantly so. Thus the evidence from these six species suggests strongly that birds are more morphologically variable on islands than on the mainland. Further studies on morphological variability in birds were undertaken by Soule and Stewart (1970). These authors compared the variability of three species of relatively generalist feeders with three relative specialists, and found no evidence that the former group were consistently more variable than the latter. On the basis of this finding and several other arguments Soule and Stewart rejected Van Valen’s (1965) hypothesis. While the use of a comparison of different species to comment on a hypothesis of intraspecific variation is questionable (Van Valen and Grant, 1970), some of the other points made by Soule and Stewart (1970) reveal some serious difficulties in accepting Van Valen’s interpretation of his data. Their most important criticism is that there are various possible explanations for Van Valen’s (1965) data, none of which has been ruled out as the cause of the increased variance on islands. These possible explanations (in addition to Van Valen’s) are: firstly, immigration to an island from a number of genetically different mainland populations; secondly, directional selection in a new environment temporarily exposing genetic variation already present; and thirdly, sampling from more than one panmictic unit on islands. In addition to these points, it is necessary to stress once again that, although morphological characters usually have higher heritabilities than behavioural ones, it is nevertheless quite possible that the increased variation in bill measurements on islands, as observed by Van Valen, reflects a non-evolutionary response to a reduction in the degree of interspecific competition or to some other feature of the island environment. Further work by Rothstein (l973), which supports Van Valen’s (1965) hypothesis, is subject to the same difficulties. However, Grant et al. (1976) have also provided evidence for Van Valen’s hypothesis from studies of Darwin’s finches, and there is now (Boag and Grant, 1978) evidence that the characters concerned, such as beak dimensions, have high heritabilities (as discussed in Section V.A) which favours an evolutionary explanation. A detailed discussion of the ecology of landbirds on islands, which is relevant to the issue ofcharacter release, has been provided recently by Abbott (1980).

C. Changes in Heterozygosity and Gene-frequency There are both advantages and disadvantages of working with gene-frequency or phenotype-frequency at a single locus (or a group of loci) rather than with the mean or variance of a quantitative character. The main advantage is that,

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

1 75

at least for those polymorphisms whose genetics have been established, there is no problem of unknown heritability-and indeed many cases of polymorphic variation are completely genetic in nature, a situation probably never found with continuous variation. (Note that, with a “new” enzyme polymorphism, where the electromorphs have not yet been analysed genetically, the problem of heritability remains.) The greatest disadvantage is that the link between the variation under study and the mechanism of competition is often more obscure. It is fairly obvious, at least in general terms, that the size and shape of feeding apparatus may affect competition for food. It is much less obvious how (or whether) the frequency of the “fast” allele at a particular enzyme locus will affect competition. It may be, of course, that the locus concerned is one of the polygenes which contribute to the size and shape of the mouthparts: here we approach the general problem of the relationship between enzymic and quantitative variation, a problem which requires further investigation and is beyond the scope of the present article. If it is not clear how a particular locus might affect competitive ability, then of course selection may be acting not on the locus under study, but on a closely-linked locus. This problem has been discussed by Clarke (1975). As yet there have been few studies on the effects of interspecific competition on polymorphisms, and so far they have not been reviewed as a group. I will deal fairly intensively with these, treating experimental studies first and following with a discussion of studies on natural populations.

I . Experimental Populations (a) Drosophila pseudoobscura and Drosophila persirnilis Powell and Wistrand (1978) examined the effect of a competitor (D.persirnilis) on the heterozygosity, with respect to nine polymorphic loci, of D. pseudoobscura. This was part of a more general investigation on the effects of environmental variability on heterozygosity in the latter species. Two types of comparison were made which are of relevance to competitive selection. Firstly, single populations of D. pseudoobscura kept at 25°C on a single medium-type were compared, for heterozygosity, with populations competing against D. persirnilis but under otherwise identical conditions. Secondly, D. pseudoobscura from single and mixed populations, both of which experienced two media and a variable temperature, were compared in the same way. Comparisons, in both of the above cases, were made after 12, 18 and 24 months. (D. persirnilis, the weaker competitor, was continually replenished throughout the experiment.) In the first type of comparison, the presence of D. persirnilis significantly increased the heterozygosity of D. pseudoobscura after 24 months of competition. In the second comparison, however, the competitor had no statisticallydetectable effect on heterozygosity in D. pseudoobscura. These results are

176

WALLACE A R T H U R

difficult to interpret, both in the inconsistency between different comparisons, and in the direction of the competitive effect when it did occur. Powell and Wistrand (1978) argued that D . persimilis might have increased the genetic variability in its congener by adding excreta and other substances to the environment and so making it more complex. However, as the authors point out, it might equally have been predicted that genetic variability would decline in D. pseudoobscura in the mixed population due to some form of resource-partitioning. If D. persimilis did add something to the environment, the unknown substance presumably must have been already present in the second medium-type in the “variable” populations if the lack of competitive selection in the second comparison is to be explained. An alternative explanation could be that competition favours heterozygotes and that there is less competition in heterogeneous environments than in homogeneous ones. Finally, the question of whether and how selection was acting on the particular loci studied remains unanswered, though at least the loci concerned were shown not to be involved in chromosomal inversions. (b) Drosophila melanogaster and Drosophilu simulans A second study of the effects of interspecific competition on polymorphic variation in Drosophila was carried out by Clark (1979). A stock of D. melanoyaster with a somewhat artificial fourth-chromosome polymorphism was produced. The stock was obtained by crossing a homozygous sparkling poliert spap’’ strain with a balanced lethal strain (ciD/1(4)29).The resultant stock contained only heterozygotes and sparkling homozygotes, because of the lethality of 1(4)29 homozygotes. Due to the superior fitness of heterozygotes over sparkling homozygotes, the polymorphism was maintained in all treatments. The question asked was whether competition with D. simulans altered the equilibrium frequency or the rate of attainment of the equilibrium. To answer this question, four replicates of three treatments were set up. In treatment A, D. melanoyaster populations were cultured in the absence of D. simulans; in treatment B, the species-frequency was maintained at 0.67 D. melanoyaster, and in C, at 0.33 D.melanoyaster. Species-frequencies were held constant in B and C by addition, when necessary, of extra D. simulans (the weaker competitor). In fact, all individuals of D. simulans were periodically replaced with new flies to prevent this species from evolving in response to interspecific competition. The differences between treatments A, B and C in the frequency of the fourth-chromosome lethal allele were then observed, and are shown in Fig. 14. It can be seen that populations of D. melanogaster subject to competition from D.simulans reached a significantly different allele-frequency to the single culture, and they appeared to reach that equilibrium more quickly. An additional experiment confirmed that the different results between treatments were not simply due to different densities of D.melanoyaster. There was little

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

1 77

Generation

Fig. 14. Frequencies of the 1(4)29 lethal allele in D. melnnogaster. A-single-species population. B, C-populations mixed with D. simulans. Each curve is based on mean of four replicates. Bars represent f2 standard errors. From Clark (1979).

or no difference between allele-frequencies in treatments B and C, indicating that the intensity of interspecific competition, given that it occurred, had no effect (or at least no detectable effect) on the polymorphism. This study shows rather clearly that interspecific competition can affect a polymorphism, but the relevance of the sort of polymorphism involved to the more subtle forms of variation usually found in natural populations is questionable.

2. Natural Populations There appear to have been only three studies explicitly dealing with the selective effects of interspecific competition on individual polymorphic loci in natural populations. These studies, by Murphy (1976),Arthur (1978,1980~) and Gosling (1980) were all conducted on populations of molluscs, but all reached different conclusions. Murphy (1976) concluded that, in the genus Acmaea, selection produced interspecific divergence in allele-frequency. Arthur (1978, 1980c) concluded that interspecific competition gave rise to selection favouring a particular phenotype, in each of two species of Cepaea, regardless of the gene-frequency in the other. Gosling (1 980) concluded that convergent changes in allele-frequency in sympatry in Cerastoderma were not

178

WALLACE ARTHUR

Alleles

Fig. 15. Cumulative frequency diagrams of Lap alleles of unispecific (-) and coexisting (---) populations of limpets. A, A . pelta; 0, A digitalis; H, A . scabra. a and b, Pigeon Point. c, Pacific Grove. N, number of animals. From Murphy (1976).

due to interspecific competition at all. I will now consider these studies in more detail. (a) Acmaea. Murphy (1976) studied three species of this genus of intertidal limpets, namely A . pelta, A . digitalis and A . scabra. He examined populations from two areas of Californian coastline-Pigeon Point, where all three species were sampled, and Pacific Grove, where only the first two were studied. The locus examined was the Lap locus, coding for leucine aminopeptidase. The results are given in Fig. 15. All three allopatric/sympatric comparisons show apparent unilateral divergence in allele-frequency in sympatric populations.

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFIC COMPETITION

179

However, there are two main problems in interpreting this as competitive selection on allele-frequency. (i) Only one allopatric and one sympatric sample was taken of each species in each area (except for A. digitalis at Pigeon Point which was used to compare with A. pelta and A . scabra separately). Thus there is no information on variation of these species within allopatry or within sympatry. (ii) This study was in fact based on electromorphs, and alleles were “inferred” rather than known. Thus, in common with most studies on morphological characters (see Section V.A), there is uncertainty as to whether the variation observed is genetic. (The possibility of non-genetic “polymorphism” must be kept in mind due to the known occurrence, in many species, of post-translational modification of proteins.) As a result of these problems, it is not possible to draw a firm conclusion from this study of electrophoretic variation in Acmaea. (b) Cepaea. Arthur (1978, 198Oc) studied allopatric and sympatric populations of the helicid landsnails C. nemoralis and C. hortensis from a number of geographically separate areas in Britain and Europe. The locus examined was that determining the presence or absence of bands on the shell. This locus is known to have two alleles, with unbanded being dominant to banded in both species (see Cain and Sheppard (1957)and Murray (1963)).A summary of the results in all areas studied (Arthur, 198Oc) showed that in many though by no means all areas, sympatric populations exhibited a significantly higher frequency of bandeds than allopatric populations. This was true of both species, and in some cases the significance levels were extremely high. The results for the area in which this effect of sympatry was greatest are shown in Fig. 16. It is important to note that although this individual area appears to represent a displacement of C. nemoralis away from C . hortensis in sympatry, other areas showed sympatric convergence. However, although the results were not consistent from place to place in terms of displacement/ convergence, they were consistent in that all areas showing a significant effect of sympatry exhibited a decline in the frequency of unbandeds. Thus the change in frequency in one species was not dependent on the value of the equivalent phenotype-frequency in the other co-existing species. The evolutionary changes in the two species are thus in parallel, as described in Section I1.F. The easiest interpretation of these results is that unbanded snails, of either species, are weaker interspecific competitors than bandeds. Certainly, the variation associated with sympatric areas cannot be nongenetic. Nor could the pattern of variation observed be caused by interspecific hybridization or by any of the non-competitive selective forces known in Cepaea, acting alone (Arthur, 198Oc). However, there are still two important weaknesses in this case-study.

180

WALLACE ARTHUR 100

I

Sympatry

I I I I

II

I I

I

I I I

I I

40

I I

!I I

20

1

0

2

I

4

I I I

6

I 14

Distance(m x 100)

Fig. 16. The change in the frequency of unbandeds (XB') in C. nemoralis (0)on entering an area of sympatry with its congener, C. korrensis. (The frequency of unbandeds in the latter species is designated W.) Bars indicate 957" confidence limits. Distance is measured north from the southernmost sample. From Arthur (1978).

(i) Significant changes in morph-frequency between allopatry and sympatry are not observed in all geographical areas. This might not be expected, since the habitats differ and not all mixed-species colonies need entail interspecific competition. Also, the most marked shift in morph-frequency occurred in the very habitat (dunes) where competition is thought to be most severe in Cepaea (see Oldham, 1929; Boycott, 1934). Nevertheless, the lack of shifts in morph-frequency at allopatry/sympatry borders in some areas does render the interpretation of this case-study more difficult. (ii) Although the hypothesis that unbanded snails of either species are weaker interspecific competitors would explain all the results, it is not yet clear why-i.e. by what physiological or behavioural mechanism-unbandeds should indeed be less able to compete. Until this is established, a combination of other selective agents cannot be ruled out as a possible explanation for the changes in morph-frequency observed. ( c ) Cerastoderma. Gosling (1980) studied variation at the phosphoglucomutase locus (Pgm)in two species of marine cockle, Cerastoderma rdule and C. gluucum, with particular reference to the effect of sympatry on allelefrequencies. Although allopatric samples showed little variation from place to place, there was highly significant convergence in sympatry, this being of a unilateral kind, entirely due to a shift in allele-frequency in C. gluucum.

EVOLUTIONARY CONSEQUENCESOF INTERSPECIFICCOMPETITION

18 1

Gosling (1980) argues that this convergence is the result of selection for common characteristics in a common environment, and two lines of evidence support this assertion. Firstly, the habitat of all the mixed populations and the single C. edule populations was an intertidal one whereas C. glaucum normally occurs allopatrically in stagnant saline pools. Thus the species which shows a change in gene-frequency is the one which encounters a marked change in habitat. Secondly, in one of the “mixed” populations, the two species were in fact separated by a distance of 0.5 km yet the convergence still occurred. It should also be noted that interspecific hybridization is known to be possible between C. edule and C . glaucum (Kingston, 1973) and this is clearly another potential cause of sympatric convergence, although the pattern of electrophoretic variation observed in Gosling’s study indicated that hybridization was not occurring in the populations sampled. In conclusion, there appears to be no need to invoke competitive selection in this particular example.

VI. CONCLUSIONS Several possible evolutionary consequences of competition between species have been proposed, and some of these have been developed in detail by theorists. Many experimental and observational case-studies have now been conducted in which evolutionary aspects of interspecific competition have been examined. Yet in very few instances have such studies been able to conclusively demonstrate that variation observed in a character was a direct consequence of selection resulting from the competitive process. On the present evidence, it seems unlikely that character convergence as a direct result of interspecific competition is a common event, and indeed it is questionable whether truly competitive convergence occurs at all. Also, there is considerable doubt as to whether the elaborate genetic feedback hypothesis is correct. However, despite a number of problems besetting many individual case-studies, there is increasing evidence that, in at least some situations, competition may result in character displacement, or in the evolution of increased competitive ability, in one or both competing species. There is also a reasonable case (though perhaps a less convincing one) for the view that competition reduces genetic variability in morphological characters or, conversely, that the lack of competition acts to increase such variability. However, as regards the relative commonness of character displacement, character release and the evolution of competitive ability, and indeed the extent to which these processes occur separately to each other, almost nothing is known. From the few studies that have been conducted on the evolutionary effects of interspecific competition at the level of the

182

WALLACE ARTHUR

individual locus, there is some evidence that competitive selection does operate at this level. However, again, the relative commonness of different coevolutionary patterns is uncertain. In order that these gaps in evolutionary knowledge be reduced, future studies ought to become more preoccupied with the heritability of characters, more analytic as regards the meaning of competitive ability, and more determined in their attempts to distinguish interspecific competition from other selective agents, than the majority of studies conducted to date.

ACKNOWLEDGEMENTS I would like to thank Paul Greenwood and Gordon Robertson for reading and criticizing the manuscript; and Jan Laverick for doing the typing. I am grateful to the Universities of Newcastle upon Tyne and Durham for the use of their libraries; and to the authors and publishers concerned for their permission to reproduce the Figures shown in the text.

REFERENCES Abbott, I. (1980). Theories dealing with the ecology of landbirds on islands. I n “Advances in Ecological Research”, Vol. 1 1, pp. 329-371. Academic Press, London and New York. Abbott, I., Abbott, L. K. and Grant, P. R. (1977).Comparative ecology of Galapagos ground finches (Geospiza Gould): Evaluation of the importance of floristic diversity and interspecific competition. Ecol. Monogr. 47, 151-184. Arthur, W. (1978).Morph-frequency and coexistence in Cepaea. Heredity 41,335-346. Arthur, W. (1980a). Interspecific competition in Drosophila I. Reversal of competitive superiority due to varying concentration of ethanol. Biol. J . Linn. SOC.13, 109-1 18. Arthur, W. (1980b). Interspecific competition in Drosophila 11. Competitive outcome in some 2-resource environments. Biol. J. Linn. Soc. 13, 119-128. Arthur, W. (1980~).Further associations between morph-frequency and coexistence in Cepaea. Heredity 44,417421. Ayala, F. J. (1966). Reversal of dominance in competing species of Drosophila. Am. Nat. 100, 81-83. Ayala, F. J. (1969). Evolution of fitness IV. Genetic evolution of interspecific competitive ability in Drosophila. Genetics 61, 737-747. Ayala, F. J. (1971). Competition between species: frequency dependence. Science 171, 82C824. Bakker, K. (1961). An analysis of factors which determine success in competition for food among larvae of Drosophila melanogaster. Arch. N e e d Zool. 14, 200-281. Barker, J. S. F. (1973). Natural selection for coexistence or competitive ability in laboratory populations of Drosophila. Egypt. J . Genet. Cytol. 2, 288-315.

EVOLUTIONARY CONSEQUENCESOF INTERSPECIFIC COMPETITION

I 83

Barnard, C. J. (1979). Predation and the evolution of social mimicry in birds. Am. Nat. 113, 613-618. Boag, P. T. and Grant, P. R. (1978). Heritability of external morphology in Darwin’s finches. Nature 274, 793-794. Boycott, A. E. (1934). The habitats of land Mollusca in Britain. J. Ecol. 22, 1-38. Brown, J. H. and Kodric-Brown, A. (1979). Convergence, competition and mimicry in a temperate community of humming bird-pollinated flowers. Ecology 60, 1022-1035. Brown, W. L. and Wilson, E. 0. (1956). Character displacement. Syst. 2001.5, 4964. Bulmer, M. G. (1974). Density-dependent selection and character displacement. Am. Nat. 108, 45-58. Cain, A. J. and Sheppard, P. M. (1957). Some breeding experiments with Cepaea nemoralis (L). J . Genet. 55, 195-199. Clark, A. (1979). The effects of interspecific competition on the dynamics of a polymorphism in an experimental population of D. melanogaster. Genetics 92, 1315-1328. Clarke, B. (1962). Natural selection in mixed populations of two polymorphic snails. Heredity 17, 319-345. Clarke, B. (1966). The evolution of morph-ratio clines. Am. Nat. 100, 389402. Clarke, B. (1972). Density-dependent selection. Am. Nat. 106, 1-13. Clarke, B. (1975). The contribution of ecological genetics to evolutionary theory: detecting the direct effects of natural selection on particular polymorphic loci. Genetics Suppl. 79, 101-113. Clarke, B. (1976). The ecological genetics of host-parasite relationships. I n “Genetic Aspects of Host-Parasite Relationships” (Eds A. E. R. Taylor and R. Muller), pp. 87-103. Symposia of the British Society for Parasitology, Vol. 14. Blackwell, Oxford. Clarke, B. and ODonald, P. (1964). Frequency-dependent selection. Heredity 19, 201-206. Cody, M. L. (1973). Character convergence. Ann. Rev. Ecol. Syst. 4, 189-21 1. Collins, P. M. (1978). Studies on genetic polymorphism in Coelopa frigida. Ph.D. Thesis, University of Nottingham. Cook, L. M. (1965). Inheritance of shell size in the snail Arianta arbustorum. Evolution 19, 8 6 9 4 . Cook, L. M . (1967). The genetics of Cepaea nemoralis. Heredity 22, 397410. Cook, L. M. (1971). “Coefficients of Natural Selection”. Hutchinson, London. Crozier, R. H. (1974). Niche shape and genetic aspects of character displacement. Amer. Zool. 14, 1151-1157. Darwin, C. (1859). “On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life”. John Murray, London, (1st edition). Dawson, P. S. (1973). Evolution in mixed populations of Tribolium. Evolution 26, 357-365. Dawson, P. S. (1979). Evolutionary changes in egg-eating behaviour of flour beetles in mixed-species populations. Evolution 33, 585-594. Dunham, A. E., Smith, G. R.and Taylor, J. N. (1979). Evidence for ecological character displacement in western American catostomid fishes. Evolution 33, 877-896. Eldredge, N. (1974). Character displacement in evolutionary time. Amer. 2001.14, 1083-1097.

184

WALLACE ARTHUR

Falconer, D. S. (1960). “Introduction to Quantitative Genetics”. Oliver and Boyd, Edinburgh and London. Fenchel, T. (1975a). Factors determining the distribution patterns of mud snails (Hydrobiidae). Oecologia 20, 1-17. Fenchel, T. (1975b). Character displacement and coexistence in mud snails (Hydrobiidae). Oecologia 20, 19-32. Fenchel, T. M. and Christiansen, F. B. (1977). Selection and interspecific competition. I n “Measuring Selection in Natural Populations”, pp. 477499. Lecture Notes in Biomathematics, Vol. 19. Springer-Verlag, Berlin. Forbes, G. S. and Crampton, H. E. (1942). The effects of population density upon growth and size in Lymnaea palustris. Biol. Bull. 83, 283-289. Futuyma, D. J. (1970). Variation in genetic response to interspecific competition in laboratory populations of Drosophila. Am. N a t . 104, 239-252. Gill, D. E. (1974). Intrinsic rate of increase, saturation density, and competitive ability. 11. The evolution of competitive ability. Am. N a t . 108, 103-1 16. Gosling, E. (1980). Gene frequency changes and adaptation in marine cockles. Nature 286, 601-602. Grant, P. R. (1966). The coexistence of two wren species of the genus Thryothorus. Wilson Bull. 78, 266278. Grant, P. R. (1972). Convergent and divergent character displacement. Biol. J . Linn. SOC. 4, 39-68. Grant, P. R. (1975). The classical case of character displacement. I n “Evolutionary Biology”, Vol. 8 (Eds T. Dobzhansky, M. K. Hecht and W. C. Steere). Plenum Press, New York and London. Grant, P. R., Grant, B. R., Smith, J. N. M., Abbott, I. J. and Abbott, L. K. (1976). Darwin’s finches: population variation and natural selection. Proc. N a t . Acad. Sci. U.S.A. 73, 257-261. Grant, V. (1966). The selective origin of incompatibility barriers in the plant genus Gilia. Am. N a t . 100, 99-118. Hairston, N. G. (1980). Evolution under interspecific competition: Field experiments on terrestrial salamanders. Evolution 34, 409420. Harper, J. L. (1977). “Population Biology of Plants”. Academic Press, London and New York. Hedrick, P. W. (1972). Factors responsible for a change in interspecific competitive ability in Drosophila. Evolution 26, 513-522. Hoenigsberg, H. F. (1968). An ecological situation which produced a change in the proportion of Drosophila melanogaster to Drosophila simulans. Am. N a t . 102, 389-390. Huey, R. B. and Pianka, E. R. (1974). Ecological character displacement in a lizard. Amer. Zool. 14, 1127-1 136. Huey, R. B., Pianka, E. R., Egan, M. E. and Coons, L. W. (1974). Ecological shifts in sympatry: Kalahari fossorial lizards (Typhlosaurus).Ecology 55, 304-316. Kellogg, D. E. (1975). Character displacement in the Radiolarian genus Eucyrtidium. Evolution 29, 736749. Kingston, P. (1973). Interspecific hybridization in Cardium. Nature 243, 360. Lack, D. (1947). “Darwin’s Finches”. Cambridge University Press, Cambridge. Lanyon, W. E. (1956). Ecological aspects of the sympatric distribution of meadowlarks in the north-central states. Ecology 37, 98-108. Lawlor, R. and Maynard Smith, J. (1976).The coevolution and stability of competing species. Am. N a t . 110, 79-99.

EVOLUTIONARY CONSEQUENCES OF INTERSPECIFICCOMPETITION

1 85

Leon, J. A. (1974). Selection in contexts of interspecific competition. Am. Nat. 108, 739-757. Lerner, I. M. and Ho, F. K. (1961). Genotype and competitive ability of Tribolium species. Am. Nat. 95, 329-343. Levin, B. R. (1969a). A model for selection in systems of species competition. In “Concepts and Models in Biomathematics” (Ed. F. Heinmetz). M. Dekker, New York. Levin, B. R. (1969b). Genetic variability and competitive performance in species of Drosophila. Genetics Suppl. 61, 3 6 3 7 . Levin, B. R. (1971). The operation of selection in situations of interspecific competition. Evolution 25, 249-264. Levin, D. A. (1970). Reinforcement of reproductive isolation: plants versus animals. Am. Nar. 104, 571-581. Lewontin, R. C. (1974). “The Genetic Basis of Evolutionary Change”. Columbia University Press, New York. Lister, B. C. (1976a). The nature of niche expansion in West Indian Anolis lizards I: Ecological consequences of reduced competition. Evolution 30,659-676. Lister, B. C. (1976b). The nature of niche expansion in West Indian Anolis lizards: 11: Evolutionary components. Evolution 30,677-692. Lister, B. C. and McMurtie, R. E. (1976). O n size variation in anoline lizards. Am. Nat. 110, 311-314. MacArthur, R. H. (1972). “Geographical Ecology”. Harper and Row, New York. MacArthur, R. H. and Levins, R. (1964). Competition, habitat selection and character displacement in a patchy environment. Proc. Nat. Acad. Sci. U.S.A. 51, 12071210. MacArthur, R. H. and Levins, R. (1967). The limiting similarity, convergence, and divergence of coexisting species. Am. Nat. 101, 377-385. McEachran, J. D. and Martin, C. 0.(1977). Possible occurrence of character displacement in sympatric skates Raja erinacea and R . ocellata (Pisces: Rejidae). Enu. Biol. Fish. 2, 121-130. Mather, K. and Jinks, J. L. (1977). “Introduction to Biometrical Genetics”. Chapman and Hall, London. Mayr, E. (1963). “Animal Species and Evolution”. Belknap Press of Harvard University, Cambridge, Massachusetts. Moore, J. A. (1952a). Competition between Drosophila melanogaster and Drosophila simulans. I. Population cage experiments. Evolution 6, 407420. Moore, J. A. (1952b). Competition between Drosophila melanogaster and Drosophila simulans 11. The improvement of competitive ability through selection. Proc. Nat. Acad. Sci. U.S.A. 38, 813-817. Muggleton, J. (1979). Non-random mating in wild populations of polymorphic Adalia bipunctata. Heredity 42, 57-65. Muller, C. H. (1970). The role of allelopathy in the evolution of vegetation. In “Biochemical coevolution” (Ed. K. L. Chambers), pp. 13-31. Oregon State University Press, Corvallis, Oregon. Murdoch, W. W. (1969). Switching in general predators: experiments on predator specificity and stability of prey populations. Ecol. Monogr. 39,335-354. Murphy, P. G. (1976). Electrophoretic evidence that selection reduces ecological overlap in marine limpets. Nature 261, 228-230. Murray, J. J. (1963). The inheritance of some characters in Cepaea horrensis and Cepaea nemoralis (Gastropoda). Genetics 48, 605-61 5.

186

WALLACE ARTHUR

Murray, J. J. (1972). “Genetic Diversity and Natural Selection”. Oliver and Boyd, Edinburgh. Odum, E. P. (197 1). “Fundamentals of Ecology”. Saunders, Philadelphia. Oldham, C. (1929). Cepaea hortensis (Muller) and Arianta arbustorum (L.) on blown sand. Proc. Malac. SOC. London 18, 144146. Park, T. (1948). Experimental studies of interspecies competition I. Competition between populations of the flour beetles Tribolium confusum and Tribolium castaneum Herbst. Ecol. Monogr. 18, 265-307. Park, T. (1954). Experimental studies of interspecies competition 11. Temperature, humidity and competition in two species of Tribolium. Physiol. Zool. 27, 177-238. Park, T. and Lloyd, M. (1955). Natural selection and the outcome of competition. Am. Nat. 89, 235-240. Park, T., Leslie, P. H. and Mertz, D. B. (1964). Genetic strains and competition in populations of Tribolium. Physiol. Zool. 37, 97-1 62. Pianka, E. R. (1976). Competition and niche theory. In “Theoretical Ecology” (Ed. R. M. May). Blackwell, Oxford. Pimentel, D., Feinberg, E. H., Wood, P. W. and Hayes, J. T. (1965). Selection, spatial distribution and the coexistence of competing fly species. Am. Nat. 99, 97-109. Powell, J. R. and Wistrand, H. (1978). The effect of heterogeneous environments and a competitor on genetic variation in Drosophila. Am. Nat. 112, 935-947. Rohwer, S. A. (1973). Significance of sympatry to behaviour and evolution of great plains meadowlarks. Evolution 27, 44-57. Rothstein, S. I. (1973). The niche-variation model-is it valid? Am. Nat. 107, 598-620. Roughgarden, J. (1972). Evolution of niche width. Am. Nat. 106, 683-718. Roughgarden, J. (1976). Resource partitioning among competing species-a coevolutionary approach. Theor. Pop. Biol. 9, 388424. Sakai, K.-I. (1955). Competition in plants and its relation to selection. Cold Spring Harbor Symp. Quant. Biol. 20, 137-157. Sakai, K.-I. (1961). Competitive ability in plants: its inheritance and some related problems. Symp. SOC. exp. B i d . 15, 245-263. Sakai, K.-I. and Gotoh, K. (1955). Studies on competition in plants. IV. Competitive ability of FI hybrids in barley. J . Hered. 46, 139-143. Sammeta, K. P. V. and Levins, R. (1970). Genetics and Ecology. Ann. Reo. Gen. 4, 469488. Schindel, D. E. and Gould, S. J. (1977). Biological interaction between fossil species: character displacement in Bermudian land snails. Paleobiology 3, 259-269. Schoener, T. W. (1975). Presence and absence of habitat shift in some widespread lizard species. Ecol. Monogr. 45, 233-258. Schoener, T. W., Huey, R. B. and Pianka, E. R. (1979). A biogeographic extension of the compression hypothesis: competitors in narrow sympatry. Am. Nat. 113, 295-298. Selander, R. K. (1966). Sexual dimorphism and differential niche utilization in birds. Condor 68, 113- 151. Sheppard, P. M. (1967). “Natural Selection and Heredity”, Third edition. Hutchinson, London. Slatkin, M. (1980). Ecological character displacement. Ecology 61, 163-1 77. Slatkin, M. and Maynard Smith, J. (1979). Models of coevolution. Quart. Rev. B i d . 54, 233-263. Snodgrass, R. E. (1902). The relation of the food to the size and shape of the bill in the Galapagos genus Geospiza. Auk 19, 367-381.

EVOLUTIONARY CONSEQUENCESOF INTERSPECIFIC COMPETITION

187

Soule, M. and Stewart, B. R. (1970). The “niche-variation” hypothesis: a test and alternatives. Am. Nat. 104, 85-97. Stewart, F. M. and Levin, B. R. (1973). Partitioning of resources and the outcome of interspecific competition: a model and some general considerations. Am. Nat. 107, 171-198. Tantawy, A. O., Mourad, A. M. and Masry, A. M. (1970). Studies on natural populations of Drosophila. VIII. A note on the directional changes over a long period of time in the structure of Drosophila near Alexandria, Egypt. Am. Nat. 104, 105-109. Turkington, R. A. (1975). Relationships between neighbours among species of permanent grassland (especially Trifolium repens L.) Ph.D. thesis, University of Wales. Van Valen, L. (1965). Morphological variation and width of ecological niche. Am. Nat. 99,377-390. Van Valen, L. and Grant, P. R. (1970). Variation and niche-width re-examined. Am. Nat. 104, 589-590. Vaurie, C. (1951). Adaptive differences between two sympatric species of nuthatches. Proc. Xth Internat. Ornith. Congr., Uppsala, 163-166. Volterra, V. (1926). Variations and fluctuations of the number of individuals in animal species living together. Translation in “Animal Ecology” by R. N. Chapman, McGraw-Hill, New York, 1931, pp. 409-448. Williamson, M. H. (1972). “The Analysis of Biological Populations”. Edward Arnold, London. Williamson, P., Cameron, R. A. D. and Carter, M. A. (1976). Population density affecting adult shell size of the snail Cepaea nemoralis L. Nature 263,496-497. Wilson, D. S . (1975). The adequacy of body size as a niche difference. Am. Nat. 109, 769-784. Wilson, E. 0. (1961). The nature of the taxon cycle in the Melanesian ant fauna. Am. Nat. 95, 169-193. Yeaton, R. I. and Cody, M. L. (1974). Competitive release in island song sparrow populations. Theor. Pop. Biol. 5, 42-58.