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On the Engine of Speciation
J. theor. Biol. (1995) 177, 401–409
On the Engine of Speciation J H. K* Department of Medical Physiology and Biochemistry, University of Stellenbosch, PO Box 19063, Tygerberg 7505, South Africa (Received on 16 December 1994, Accepted in revised form on 14 August 1995)
A major biological problem is how phenotypic clusters, known as species, separated one from the other by prominent phenotypic gaps, are produced. Palaeontological evidence suggests that species remain remarkably stable over long periods of time. When phenotypic change occurs it tends to be abrupt, again producing phenotypic gaps, but now between successive species. A surprisingly simple mechanism might explain both phenomena. Because, by definition, fit traits replace less fit traits, fit traits tend to become common, while maladaptive traits tend to develop low to very low allelomorphic frequencies. Sexual creatures would therefore be expected to prefer mates sporting predominantly common features. This is termed koinophilia. When two polygenic traits initially formed independent, continuously variable, phenotypic clines on a continuous resource gradient, a stochastic computer model of koinophilia invariably caused the de novo evolution of distinct morphospecies separated by prominent phenotypic gaps, involving both traits, under a wide range of selection criteria. Koinophilia reproductively isolated the morphospecies from one another, suggesting that this might be the crucial first step in the development of other barriers to hybridization. The rapidity with which koinophilia canalized the initial continuum of interbreeding phenotypes into reproductively isolated species, and its subsequent defence of those phenotypes against invasion by unusual or unfamiliar phenotypes, might be a paradigm of punctuated equilibrium. 7 1995 Academic Press Limited
climatic changes as glacial cycling (Cronin, 1985). When phenotypic change occurs it tends to be abrupt (in geological terms), again producing phenotypic gaps, but now between successive species, which sometimes co-exist for a time as contemporaries (Gould & Eldredge, 1993; Gould, 1995). While aspects of the vertical component of the problem could conceivably be ascribed to the notorious imperfections of the fossil record (Maynard Smith, 1983; Gould and Eldredge, 1993), the horizontal component is unlikely to be an artifact of fragmentary evidence. Although instances are known of ranges of intermediates between two morphological extremes, which, in the absence of those intermediates, would be classified as separate species, the overwhelming impression is that sexual creatures form tight phenotypic clusters (at least as far as their external appearances are concerned), separated by pronounced morphological and behavioural gaps (Gould, 1982; Maynard Smith, 1983; Bernstein et al.,
Introduction A major biological problem is how the continuous process of evolution produces the morphologically discontinuous groups known as species. Darwin termed it ‘‘the mystery of mysteries’’, which, after more than a century, it still is (Maynard Smith, 1983, 1990; Coyne & Barton, 1988; Coyne, 1992). The problem is: why are there lions, leopards and cheetahs on the African savannah, and not a continuous range of forms? This is, however, only one aspect of what is probably a two-dimensional problem (Bernstein et al., 1985; Hopf, 1990). The ‘‘horizontal’’ dimension refers to the paucity of transitional forms between extant species. The ‘‘vertical’’ dimension concerns the fossil record. Palaeontological morphospecies are often remarkably stable over long periods of geological time, sometimes through such intense * e-mail: jhk1.maties.sun.ac.za. 0022–5193/95/240401+09 $12.00/0
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1985; Glazier, 1987; Coyne & Barton, 1988). Present-day species are, thus, biological realities, and not arbitrary subdivisions of a continuum (Gould, 1982; Maynard Smith, 1989; Diamond, 1992). A species is a group of interbreeding populations that is reproductively isolated from other such groups (Mayr, 1942, 1963; Coyne, 1992; Diamond, 1992). The reproductive isolation is caused by pre- and post-zygotic isolating factors (Ayala, 1982; Maynard Smith, 1989; Coyne, 1992). It is this reproductive isolation, working in conjunction with selection, random extinctions, and genetic drift, that is currently believed to create, and then to expand, the morphological gaps between species living in the same area (Ehrman, 1965; Bernstein et al., 1985; Paterson, 1985; Hopf, 1990; Maynard Smith, 1990; Coyne, 1992; Fialkowski, 1992). Why should such isolating factors arise amongst a phenotypic continuum of individuals with such ubiquitous regularity (Coyne, 1992)? Geographic separation, in one form or another, provides a partial answer (Mayr, 1942, 1963; Ayala, 1982; Maynard Smith, 1989; Coyne, 1992), but it clearly does not encompass the full range of biological experience (Coyne, 1992). In particular, it does not explain why the fossil record seems to indicate that phenotypic divergence is, in geological terms, an apparently discontinuous process. Reproductive isolation, through whatever mechanism (genetic and/or geographic), will almost inevitably cause phenotypic divergence, but this would be expected to increase with time, as it does at the molecular level. At the body surface this appears not to be the case. The external morphology changes abruptly (in geological terms), and is then remarkably resistant to further evolution. Although assemblies of species often share a number of supraspecific characteristics, such as hooves in ungulates, feathers in birds, or two eyes in vertebrates (for which there are very small or non-existent interspecific phenotypic gaps), morphospeciation nevertheless involves the entire external phenotype, meaning that a single drawing frequently suffices to depict the full external appearance of all the adult females, or males, of a species. The evolutionary problem is therefore concerned not merely with the existence of interspecific phenotypic gaps, but, probably more importantly with the overwhelming impression of intraspecific phenotypic uniformity, involving virtually the entire external appearance. Speciation thus appears to canalize, and not merely isolate, the entire external phenotype, despite inevitable variations in the selective pressures on, and the potential for drift of, each of the individual components of that phenotype.
Here I present a surprisingly simple mechanism, never considered before, which might explain why both the horizontal and vertical manifestations of speciation are inevitable, and why they involve most (if not all) of the external phenotype. As, by definition, fit traits replace less fit traits, each (fit trait) tends to become the most common of its set of allelomorphs. By the same token, maladaptive traits tend to develop low to very low allelomorphic frequencies. Sexual creatures would therefore be expected to prefer mates sporting predominantly common features, and to avoid individuals with unusual or unfamiliar attributes. This is termed koinophilia (Koeslag, 1994; Koeslag & Koeslag, 1993, 1994a, b). When two polygenic traits initially formed independent, continuously variable, phenotypic clines on a continuous resource gradient (Fig. 1), a stochastic computer model of koinophilia invariably caused the de novo evolution of distinct morphospecies, separated by prominent phenotypic gaps, involving both traits, under a wide range of selection criteria (Fig. 2). Koinophilia reproductively isolated the morphospecies one from the other, suggesting that this might be the crucial first step in the development, ultimately, of molecular biological, physiological, behavioural, and anatomical barriers to hybridization (Ayala, 1982; Maynard Smith, 1989; Coyne, 1992). The rapidity with which koinophilia canalized the initial continuum of interbreeding phenotypes into reproductively isolated species, and its subsequent defence of those phenotypes against invasion by unusual or unfamiliar phenotypes (Koeslag & Koeslag, 1994a), might be a paradigm of punctuated equilibrium (Gould & Eldredge, 1993;
F. 1. The phenotypic values of the two polygenic traits of the 750 individuals forming a typical generation 0. Individuals are living on a continuous, linear, environmental gradient comprising 1000 niches. Each individual’s phenotypic features are ideally suited to the niche occupied by that individual (i.e. each individual’s fitness=1.0). The 750 individuals are randomly scattered on the environmental gradient. The environment appears fuller than it really is (75% occupancy) because the bars representing the individual phenotypic values overlap. Gaps less than four niches wide are, therefore, invisible.
F. 2. The phenotypic values of the two polygenic traits in each of the 750 individuals who made up generation 30 of a randomly chosen experimental (koinophilia) and control (panmixis) run under default conditions. The koinophilic individuals are clustered into groups with minimal phenotypic clines for either trait. The phenotypic gaps between groups ensured that the probability of a hybrid mating (should members of the two adjacent groups meet) was generally P=0.0000001.
Gould, 1995), or the ‘‘vertical’’ aspect of the speciation problem.
The Model The model consists of a continuous, linear, environmental gradient compromising 1000 niches (microhabitats which could be occupied by only one individual at a time). The population consists of 750 hermaphrodites with discreet generations. Each individual sports two independent polygenic traits. Each trait was determined by the additive effects of 50 unlinked, haploid, Boolean genes. Total genome size was therefore 100 genes. If the environmental extremes are called the equator and pole respectively, and the two traits are fur length and colour, then the shortest fur length (all off-genes) and maximum colouration (all on-genes) were most adaptive for the equator. The opposite would be most adaptive at the pole. The number of on-genes which made a trait best suited (fitness=1.0) for a given niche was determined by niche location (working from the equator for fur length, and from the pole for colour) divided by 20. Trait fitness decreased by zero (no selection), 0.02 (the default), or 0.2 per phenotypic unit deviation from the
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ideal at a given location. (One phenotypic unit equalled the phenotypic influence of one on-gene. As the phenotypic effect of each on-gene carried the same weight, the maximum possible phenotypic difference between two individuals was 50 units per trait.) The selective pressures on the two traits could differ. The fitnesses of the two traits interacted multiplicatively (Franklin & Lewontin, 1970; Lewontin, 1974; Ewens, 1979). On- and off-genes, in generation 0, were randomly distributed throughout the individual genomes, but in such a manner that the individuals (randomly distributed in the environment) formed two phenotypic clines in opposite directions (Fig. 1). Stochastic effects were produced by the Real Version 1 Minimal Standard random number generator described by Park & Miller (1988). Individuals sought mates from amongst the individuals in their geographic locality. Localities consisted, in the default, of the 250 (occupied and unoccupied) niches surrounding each individual. The individuals occupying any of the 125 niches at an environmental extremity shared a common locality: the rest all had individualized localities, of which they occupied the geographic mid-point. Encounters between potential mates were in direct proportion to fitness. Panmictic individuals mated without further ado, producing one offspring, who, in the next generation, occupied the ‘‘mother’s’’ niche, or the nearest unoccupied site to it. Koinophilic individuals preferred the two modal traits in their respective localities. The modal trait, and those that deviated by fewer than five phenotypic units from the mode, had an attractiveness of 1.0. A phenotypic deviation from the mode of between five and nine units had an attractiveness of 0.8. All other phenotypes had an attractiveness, in the default, of 0.01. The probability of mating between two koinophilic individuals was the product of the four attractivenesses per encounter. Mating in the first two generations was always panmictic. Thereafter it was either koinophilic (experimental) or panmictic (control) for a further 28 generations. Each run (experimental plus a control) was repeated 30 times under a given set of parameter conditions. Analysis The phenotypic values of the two polygenic traits for each of the 750 individuals who made up generation 30 of a randomly chosen experimental (koinophilia) and control (panmixis) run under default conditions are displayed in Fig. 2. To describe the evolution of these patterns, groups or clusters
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were first defined as any geographic concentration of e5 individuals separated by e5 unoccupied sites from the next occupied niche. The within-group phenotypic variance was calculated, treating the groups as if they were samples in an analysis of variance (anova). The results, expressed in the form of standard deviations, are displayed on the graphs (Figs 3–5) as dashed lines, labelled a (y-axis scale×2). Quantification of within-group phenotypic clines and between-group phenotypic gaps was done as follows. Regression analysis was performed on the phenotypic values (versus niche location) of each group. Individuals’ actual phenotypic values were then replaced by those obtained (for the individual’s
niche) from the appropriate regression formula. (These analytical manipulations in no way affected the model proper. Individuals’ real phenotypes were immutable and rigidly determined by strict Mendelian principles.) The phenotypic gap between adjacent groups was considered to be the difference between the phenotypic value (calculated by regression analysis) of the individual closest to the pole of one group and that of the most equatorial individual of the adjacent group. Value b was the sum of the differences between the phenotypic values (calculated by regression analysis) of the first and last individuals of each group. This therefore equalled the total phenotypic cline, minus the between-group phenotypic gaps. Thus, if the population was comprised of
F. 3. The evolution of species from an initial phenotypic gradient of interbreeding individuals. Generation time is on the x-axis. The two independent polygenic traits per individual are shown on the z-axis (as the deviation from the ideal of the coefficients of selection, per phenotypic unit, were the same for both traits, as indicated on the z-axis, the evolution of only one of them is shown for clarity’s sake). The graphs represent the means of 30 independent runs under the same parameter conditions. The dashed line (a) depicts the evolution of the within-group phenotype variance (expressed as a standard deviation) for one of the traits (y-axis scale×2). Lines b and c, depict the evolution of the within-group phenotypic clines (calculated by regression analysis for each group): each point in graph b depicts the sum of the within-group increments in phenotypic value (y-axis scale×20). Points along the heavy solid line, (c), depict the sums of the products of the within-group increment in phenotypic value and habitat size (y-axis scale×10). Line d depicts the same as c, except for the phenotypic gaps between the groups.
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F. 4. The same applies as for Fig. 3, except that the strengths of selection for the two traits differ. The evolution of the trait subject to the default decrement in fitness of 0.02 per phenotypic unit deviation from the ideal (maximum fitness=1.0) for its niche is shown in front (lines a1, b1, c1, and d1). The evolution of the other trait, subject to selective neutrality (top), or a decrease in fitness of 0.2 per phenotypic unit deviation from the ideal (bottom), is shown behind (lines a2, b2, c2, and d2). The scales and symbols are the same as in Fig. 3.
compact groups only, and the phenotypic cline in generation 0 was perfectly preserved, then b=50×0.75=37.5. In the absence of within-group phenotypic clines, b=0, and any phenotypic difference between the individual nearest the equator and the one nearest the pole, would be entirely because of the phenotypic gaps between the groups. Value c was calculated as the sum of the products of the within-group increments in phenotypic values (using the results of the regression analysis) and habitat size. Value d denotes the same as c, but for the phenotypic gaps between the groups. The graphs labelled a, b, c, and d, in Figs 3–5 depict the means of 30 values of the corresponding variable (per generation) obtained from 30 separate runs under a same set of parameter conditions. Standard errors of the mean were calculated; but, because they imparted no information that cannot be derived, by inspection, from the fluctuations (from one generation to the next) in the mean values of a, b, c, and d, they are not displayed on the graphs.
Results The phenotypic values for each individual’s two traits in generation 30, in a randomly chosen experimental and control population under default conditions, are displayed in Fig. 2. The number of
groups, their average morphologies, and their locations varied from run to run, but always gave the same impression: the koinophilic populations always coalesced into well-defined groups, whose withingroup phenotypic variance (per trait), although always greater than zero (see lines a in Figs 3–5), was small compared to the between-group phenotypic variance (Fig. 2). Within-group clines were minimal or absent. A group’s average phenotype in generation 30 was always best suited (i.e. had a fitness of 1.0, or very nearly 1.0) for a niche close to the group’s geographic mid-point. That is to say, if a group occupied niches 250–350, its average phenotype, taking both traits into account, was best suited for niche 300 (2SD 9). (The groups’ geographic positions, and therefore the mid-point niches to which they were best adapted, varied randomly, however, from run to run.) The average magnitude of the phenotypic gaps between adjacent groups was such that the chance of a hybrid mating was generally P=0.00000001. This was largely because of the ‘‘survival of the first’’ (Bernstein et al., 1985; Hopf, 1992), by which it is meant that the phenotype which, by chance, became the first to dominate an area was also the one most likely to replace its regional rivals. Since koinophilic individuals preferred common phenotypes, any locally dominant phenotype always tended to become commoner still. Rarer,
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phenotypically intermediate groupings tended to incur increasing costs of rarity, leading to their extinction, the widening of existing phenotypic gaps and thus the dramatic rise, amongst the koinophilic populations, in the value of d (Figs 3–5) compared to that of the panmictic populations. As there were no penalties associated with phenotypic rarity in the panmictic populations, phenotypic gaps and group formation were more variable, within-group clines often remained striking, and reproductive isolation was nonexistent. When both traits were subject to excessive selection (survival restricted to a 35 niche range per trait) koinophilic groups retained remnant clines and were smaller (and, therefore, more numerous) than otherwise (Fig. 3). Clines vanished altogether when both traits were selectively neutral (i.e. there was no environmental gradient affecting the traits) but, because there were no barriers to migration, species frequently splintered into geographically separated but phenotypically identical populations (accounting for the decline in the average value of d after generation 15). When the two traits were subject to different strengths of selection (Fig. 4), group
cohesion was maintained even if one trait was selectively neutral. There was, then, little phenotypic indication of the difference in the strengths of selection acting on the two traits. Variations in the attractiveness of the least desirable phenotypes from 0.01 (the default) to 0.3 had no discernible effect on the process of speciation (Fig. 5). Discussion The results of the model suggest that koinophilia not only converts phenotypic clines of interbreeding individuals into reproductively isolated morphospecies, but also endows the process with inevitability. If sexual creatures avoid mates with unusual or unfamiliar features then groupings of phenotypically similar individuals are bound to form. This phenotypic canalization, as the present two trait model suggests, affects most of the outward appearance regardless, to a large extent, of how the individual components of that appearance are influenced by natural selection. The model suggests, furthermore, a reason for the hallmark of speciation: the reproductive isolation of the morphospecies (Mayr, 1942;
F. 5. The same applies as for Fig. 3, except that there is only one polygenic trait per individual. All the graphs depict the evolution of morphospecies in koinophilic populations. They differ only with respect to the attractiveness of the least common phenotypes in each individual’s locality. The modal phenotype, and those that deviated by fewer than five phenotypic units from the mode always had an attractiveness of 1.0. Those that deviated by between five and nine phenotypic units from the mode had an attractiveness of 0.8. These graphs show the effects of varying the attractiveness (indicated on each graph) of the individuals who deviated by 10 phenotypic units or more from the mode.
Coyne, 1992). The phenotypic discontinuities produced by our model were almost invariably of such a size that the probability of a hybrid mating was the lowest that the model parameters would allow (excluding natural selection). While panmixis frequently created phenotypic clusters, with accompanying phenotypic gaps, the clusters were never reproductively isolated from one another (unless a geographic gap of q125 niches was formed). Compared with koinophilia, panmixis canalized the phenotype haphazardly (see Fig. 2). Clustering of one or a few phenotypic features can occur through a wide variety of means (Wright, 1931; Lande, 1982; Paterson, 1985; Coyne & Barton, 1988; Maynard Smith, 1989; Coyne, 1992; Fialkowski, 1992). None, however, explains why it is almost universal among sexual creatures, nor why it should canalize virtually the entire outward appearance of both sexes, regardless of the traits’ involvement with sexual dimorphism. Nevertheless, the most convincing explanations for the de novo development of reproductive isolation (with subsequent phenotypic divergence into morphospecies), are provided by models that invoke mate choice as the engine of incipient speciation (Lande, 1981, 1982; Ryan & Rand, 1993). The origin and maintenance of mating preferences present many unresolved theoretical problems (Borgia, 1987; Maynard Smith, 1987; Kirkpatrick & Ryan, 1991; Taylor & Williams, 1982). A sexual creature would clearly be expected to choose the fittest available mate with whom to exchange its DNA (Charlesworth, 1987, 1988; Kirkpatrick & Ryan, 1991; Koeslag & Koeslag, 1993, 1994b). Natural selection, however, tends to exhaust the additive variance in fitness in a population, creating serious difficulties for models of the evolution of mate choice for ‘‘good genes’’ (Charlesworth, 1987, 1988). Furthermore, even when present, differences in heritable fitness can only be observed and measured a posteriori (i.e. after several generations have elapsed). A preference for ‘‘good genes’’, therefore, almost inevitably invites cheating through the elaboration of fake ‘‘good phenotypes’’. Nevertheless, plausible models for the origin of mate preference abound (Maynard Smith, 1987; Kirkpatrick & Ryan, 1991). Hamilton & Zuk (1982) have suggested that male ornaments, which females find attractive, may have evolved because they allow the females to discriminate between males who differ heritably in their parasitic loads, and hence in fitness, when cycles in gene frequencies at loci controlling host susceptibility are maintained by shifting selection. Alternatively, it has been suggested that mate choice may simply be
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driven by economic forces. Females who prefer conspicuous males spend less time searching for mates than females preferring drab (and possibly fitter) mates (Kirkpatrick & Ryan, 1991). A third suggestion for the evolution of mate choice proposes that a male characteristic may become genetically correlated with a female mating preference. The favoured male characteristic and the preference need neither be adaptive (although they could have arisen by either of the previous two mechanisms). Once they exist they tend to re-inforce one another, often leading to a runaway process (Fisher, 1930; Lande, 1981). No matter how it arises, a female mating preference for a quantitative secondary sexual characteristic tends to initiate reproductive isolation and phenotypic canalization of the male sexual ornament (Lande, 1981, 1982). Once groups become reproductively isolated, the rest of the phenotype will diverge (though not necessarily become canalized), causing phenotypic gaps to appear for traits not involved in sexual dimorphism. Furthermore, Bernstein et al. (1985) and Hopf (1990) have shown that a phenotypic continuum of species (i.e. groups that are already reproductively isolated one from the other), distributed along a continuous resource gradient, rapidly coalescese into distinct species. Chance fluctuations in population density will bring about variations in the ease with which individuals can find appropriate mates (especially if each species is initially very rare). The fitness of the larger species will, therefore, be greater than that of the smaller species. Bernstein et al. (1985) term this the cost of rarity, which tends to make large species larger at the expense of smaller species. This has a snowball effect which proceeds with increasing speed as it develops. Eventually only a few, phenotypically very distinct species remain. Paterson (1985) and Fialkowski (1992) propose that hybrid disadvantage promotes assortative mating and the exaggeration of existing phenotypic gaps (Ryan & Rand, 1993). Hybrid disadvantage could therefore complement and reinforce the Bernstein et al. (1985) model. However, neither the Bernstein et al. (1985), the Hopf (1990), the Paterson (1985) or the Fialkowski (1992) proposals explain how the reproductive isolation, on which their models rely, arises in the first place. If it depends for its origin primarily on the evolution of mate preferences (Lande, 1981, 1982), then two problems arise. The first is that the evolutionary imperative for mate preferences has to be very strong, and circumstance-independent, to be able to explain the near universality of speciation among sexual creatures. The second problem concerns arbitrary fashion and fakes. If mate preference is as ancient and widespread as speciation,
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then sexual creatures must inevitably become burdened with a surfeit of traits to which the opposite sex has become arbitrarily attracted, and fake ‘‘good phenotypes’’, all of which are presumably largely maladaptive. The present model is also based on mate choice. Its assumptions are that sexual creatures have senses with which they evaluate potential mates; that they are capable of frequency analysis; and that they exploit these capabilities to avoid mates with unusual or unfamiliar traits which are assumed to be, on average, less fit than their common counterparts (Koeslag, 1994; Koeslag & Koeslag, 1994b). The resulting mate choice is clearly not infallible, but it probably represents a sexual creature’s best bet: the chance that a rare or unusual characteristic is maladaptive is extremely high and it would presumably be evolutionary foolishness not to avoid it. Koinophilia has a major advantage over other forms of mate choice because commonality cannot be faked. Its betting chances are also circumstanceindependent. As it is evolutionarily robust (Koeslag, 1994; Koeslag & Koeslag, 1994a, b), it is likely to be widespread, occurring wherever creatures practice sex. Being fallible, however, groups could cling to random phenotypic errors (having achieved commonality through, for instance, a founder effect). These can only be eliminated, or promoted, by intergroup competition (Koeslag 1994; Koeslag & Koeslag 1994a). In the present simulations, however, no such errors survived 30 generations: the koinophilic groups’ average phenotypes in generation 30 were always best suited for the geographic mid-points of their ranges. If these assumptions are valid and realistic, then koinophilia provides an obvious and simple explanation for many, if not most, of the problems concerning speciation, especially its virtual universality among sexual creatures: its canalization of the entire visible (to conspecifics) phenotype of both sexes apparently regardless of differences in the selective advantages of the individual traits; and the inevitability of reproductive isolation. As koinophilia denies individuals with rare or unusual phenotypes the opportunity to mate, the groups’ phenotype becomes evolutionarily static, resisting change even when 5% of mutations are beneficial (Koeslag & Koeslag, 1994a). Species would, therefore, be expected to persist in more or less unchanged form for long periods of time. Transitional forms produced when groups disintegrate, or when new species bud from the established form, are likely to be evanescent. They are, therefore, as
unlikely to be represented in the fossil record as they are to appear in the catalogues of present day forms.
REFERENCES A, F. J. (1982). Population and Evolutionary Genetics. Menlo Park, California: Benjamin Cummings. B, G. (1987). A critical review of sexual selection models. In: Sexual Selection: Testing the Alternatives (Bradbury, J. W. & Andersson, M. B., eds) pp. 55–66. Chichester: John Wiley & Sons. B, H., B, H. C., H, F. A. & M, R. E. (1985). Sex and the emergence of species. J. theor. Biol. 117, 665–690. C, B. (1987). The heritability of fitness. In: Sexual Selection: Testing the Alternatives (Bradbury, J. W. & Andersson, M. B., eds) pp. 21–40. Chichester: John Wiley & Sons. C, B. (1988). The evolution of mate choice in a fluctuating environment. J. theor. Biol. 130, 191–204. C, J. A. (1992). Genetics and speciation. Nature 355, 511–515. C, J. A. & B, N. H. (1988). What do we know about speciation? Nature 331, 485–486. C, T. M. (1985). Speciation and stasis in marine Ostracoda: climatic modulation of evolution. Science 227, 60–63. D, J. M. (1992). Horrible plant species. Nature 360, 627–628. E, L. (1965). Direct observation of sexual isolation between allopatric and between sympatric strains of the different Drosophila paulistorum races. Evolution 19, 459–464. E, W. (1979). Mathematical Population Genetics. New York: Springer-Verlag. F, K. R. (1992). Sympatric speciation: a simulation model of imperfect assortative mating. J. theor. Biol. 157, 9–30. F, R. A. (1985). The Genetical Theory of Natural Selection. 2nd edn. New York: Dover. F, I. & L, R. C. (1970). Is the gene the unit of selection? Genetics 65, 707–734. G, D. S. (1987). Towards a predictive theory of speciation: the ecology of isolate selection. J. theor. Biol. 126, 323–333. G, S. J. (1982). A quahog is a quahog. In: The Panda’s Thumb. pp. 204–213. New York: Norton. G, S. J. (1995). The evolution of life on earth. Sci. Am. 271, 62–69. G, S. J. & E, N. (1993). Punctuated equilibrium comes of age. Nature 366, 223–227. H, W. D. & Z, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387. H, F. A. (1990). Darwin’s dilemma of transitional; forms: a comparison of a model with data. In: Organizational Constraints on the Dynamics of Evolution. (Maynard Smith, J. & Vida, G., eds) pp. 357–372. Manchester: Manchester University Press. K, M. & R, M. J. (1991). The evolution of mating preferences and the paradox of the lek. Nature 350, 33–38. K, J. H. (1994). Koinophilia replaces random mating in populations subject to mutations with randomly varying fitnesses. J. theor. Biol. 171, 341–345. K, J. H. & K, P. D. (1993). Evolutionarily stable meiotic sex. J. Hered. 84, 369–399. K, J. H. & K, P. D. (1994a). Koinophilia. J. theor. Biol. 167, 55–65. K, P. D. & K, J. H. (1994b). Koinophilia stabilizes bi-gender sexual reproduction against asex in an unchanging environment. J. theor. Biol. 166, 251–260. L, R. (1981). Models of speciation by sexual selection on polygenic traits. Proc. natl. Acad. Sci. 78, 3721–3725. L, R. (1982). Rapid origin of sexual isolation and character divergence in a cline. Evolution 36, 213–223. L, R. C. (1974). The Genetic Basis of Evolutionary Change. New York: Columbia University Press.
M S, J. (1983). The genetics of stasis and punctuation. Ann. Rev. Genet. 17, 11–25. M S, J. (1987) Sexual selection—a classification of models. In: Sexual Selection: Testing the Alternatives (Bradbury, J. W. & Andersson, M. B., eds) pp. 9–20. Chichester: John Wiley & Sons. M S, J. (1989). Evolutionary Genetics. Oxford University Press. M S, J. (1990). Concluding remarks. In: Organizational Constraints on the Dynamics of Evolution. (Maynard Smith, J. & Vida, G., eds) pp. 433–437. Manchester: Manchester University Press. M, E. (1942). Systematics and the Origin of Species. New York: Columbia University Press.
409
M, E. (1963). Animal Species and Evolution. Cambridge: Harvard University Press. P, S. K. & M, K. W. (1988). Random number generators: good ones are hard to find. Communs. Assoc. Comput. Mach. 31, 1192–1201. P, H. E. H. (1985). The recognition concept of species. In: Species and Speciation (Vbra, E. S. ed.) pp. 21–29. Pretoria: Transvaal Museum Monographs No. 4. R, M. J. & R, A. S. (1993). Species recognition and sexual selection as a unitary problem in animal communication. Evolution 47, 647–657. T, P. D. & W, G. C. (1982). The lek paradox is not resolved. Theor. Popul. Biol. 22, 392–409. W, S. (1931). Evolution in Mendelian populations. Genetics 16, 97–159.
On the Engine of Speciation J H. K* Department of Medical Physiology and Biochemistry, University of Stellenbosch, PO Box 19063, Tygerberg 7505, South Africa (Received on 16 December 1994, Accepted in revised form on 14 August 1995)
A major biological problem is how phenotypic clusters, known as species, separated one from the other by prominent phenotypic gaps, are produced. Palaeontological evidence suggests that species remain remarkably stable over long periods of time. When phenotypic change occurs it tends to be abrupt, again producing phenotypic gaps, but now between successive species. A surprisingly simple mechanism might explain both phenomena. Because, by definition, fit traits replace less fit traits, fit traits tend to become common, while maladaptive traits tend to develop low to very low allelomorphic frequencies. Sexual creatures would therefore be expected to prefer mates sporting predominantly common features. This is termed koinophilia. When two polygenic traits initially formed independent, continuously variable, phenotypic clines on a continuous resource gradient, a stochastic computer model of koinophilia invariably caused the de novo evolution of distinct morphospecies separated by prominent phenotypic gaps, involving both traits, under a wide range of selection criteria. Koinophilia reproductively isolated the morphospecies from one another, suggesting that this might be the crucial first step in the development of other barriers to hybridization. The rapidity with which koinophilia canalized the initial continuum of interbreeding phenotypes into reproductively isolated species, and its subsequent defence of those phenotypes against invasion by unusual or unfamiliar phenotypes, might be a paradigm of punctuated equilibrium. 7 1995 Academic Press Limited
climatic changes as glacial cycling (Cronin, 1985). When phenotypic change occurs it tends to be abrupt (in geological terms), again producing phenotypic gaps, but now between successive species, which sometimes co-exist for a time as contemporaries (Gould & Eldredge, 1993; Gould, 1995). While aspects of the vertical component of the problem could conceivably be ascribed to the notorious imperfections of the fossil record (Maynard Smith, 1983; Gould and Eldredge, 1993), the horizontal component is unlikely to be an artifact of fragmentary evidence. Although instances are known of ranges of intermediates between two morphological extremes, which, in the absence of those intermediates, would be classified as separate species, the overwhelming impression is that sexual creatures form tight phenotypic clusters (at least as far as their external appearances are concerned), separated by pronounced morphological and behavioural gaps (Gould, 1982; Maynard Smith, 1983; Bernstein et al.,
Introduction A major biological problem is how the continuous process of evolution produces the morphologically discontinuous groups known as species. Darwin termed it ‘‘the mystery of mysteries’’, which, after more than a century, it still is (Maynard Smith, 1983, 1990; Coyne & Barton, 1988; Coyne, 1992). The problem is: why are there lions, leopards and cheetahs on the African savannah, and not a continuous range of forms? This is, however, only one aspect of what is probably a two-dimensional problem (Bernstein et al., 1985; Hopf, 1990). The ‘‘horizontal’’ dimension refers to the paucity of transitional forms between extant species. The ‘‘vertical’’ dimension concerns the fossil record. Palaeontological morphospecies are often remarkably stable over long periods of geological time, sometimes through such intense * e-mail: jhk1.maties.sun.ac.za. 0022–5193/95/240401+09 $12.00/0
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1985; Glazier, 1987; Coyne & Barton, 1988). Present-day species are, thus, biological realities, and not arbitrary subdivisions of a continuum (Gould, 1982; Maynard Smith, 1989; Diamond, 1992). A species is a group of interbreeding populations that is reproductively isolated from other such groups (Mayr, 1942, 1963; Coyne, 1992; Diamond, 1992). The reproductive isolation is caused by pre- and post-zygotic isolating factors (Ayala, 1982; Maynard Smith, 1989; Coyne, 1992). It is this reproductive isolation, working in conjunction with selection, random extinctions, and genetic drift, that is currently believed to create, and then to expand, the morphological gaps between species living in the same area (Ehrman, 1965; Bernstein et al., 1985; Paterson, 1985; Hopf, 1990; Maynard Smith, 1990; Coyne, 1992; Fialkowski, 1992). Why should such isolating factors arise amongst a phenotypic continuum of individuals with such ubiquitous regularity (Coyne, 1992)? Geographic separation, in one form or another, provides a partial answer (Mayr, 1942, 1963; Ayala, 1982; Maynard Smith, 1989; Coyne, 1992), but it clearly does not encompass the full range of biological experience (Coyne, 1992). In particular, it does not explain why the fossil record seems to indicate that phenotypic divergence is, in geological terms, an apparently discontinuous process. Reproductive isolation, through whatever mechanism (genetic and/or geographic), will almost inevitably cause phenotypic divergence, but this would be expected to increase with time, as it does at the molecular level. At the body surface this appears not to be the case. The external morphology changes abruptly (in geological terms), and is then remarkably resistant to further evolution. Although assemblies of species often share a number of supraspecific characteristics, such as hooves in ungulates, feathers in birds, or two eyes in vertebrates (for which there are very small or non-existent interspecific phenotypic gaps), morphospeciation nevertheless involves the entire external phenotype, meaning that a single drawing frequently suffices to depict the full external appearance of all the adult females, or males, of a species. The evolutionary problem is therefore concerned not merely with the existence of interspecific phenotypic gaps, but, probably more importantly with the overwhelming impression of intraspecific phenotypic uniformity, involving virtually the entire external appearance. Speciation thus appears to canalize, and not merely isolate, the entire external phenotype, despite inevitable variations in the selective pressures on, and the potential for drift of, each of the individual components of that phenotype.
Here I present a surprisingly simple mechanism, never considered before, which might explain why both the horizontal and vertical manifestations of speciation are inevitable, and why they involve most (if not all) of the external phenotype. As, by definition, fit traits replace less fit traits, each (fit trait) tends to become the most common of its set of allelomorphs. By the same token, maladaptive traits tend to develop low to very low allelomorphic frequencies. Sexual creatures would therefore be expected to prefer mates sporting predominantly common features, and to avoid individuals with unusual or unfamiliar attributes. This is termed koinophilia (Koeslag, 1994; Koeslag & Koeslag, 1993, 1994a, b). When two polygenic traits initially formed independent, continuously variable, phenotypic clines on a continuous resource gradient (Fig. 1), a stochastic computer model of koinophilia invariably caused the de novo evolution of distinct morphospecies, separated by prominent phenotypic gaps, involving both traits, under a wide range of selection criteria (Fig. 2). Koinophilia reproductively isolated the morphospecies one from the other, suggesting that this might be the crucial first step in the development, ultimately, of molecular biological, physiological, behavioural, and anatomical barriers to hybridization (Ayala, 1982; Maynard Smith, 1989; Coyne, 1992). The rapidity with which koinophilia canalized the initial continuum of interbreeding phenotypes into reproductively isolated species, and its subsequent defence of those phenotypes against invasion by unusual or unfamiliar phenotypes (Koeslag & Koeslag, 1994a), might be a paradigm of punctuated equilibrium (Gould & Eldredge, 1993;
F. 1. The phenotypic values of the two polygenic traits of the 750 individuals forming a typical generation 0. Individuals are living on a continuous, linear, environmental gradient comprising 1000 niches. Each individual’s phenotypic features are ideally suited to the niche occupied by that individual (i.e. each individual’s fitness=1.0). The 750 individuals are randomly scattered on the environmental gradient. The environment appears fuller than it really is (75% occupancy) because the bars representing the individual phenotypic values overlap. Gaps less than four niches wide are, therefore, invisible.
F. 2. The phenotypic values of the two polygenic traits in each of the 750 individuals who made up generation 30 of a randomly chosen experimental (koinophilia) and control (panmixis) run under default conditions. The koinophilic individuals are clustered into groups with minimal phenotypic clines for either trait. The phenotypic gaps between groups ensured that the probability of a hybrid mating (should members of the two adjacent groups meet) was generally P=0.0000001.
Gould, 1995), or the ‘‘vertical’’ aspect of the speciation problem.
The Model The model consists of a continuous, linear, environmental gradient compromising 1000 niches (microhabitats which could be occupied by only one individual at a time). The population consists of 750 hermaphrodites with discreet generations. Each individual sports two independent polygenic traits. Each trait was determined by the additive effects of 50 unlinked, haploid, Boolean genes. Total genome size was therefore 100 genes. If the environmental extremes are called the equator and pole respectively, and the two traits are fur length and colour, then the shortest fur length (all off-genes) and maximum colouration (all on-genes) were most adaptive for the equator. The opposite would be most adaptive at the pole. The number of on-genes which made a trait best suited (fitness=1.0) for a given niche was determined by niche location (working from the equator for fur length, and from the pole for colour) divided by 20. Trait fitness decreased by zero (no selection), 0.02 (the default), or 0.2 per phenotypic unit deviation from the
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ideal at a given location. (One phenotypic unit equalled the phenotypic influence of one on-gene. As the phenotypic effect of each on-gene carried the same weight, the maximum possible phenotypic difference between two individuals was 50 units per trait.) The selective pressures on the two traits could differ. The fitnesses of the two traits interacted multiplicatively (Franklin & Lewontin, 1970; Lewontin, 1974; Ewens, 1979). On- and off-genes, in generation 0, were randomly distributed throughout the individual genomes, but in such a manner that the individuals (randomly distributed in the environment) formed two phenotypic clines in opposite directions (Fig. 1). Stochastic effects were produced by the Real Version 1 Minimal Standard random number generator described by Park & Miller (1988). Individuals sought mates from amongst the individuals in their geographic locality. Localities consisted, in the default, of the 250 (occupied and unoccupied) niches surrounding each individual. The individuals occupying any of the 125 niches at an environmental extremity shared a common locality: the rest all had individualized localities, of which they occupied the geographic mid-point. Encounters between potential mates were in direct proportion to fitness. Panmictic individuals mated without further ado, producing one offspring, who, in the next generation, occupied the ‘‘mother’s’’ niche, or the nearest unoccupied site to it. Koinophilic individuals preferred the two modal traits in their respective localities. The modal trait, and those that deviated by fewer than five phenotypic units from the mode, had an attractiveness of 1.0. A phenotypic deviation from the mode of between five and nine units had an attractiveness of 0.8. All other phenotypes had an attractiveness, in the default, of 0.01. The probability of mating between two koinophilic individuals was the product of the four attractivenesses per encounter. Mating in the first two generations was always panmictic. Thereafter it was either koinophilic (experimental) or panmictic (control) for a further 28 generations. Each run (experimental plus a control) was repeated 30 times under a given set of parameter conditions. Analysis The phenotypic values of the two polygenic traits for each of the 750 individuals who made up generation 30 of a randomly chosen experimental (koinophilia) and control (panmixis) run under default conditions are displayed in Fig. 2. To describe the evolution of these patterns, groups or clusters
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were first defined as any geographic concentration of e5 individuals separated by e5 unoccupied sites from the next occupied niche. The within-group phenotypic variance was calculated, treating the groups as if they were samples in an analysis of variance (anova). The results, expressed in the form of standard deviations, are displayed on the graphs (Figs 3–5) as dashed lines, labelled a (y-axis scale×2). Quantification of within-group phenotypic clines and between-group phenotypic gaps was done as follows. Regression analysis was performed on the phenotypic values (versus niche location) of each group. Individuals’ actual phenotypic values were then replaced by those obtained (for the individual’s
niche) from the appropriate regression formula. (These analytical manipulations in no way affected the model proper. Individuals’ real phenotypes were immutable and rigidly determined by strict Mendelian principles.) The phenotypic gap between adjacent groups was considered to be the difference between the phenotypic value (calculated by regression analysis) of the individual closest to the pole of one group and that of the most equatorial individual of the adjacent group. Value b was the sum of the differences between the phenotypic values (calculated by regression analysis) of the first and last individuals of each group. This therefore equalled the total phenotypic cline, minus the between-group phenotypic gaps. Thus, if the population was comprised of
F. 3. The evolution of species from an initial phenotypic gradient of interbreeding individuals. Generation time is on the x-axis. The two independent polygenic traits per individual are shown on the z-axis (as the deviation from the ideal of the coefficients of selection, per phenotypic unit, were the same for both traits, as indicated on the z-axis, the evolution of only one of them is shown for clarity’s sake). The graphs represent the means of 30 independent runs under the same parameter conditions. The dashed line (a) depicts the evolution of the within-group phenotype variance (expressed as a standard deviation) for one of the traits (y-axis scale×2). Lines b and c, depict the evolution of the within-group phenotypic clines (calculated by regression analysis for each group): each point in graph b depicts the sum of the within-group increments in phenotypic value (y-axis scale×20). Points along the heavy solid line, (c), depict the sums of the products of the within-group increment in phenotypic value and habitat size (y-axis scale×10). Line d depicts the same as c, except for the phenotypic gaps between the groups.
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F. 4. The same applies as for Fig. 3, except that the strengths of selection for the two traits differ. The evolution of the trait subject to the default decrement in fitness of 0.02 per phenotypic unit deviation from the ideal (maximum fitness=1.0) for its niche is shown in front (lines a1, b1, c1, and d1). The evolution of the other trait, subject to selective neutrality (top), or a decrease in fitness of 0.2 per phenotypic unit deviation from the ideal (bottom), is shown behind (lines a2, b2, c2, and d2). The scales and symbols are the same as in Fig. 3.
compact groups only, and the phenotypic cline in generation 0 was perfectly preserved, then b=50×0.75=37.5. In the absence of within-group phenotypic clines, b=0, and any phenotypic difference between the individual nearest the equator and the one nearest the pole, would be entirely because of the phenotypic gaps between the groups. Value c was calculated as the sum of the products of the within-group increments in phenotypic values (using the results of the regression analysis) and habitat size. Value d denotes the same as c, but for the phenotypic gaps between the groups. The graphs labelled a, b, c, and d, in Figs 3–5 depict the means of 30 values of the corresponding variable (per generation) obtained from 30 separate runs under a same set of parameter conditions. Standard errors of the mean were calculated; but, because they imparted no information that cannot be derived, by inspection, from the fluctuations (from one generation to the next) in the mean values of a, b, c, and d, they are not displayed on the graphs.
Results The phenotypic values for each individual’s two traits in generation 30, in a randomly chosen experimental and control population under default conditions, are displayed in Fig. 2. The number of
groups, their average morphologies, and their locations varied from run to run, but always gave the same impression: the koinophilic populations always coalesced into well-defined groups, whose withingroup phenotypic variance (per trait), although always greater than zero (see lines a in Figs 3–5), was small compared to the between-group phenotypic variance (Fig. 2). Within-group clines were minimal or absent. A group’s average phenotype in generation 30 was always best suited (i.e. had a fitness of 1.0, or very nearly 1.0) for a niche close to the group’s geographic mid-point. That is to say, if a group occupied niches 250–350, its average phenotype, taking both traits into account, was best suited for niche 300 (2SD 9). (The groups’ geographic positions, and therefore the mid-point niches to which they were best adapted, varied randomly, however, from run to run.) The average magnitude of the phenotypic gaps between adjacent groups was such that the chance of a hybrid mating was generally P=0.00000001. This was largely because of the ‘‘survival of the first’’ (Bernstein et al., 1985; Hopf, 1992), by which it is meant that the phenotype which, by chance, became the first to dominate an area was also the one most likely to replace its regional rivals. Since koinophilic individuals preferred common phenotypes, any locally dominant phenotype always tended to become commoner still. Rarer,
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phenotypically intermediate groupings tended to incur increasing costs of rarity, leading to their extinction, the widening of existing phenotypic gaps and thus the dramatic rise, amongst the koinophilic populations, in the value of d (Figs 3–5) compared to that of the panmictic populations. As there were no penalties associated with phenotypic rarity in the panmictic populations, phenotypic gaps and group formation were more variable, within-group clines often remained striking, and reproductive isolation was nonexistent. When both traits were subject to excessive selection (survival restricted to a 35 niche range per trait) koinophilic groups retained remnant clines and were smaller (and, therefore, more numerous) than otherwise (Fig. 3). Clines vanished altogether when both traits were selectively neutral (i.e. there was no environmental gradient affecting the traits) but, because there were no barriers to migration, species frequently splintered into geographically separated but phenotypically identical populations (accounting for the decline in the average value of d after generation 15). When the two traits were subject to different strengths of selection (Fig. 4), group
cohesion was maintained even if one trait was selectively neutral. There was, then, little phenotypic indication of the difference in the strengths of selection acting on the two traits. Variations in the attractiveness of the least desirable phenotypes from 0.01 (the default) to 0.3 had no discernible effect on the process of speciation (Fig. 5). Discussion The results of the model suggest that koinophilia not only converts phenotypic clines of interbreeding individuals into reproductively isolated morphospecies, but also endows the process with inevitability. If sexual creatures avoid mates with unusual or unfamiliar features then groupings of phenotypically similar individuals are bound to form. This phenotypic canalization, as the present two trait model suggests, affects most of the outward appearance regardless, to a large extent, of how the individual components of that appearance are influenced by natural selection. The model suggests, furthermore, a reason for the hallmark of speciation: the reproductive isolation of the morphospecies (Mayr, 1942;
F. 5. The same applies as for Fig. 3, except that there is only one polygenic trait per individual. All the graphs depict the evolution of morphospecies in koinophilic populations. They differ only with respect to the attractiveness of the least common phenotypes in each individual’s locality. The modal phenotype, and those that deviated by fewer than five phenotypic units from the mode always had an attractiveness of 1.0. Those that deviated by between five and nine phenotypic units from the mode had an attractiveness of 0.8. These graphs show the effects of varying the attractiveness (indicated on each graph) of the individuals who deviated by 10 phenotypic units or more from the mode.
Coyne, 1992). The phenotypic discontinuities produced by our model were almost invariably of such a size that the probability of a hybrid mating was the lowest that the model parameters would allow (excluding natural selection). While panmixis frequently created phenotypic clusters, with accompanying phenotypic gaps, the clusters were never reproductively isolated from one another (unless a geographic gap of q125 niches was formed). Compared with koinophilia, panmixis canalized the phenotype haphazardly (see Fig. 2). Clustering of one or a few phenotypic features can occur through a wide variety of means (Wright, 1931; Lande, 1982; Paterson, 1985; Coyne & Barton, 1988; Maynard Smith, 1989; Coyne, 1992; Fialkowski, 1992). None, however, explains why it is almost universal among sexual creatures, nor why it should canalize virtually the entire outward appearance of both sexes, regardless of the traits’ involvement with sexual dimorphism. Nevertheless, the most convincing explanations for the de novo development of reproductive isolation (with subsequent phenotypic divergence into morphospecies), are provided by models that invoke mate choice as the engine of incipient speciation (Lande, 1981, 1982; Ryan & Rand, 1993). The origin and maintenance of mating preferences present many unresolved theoretical problems (Borgia, 1987; Maynard Smith, 1987; Kirkpatrick & Ryan, 1991; Taylor & Williams, 1982). A sexual creature would clearly be expected to choose the fittest available mate with whom to exchange its DNA (Charlesworth, 1987, 1988; Kirkpatrick & Ryan, 1991; Koeslag & Koeslag, 1993, 1994b). Natural selection, however, tends to exhaust the additive variance in fitness in a population, creating serious difficulties for models of the evolution of mate choice for ‘‘good genes’’ (Charlesworth, 1987, 1988). Furthermore, even when present, differences in heritable fitness can only be observed and measured a posteriori (i.e. after several generations have elapsed). A preference for ‘‘good genes’’, therefore, almost inevitably invites cheating through the elaboration of fake ‘‘good phenotypes’’. Nevertheless, plausible models for the origin of mate preference abound (Maynard Smith, 1987; Kirkpatrick & Ryan, 1991). Hamilton & Zuk (1982) have suggested that male ornaments, which females find attractive, may have evolved because they allow the females to discriminate between males who differ heritably in their parasitic loads, and hence in fitness, when cycles in gene frequencies at loci controlling host susceptibility are maintained by shifting selection. Alternatively, it has been suggested that mate choice may simply be
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driven by economic forces. Females who prefer conspicuous males spend less time searching for mates than females preferring drab (and possibly fitter) mates (Kirkpatrick & Ryan, 1991). A third suggestion for the evolution of mate choice proposes that a male characteristic may become genetically correlated with a female mating preference. The favoured male characteristic and the preference need neither be adaptive (although they could have arisen by either of the previous two mechanisms). Once they exist they tend to re-inforce one another, often leading to a runaway process (Fisher, 1930; Lande, 1981). No matter how it arises, a female mating preference for a quantitative secondary sexual characteristic tends to initiate reproductive isolation and phenotypic canalization of the male sexual ornament (Lande, 1981, 1982). Once groups become reproductively isolated, the rest of the phenotype will diverge (though not necessarily become canalized), causing phenotypic gaps to appear for traits not involved in sexual dimorphism. Furthermore, Bernstein et al. (1985) and Hopf (1990) have shown that a phenotypic continuum of species (i.e. groups that are already reproductively isolated one from the other), distributed along a continuous resource gradient, rapidly coalescese into distinct species. Chance fluctuations in population density will bring about variations in the ease with which individuals can find appropriate mates (especially if each species is initially very rare). The fitness of the larger species will, therefore, be greater than that of the smaller species. Bernstein et al. (1985) term this the cost of rarity, which tends to make large species larger at the expense of smaller species. This has a snowball effect which proceeds with increasing speed as it develops. Eventually only a few, phenotypically very distinct species remain. Paterson (1985) and Fialkowski (1992) propose that hybrid disadvantage promotes assortative mating and the exaggeration of existing phenotypic gaps (Ryan & Rand, 1993). Hybrid disadvantage could therefore complement and reinforce the Bernstein et al. (1985) model. However, neither the Bernstein et al. (1985), the Hopf (1990), the Paterson (1985) or the Fialkowski (1992) proposals explain how the reproductive isolation, on which their models rely, arises in the first place. If it depends for its origin primarily on the evolution of mate preferences (Lande, 1981, 1982), then two problems arise. The first is that the evolutionary imperative for mate preferences has to be very strong, and circumstance-independent, to be able to explain the near universality of speciation among sexual creatures. The second problem concerns arbitrary fashion and fakes. If mate preference is as ancient and widespread as speciation,
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then sexual creatures must inevitably become burdened with a surfeit of traits to which the opposite sex has become arbitrarily attracted, and fake ‘‘good phenotypes’’, all of which are presumably largely maladaptive. The present model is also based on mate choice. Its assumptions are that sexual creatures have senses with which they evaluate potential mates; that they are capable of frequency analysis; and that they exploit these capabilities to avoid mates with unusual or unfamiliar traits which are assumed to be, on average, less fit than their common counterparts (Koeslag, 1994; Koeslag & Koeslag, 1994b). The resulting mate choice is clearly not infallible, but it probably represents a sexual creature’s best bet: the chance that a rare or unusual characteristic is maladaptive is extremely high and it would presumably be evolutionary foolishness not to avoid it. Koinophilia has a major advantage over other forms of mate choice because commonality cannot be faked. Its betting chances are also circumstanceindependent. As it is evolutionarily robust (Koeslag, 1994; Koeslag & Koeslag, 1994a, b), it is likely to be widespread, occurring wherever creatures practice sex. Being fallible, however, groups could cling to random phenotypic errors (having achieved commonality through, for instance, a founder effect). These can only be eliminated, or promoted, by intergroup competition (Koeslag 1994; Koeslag & Koeslag 1994a). In the present simulations, however, no such errors survived 30 generations: the koinophilic groups’ average phenotypes in generation 30 were always best suited for the geographic mid-points of their ranges. If these assumptions are valid and realistic, then koinophilia provides an obvious and simple explanation for many, if not most, of the problems concerning speciation, especially its virtual universality among sexual creatures: its canalization of the entire visible (to conspecifics) phenotype of both sexes apparently regardless of differences in the selective advantages of the individual traits; and the inevitability of reproductive isolation. As koinophilia denies individuals with rare or unusual phenotypes the opportunity to mate, the groups’ phenotype becomes evolutionarily static, resisting change even when 5% of mutations are beneficial (Koeslag & Koeslag, 1994a). Species would, therefore, be expected to persist in more or less unchanged form for long periods of time. Transitional forms produced when groups disintegrate, or when new species bud from the established form, are likely to be evanescent. They are, therefore, as
unlikely to be represented in the fossil record as they are to appear in the catalogues of present day forms.
REFERENCES A, F. J. (1982). Population and Evolutionary Genetics. Menlo Park, California: Benjamin Cummings. B, G. (1987). A critical review of sexual selection models. In: Sexual Selection: Testing the Alternatives (Bradbury, J. W. & Andersson, M. B., eds) pp. 55–66. Chichester: John Wiley & Sons. B, H., B, H. C., H, F. A. & M, R. E. (1985). Sex and the emergence of species. J. theor. Biol. 117, 665–690. C, B. (1987). The heritability of fitness. In: Sexual Selection: Testing the Alternatives (Bradbury, J. W. & Andersson, M. B., eds) pp. 21–40. Chichester: John Wiley & Sons. C, B. (1988). The evolution of mate choice in a fluctuating environment. J. theor. Biol. 130, 191–204. C, J. A. (1992). Genetics and speciation. Nature 355, 511–515. C, J. A. & B, N. H. (1988). What do we know about speciation? Nature 331, 485–486. C, T. M. (1985). Speciation and stasis in marine Ostracoda: climatic modulation of evolution. Science 227, 60–63. D, J. M. (1992). Horrible plant species. Nature 360, 627–628. E, L. (1965). Direct observation of sexual isolation between allopatric and between sympatric strains of the different Drosophila paulistorum races. Evolution 19, 459–464. E, W. (1979). Mathematical Population Genetics. New York: Springer-Verlag. F, K. R. (1992). Sympatric speciation: a simulation model of imperfect assortative mating. J. theor. Biol. 157, 9–30. F, R. A. (1985). The Genetical Theory of Natural Selection. 2nd edn. New York: Dover. F, I. & L, R. C. (1970). Is the gene the unit of selection? Genetics 65, 707–734. G, D. S. (1987). Towards a predictive theory of speciation: the ecology of isolate selection. J. theor. Biol. 126, 323–333. G, S. J. (1982). A quahog is a quahog. In: The Panda’s Thumb. pp. 204–213. New York: Norton. G, S. J. (1995). The evolution of life on earth. Sci. Am. 271, 62–69. G, S. J. & E, N. (1993). Punctuated equilibrium comes of age. Nature 366, 223–227. H, W. D. & Z, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387. H, F. A. (1990). Darwin’s dilemma of transitional; forms: a comparison of a model with data. In: Organizational Constraints on the Dynamics of Evolution. (Maynard Smith, J. & Vida, G., eds) pp. 357–372. Manchester: Manchester University Press. K, M. & R, M. J. (1991). The evolution of mating preferences and the paradox of the lek. Nature 350, 33–38. K, J. H. (1994). Koinophilia replaces random mating in populations subject to mutations with randomly varying fitnesses. J. theor. Biol. 171, 341–345. K, J. H. & K, P. D. (1993). Evolutionarily stable meiotic sex. J. Hered. 84, 369–399. K, J. H. & K, P. D. (1994a). Koinophilia. J. theor. Biol. 167, 55–65. K, P. D. & K, J. H. (1994b). Koinophilia stabilizes bi-gender sexual reproduction against asex in an unchanging environment. J. theor. Biol. 166, 251–260. L, R. (1981). Models of speciation by sexual selection on polygenic traits. Proc. natl. Acad. Sci. 78, 3721–3725. L, R. (1982). Rapid origin of sexual isolation and character divergence in a cline. Evolution 36, 213–223. L, R. C. (1974). The Genetic Basis of Evolutionary Change. New York: Columbia University Press.
M S, J. (1983). The genetics of stasis and punctuation. Ann. Rev. Genet. 17, 11–25. M S, J. (1987) Sexual selection—a classification of models. In: Sexual Selection: Testing the Alternatives (Bradbury, J. W. & Andersson, M. B., eds) pp. 9–20. Chichester: John Wiley & Sons. M S, J. (1989). Evolutionary Genetics. Oxford University Press. M S, J. (1990). Concluding remarks. In: Organizational Constraints on the Dynamics of Evolution. (Maynard Smith, J. & Vida, G., eds) pp. 433–437. Manchester: Manchester University Press. M, E. (1942). Systematics and the Origin of Species. New York: Columbia University Press.
409
M, E. (1963). Animal Species and Evolution. Cambridge: Harvard University Press. P, S. K. & M, K. W. (1988). Random number generators: good ones are hard to find. Communs. Assoc. Comput. Mach. 31, 1192–1201. P, H. E. H. (1985). The recognition concept of species. In: Species and Speciation (Vbra, E. S. ed.) pp. 21–29. Pretoria: Transvaal Museum Monographs No. 4. R, M. J. & R, A. S. (1993). Species recognition and sexual selection as a unitary problem in animal communication. Evolution 47, 647–657. T, P. D. & W, G. C. (1982). The lek paradox is not resolved. Theor. Popul. Biol. 22, 392–409. W, S. (1931). Evolution in Mendelian populations. Genetics 16, 97–159.