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local algal community structure. Thus, the structure of this community appears to be determined by a tight linkage between bottom-up and top-down factors. Further, disruption of this linkage, via, for example, declines in kelp abundance resulting from El Niiio-Southern Oscillation events or glo bal warming, would most likely alter these communities dramatically. While several alternative outcomes to disruptions could be predicted (e.g. limpets could become more mobile with reduced density and maintain a system of low algal abundance; limpets could remain sedentary with reduced density, leading to an increase in abundance of algal turfs; and so on), additional insights await further study of this fascinating community. Second, the critical kelp supply is exogenously produced, indicating that the structure of this community (dense and large limpets, near-absence of foliose macrophytes within the limpet beds) depends on a food ‘subsidy’. While this source is only centimeters away for semi-exposed communities, it can be hundreds of meters

Reinforcement:

an increase in assortative mating and thus progress towards speciation. This simple prediction is the nub of the reinforcement hypothesis, which had its origins with Alfred Russel Wallace’ and has been controversial ever sincez-4. A new models and several recent empirical studies-9 look set to keep the debate about reinforcement in the foreground of speciation research. Reinforcement has been modelled several times before (see references in Ref. 5). There can be no doubt that reduced fitness of hybrids does generate a selection pressure favouring assortative mating, or divergence in sexual signals and responses that generate assortment. However, the conditions under which this selection will generate a response have usually been considered restrictive. Strong selection against hybrids is required and the reinforcement is opposed by two key processes: recombination and gene flow. Reinforcing selection works indirectly on assortative mating through the association of mating genes with the genes responsible for hybrid dysfunction. Recombination disrupts these associations and may also break-up combinations of genes that contribute to hybrid inviability or sterility, thus removing the clean distinction between parental and 2

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Hunter, M.D. and Price, P.W. (1992) Ecology 73, 724-732

Power, M.E. (1992) Ecology 73, 733-746 Menge, B.A. (1992) Ecology 73,755-765 Bustamante, R.H., Branch, C.M. and Eekhout, S. Ecology (in press) Polis, GA. and Hurd, S.D.(1995)Froc. Nat/ Acad. Sci. USA 92,4382-4386

Duggins, D.O., Simenstad, CA. and Estes, J.A. (1989) Science 245, 170-173 Menge, B.A., Daley, B. and Wheeler, P.A. in Food

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Bruce A. Menge 13

Dept of Zoology, Oregon State University, Corvallis,OR97331-2914,USA 14

References 1 Carpenter, S.C., ed. (1988) Interactions

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two divergent populations produce Iintofhybrids of low fitness where they come contact, natural selection will favour

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away for sheltered communities. Such strong external effects on community structure have been suggested in a few other instance+8, but to my knowledge, the present study is the first to test directly the proposed bottom-up influence by manipulating food input. Although further study is needed to establish the generality and importance of bottom-up influences such as that documented by Bustamante et al., their work represents a significant advance in our understanding of the regulation of natural communities, and has strong implications for the consequences of human activities on coastal environments.

hybrid genotypes and eroding the benefits of mate choice. Gene flow opposes reinforcement because the selection for increased assortment occurs only where the two populations meet. Influx of genes from other areas will, therefore, tend to dilute its effects. A new model... What does the new model by Lily Liou and Trevor Price5 add to this picture? Unlike many models that envisage secondary contact in parapatry between populations that have diverged in allopatry, this model considers secondary contact in sympatry. It combines aspects of a previous attempt to include ecological parameterslo with the production of hybrids of variable fitness. The type of scenario envisaged is the colonization of a small lake by two divergent stickleback populations where the possible outcomes are extinction of one population, permanent mixing of the gene pools, or reinforcement and speciation. This contrasts with hybrid zones where stable coexistence is a further possible outcome. Another nice feature is that mating pattern is determined by a male signal and a female preference, with separate genetic determination, rather than a mysterious ‘assortative mating locus’. The outcomes are summarized in Fig. 1. Overall, reinforcement is more likely than

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(Polis, GA. and Winemiller, K.O., eds), Chapman &Hall (in press) Connell, J.H. (1961) Ecol. Monogr. 31, 61-104 Paine, R.T. (1966) Am. Nat. 100,65-75 Castenholz, R. (1961) Ecology 42, 783-794 Lubchenco, J. and Gaines, S.D.(1981) Annu. Rev. Ecol. Syst. 12,405-437 Branch, GM. (1986) in The Ecology of Rocky Coasts (Moore, PG. and Seed, R., eds), pp. 97-l 16, Columbia University Press Eekhout, S.,Raubenheimer, C.M., Branch, G.M., Bosman, A.L. and Bergh, M.O. (1992) S.Ah: J. Mar. Sci. 12,1017-1029 Branch, G.M. and Griffiths, CL. (1988) Oceanogr. 395-486

Mar. Biol. Annu. Rev. 26,

in previous models, especially the comparable Spencer et al. modello. A major reason for this is the interaction between male signal and female preference: as in sexual selection model+, a genetic correlation is generated between signal and preference. This tends to amplify divergence initially generated by reinforcement and drives speciation to completion. In previous models a negative feedback occurred where increased assortative mating meant that (1) less hybrids were produced, (2) there was less selection for assortment, and (3) complete speciation was very unlikely. By comparison with hybrid zone models, reinforcement is more likely because the diluting effects of gene flow’* are absent, but Liou and Price do show that their model can produce divergence in a parapatric context as well. Population growth parameters influence the overall probability of the extinction of one population, and the population on which extinction falls, in predictable ways. Reinforcement remains dependent on strong selection against hybrids, is favoured by substantial prior divergence in mating signals, and is more likely where there is tight genetic linkage between hybrid fitness and mating loci, that is, it is still opposed by recombination. Liou and Price argue that the condition of zero hybrid fitness, which I have previously distinguished as ‘reproductive character displacement”, is not fundamentally distinct from reinforcement. The main reason for keeping the processes separate was that, with zero hybrid fitness, there is TREE

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NEWS no mixing of the two gene pools: selection can act on them independently and divergence is not opposed by recombination, either among loci influencing hybrid fitness, or between these loci and genes involved in mate choice. However, where hybrid fitness is very low but not zero, ‘parental’ combinations of alleles still predominate: the influence of recombination is limited by the frequency with which multiple heterozygotes are produced and survive to contribute to future generations. So, there is no absolute distinction between the two cases. The outcome of interactions with very low hybrid fitness is likely to be influenced by the genetics of hybrid dysfunction with the strongest associations among parental alleles being maintained when many loci contribute. Probably the most questionable aspect of Liou and Price’s model is the genetic basis of selection against hybrids: there are just two loci with two alleles each and all hybrids (i.e. individuals with a mixture of parental alleles) have the same fitness. Quite a lot is known about the genetics of postzygotic isolationl3, and it would be nice to know how different architectures effect the outcome of reinforcement. . . . and new data The empirical study by Mohamed Noor- addresses a situation where the current level of gene exchange is very low, too low to have much influence on the ‘parental’ combinations of genes, although this is not accounted for by observed selection against hybrids. Noor studied the species pair Drosophila pseudoobscura and D. persimilis in the western USA. Hybrid males are sterile but hybrid females are fertile and both sexes are viable in the laboratory. Rare hybrids occur in the field. Reinforcement was tested in the classic way, by asking whether D. pseudoobscura females from sympatric locations discriminated against D. persimilis males more strongly than did females from allopatric locations. Unfortunately, the opposite test is not possible because allopatric D. persimilis populations are not known. A significant deviation in the expected direction was observed in five out of six comparisons of latency to mating, involving two sympatric and three allopatric localities. This result is exciting mainly because the species involved are so well characterized in other respects, including genetically, that there is the potential to analyse the pattern reported very effectively. As it stands, the observation is really no stronger evidence for reinforcement than previous example+. The allopatric populations are all to the east of the sympatric populations so that clinal variation independent of sympatry cannot be ruled out. Also, mating latency tests are notoriously TREE

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n Hybridization

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Fig. 1. Outcomes of the sympatric version of the Liou and Price model5 as a function of hybrid fitness and the initial difference between populations (IT,) in the male secondary sexual trait. Boundaries demarcate regions of pure and mixed outcomes based on 30 simulation runs. Reproduced, with permission, from Ref. 5.

difficult to control for variables such as male vigour and environmental effects: it would be nice to see evidence for divergence in a critical sexual signal. Noor also compared mating frequency with D. pseudoobscura males by D. persimilis females from populations where D. persimilis is either rare or common relative to its sibling, arguing that the strongest selection for discrimination occurs where the risk of interspecific mating is greatest. The results for one of two comparisons showed a significant difference between populations in the expected direction. This is a novel approach that could provide more discriminating predictions than the simple sympatry/allopatry comparison, but a larger number of localities will have to be examined before a robust test is possible. The distinction between reinforcement and reproductive character displacement is more difficult to maintain if rare gene exchange, as in these Drosophila species, is common. Indeed, definitions of species based on gene exchange are difficult to apply to such cases14.Carl Gerhardt9 pro vides a much more robust demonstration of the effects of sympatry on mate choice - in this case, in the tree frog Hyla chrysoscelis - than is so far available for D. pseudoobscura, but this is attributed to reproductive character displacement because hybrids are triploid, rarely survive to adulthood, and are sterile. On the other hand, rare gene exchange is much more difficult to exclude in Cryptomyzus aphids8 where differences in phenology and specificity of pheromones between species in-

habiting the same primary host have been attributed to reinforcement. The work of Kerstin Johannesson and her colleaguesrV15has revealed a very different potential example of reinforcement. On rocky shores of north-western Spain, winkles (Littorina saxatilis) have two different ecotypes, distinguishable by shell morphology, only a few metres apart. In a narrow zone of overlap between ‘highshore’ and ‘low-shore’ forms, intermediates exist at a frequency of 1l-29%. Allozyme studies show no overall differentiation between these forms on a geographic scale but do distinguish forms on a local scale, suggesting a partial barrier to gene exchange that may have arisen in sita. Now, there is evidence from field studies7 for assortative mating between morphs where they are in contact, but not elsewhere. It is difficult to extract this pattern cleanly from the very fine-scale patchiness of winkle distributions, or from the obfuscating effect of homosexual mountings, but, as with Noor’s study, there seems to be a prima facie case for reinforcement. Reinforcement remains, for the moment, a potentially important evolutionary process that lacks a fully convincing example. However, there is good reason to hope that further work on these promising systems will place it on a firmer footing. Acknowledgements I am very grateful to Kerstin Johannesson for access to her forthcoming article and to Mohamed Noor for stimulating e-mail discussions. 433

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Roger K. Butlin Ecology and Evolution Programme, Dept of Genetics, The University of Leeds, Leeds. UK LS2 9JT

References 1 Wallace, A.R. (1889) Darwinism: 2

An Exposition of the Theory of Natural Selection with some of its Applications, Macmillan Butlin, R.K. (1987) Trends Ecol. Evol. 2,8-13

3 Howard, D.J. (1993) in Hybrid Zones and the Euolutionary Process(Harrison, R.G., ed.), pp. 46-69, Oxford University Press 4 Littlejohn, M.J. (1993) Oxf Sum. Evol. Biol. 9, 135-165 5 Liou, L.W. and Price, T.D. (1994) Evolution 48, 1451-1459 6 Noor, M.A. (1995) Nature 375,674-675 7 Johannesson, K., Rot&r-Alvarez, E. and Ekendahl, A. Evolution (in press) 8 Guldemond, J.A. and Dixon, A.F.G.(1994) Biol. J. Linn. Sot. 52,287-303

Incorporating physiological realism into models of parasitoid feeding behaviour esearchers of parasitoids have long R been aware that such insects [whose females lay their eggs on or in other invertebrates (mainly insects) and whose larvae feed on the host and eventually kill it] habitually feed on hosts, nectar, pollen or honeydew in the field, but they have been slow to apply this knowledge to ecological studies. Awareness of the potential importance of adult feeding is, however, gaining momentum among behavioural ecologistslJ and theoretical population biologist+. New papers by Collier-1and Briggs et cd.6 are the latest milestones in the modelling of this biologically complex phenomenon, as they highlight the importance of physic+ logical correlates of feeding behaviour.

Modelling feeding behaviour So far as theoretical modelling of feeding behaviour is concerned, the most convenient starting point is ‘host feeding’ the consumption of host blood or tissues. The widespread occurrence of host feeding can be explained by the benefits it confers over the consumption of other food types. Compared with carbohydrate-based ‘nonhost foods’, such as nectar and honeydew, host blood is superior as a source of egg production materials, For many parasitoids, non-host foods tend to be spatially separated from hosts in the field, so searching for them will incur losses in energy and time-two potentially important resources for foraging parasitoids. Host feeding may incur costs, however. In particular, it may bring about a reduction in quality of the host as an oviposition resource, either by causing the host to die, or by significantly reducing the amount of resource available (through non-destructive host feeding, in which the same host individuals are used for the two activities). This cost may be lessened by the use of lower quality hosts for host feeding and higher quality hosts for ovipositionr. 434

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For non-concurrent destructive host feeders, the decision of whether to feed on or oviposit in a host is an example of the classical trade-off between current reproduction (oviposition) and investment in future reproduction (feeding)lJ. The main problem faced by theoreticians has been to achieve a sufficient degree of biological realism in models, given the (I priori expectation that the decision by a female to host feed will depend dynamically on factors such as the internal state of the parasitoid, for example, the number of mature eggs it has available for oviposition (‘egg load’), the level of its nutrient reserves, the amount of host blood in its gut, and the female’s age, and also any external mortality risk. Collier’ constructed his models within the framework of dynamic state variable modellinga. The models include a number of physiological state variables - such as the quantity of the parasitoid’s nutrient reserves, and/or its egg load - that are altered when feeding or oviposition occur. Using this technique, the parasitoid’s life time is divided into numerous time-steps within each of which there is a probability of an encounter with a host. The optimal decision by the female maximizes the sum of current fitness gains from oviposition and future fitness gains, the latter depending both on alterations in the state variable(s) and on the probability of surviving the time-step. Between time-steps, the female ages and eventually approaches a ‘time horizon’ representing either its maximum longevity or the end of the season. Collier’s are among the more biologically realistic models of host-feeding behaviour in assuming that nutrients can be used for egg production and for maintenance metabolism. They predict that host feeding can occur at egg loads greater than zero, and that it is more likely at low egg loads. Critical egg loads at and below which

9 Gerhardt, H.C. (1994) Anim. Eehav. 47, 959-969

10 Spencer, H.G., McArdle, B.H. and Lambert, D.M. (1986)Am. Nat. 128,241-262 11 Maynard Smith, .I. (1991) Trends Ecol. Evol. 6, 146-151 12 Sanderson, N. (1989) Evolution 43,1223-1235 13 Wu, C-l. and Palopoli, M.F. (1994) Annu. Rev. Cenet. 27,283-308

14 Mallet, J. (1995) Trends Ecol. Evol. 10,294-299 15 Johannesson, K., Johannesson, B. and Rolarr-Alvarez, E. (1993) Evolution 47,1770-1787

host feeding occurs depend on the parasitoid’s age or closeness of the time horizon. The tendency to host feed declines as the insect approaches the end of its reproductive life, gaining little in terms of future survival or egg production. A problem faced by Collier and previous modellers has been the realistic rep resentation of the time delay between the act of host feeding and the appearance of mature eggs in the ovaries. In simpler models, host feeding leads to the formation of new eggs in the time-step immediately following feeding (e.g. the next day). Modellers have rightly suspected there to be an egg maturation delay, but some have avoided incorporating this into models, one reason being the need to involve a large number of state variables that alter over different time scales. This difficulty was resolved by Collier using the technique of ‘sequential coupling’, which involves dividing the different processes on each time scale into a number of sequentially linked or ‘coupled’ submodels*. Collier shows that the incorporation of a realistically long egg-maturation delay generally raises the critical egg load at which host feeding is predicted to occur. The functional explanation for this is that without a delay, the female can delay host-feeding until she has no eggs. With a delay, however, there is a risk of her being without any eggs to lay for an extended period of time. Collier also examined in one model the effect of resorption of mature eggs. Egg re sorption is viewed as a physiological lastresort survival tactic of parasitoidsg; if there are insufficient nutrients in the gut at the end of the daily foraging period to meet the metabolic demand, the nutrients within mature eggs are used. The model assumes, realistically, that egg resorption incurs a metabolic cost, and it predicts that host feeding should occur at higher critical egg loads when resorption occurs. What is so remarkable about Collier’s models is that (1) they incorporate physic logical features hitherto overlooked by modellers, and (2) for the first time realistic, empirically obtained values are used for a wide range of parameters, including, importantly, the egg maturation TREE

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