The Reinforcement of Mating Preferences on an Island
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Copyright 1999 by the Genetics Society of America The Reinforcement of Mating Preferences on an Island Mark Kirkpatrick*,² and Maria R. Servedio*,1 *Department of Zoology, University of Texas, Austin, Texas 78712 and ²GeÂneÂtique and Environnement, Institute de l'Evolution, Universite Montpellier 2, 34095 Montpellier, France Manuscript received April 10, 1998 Accepted for publication September 15, 1998 ABSTRACT We develop a haploid model for the reinforcement of female mating preferences on an island that receives migrants from a continent. We ®nd that preferences will evolve to favor island males under a broad range of conditions: when the average male display trait on the island and continent differ, when the preference acts on that difference, and when there is standing genetic variance for the preference. A difference between the mean display trait on the continent and on the island is suf®cient to drive reinforcement of preferences. Additional postzygotic isolation, caused, for example, by either epistatic incompatibility or ecological selection against hybrids, will amplify reinforcement but is not necessary. Under some conditions, the degree of preference reinforcement is a simple function of quantities that can be estimated entirely from phenotypic data. We go on to study how postzygotic isolation caused by epistatic incompatibilities affects reinforcement of the preference. With only one pair of epistatic loci, reinforcement is enhanced by tighter linkage between the preference genes and the genes causing hybrid incompatibility. Reinforcement of the preference is also affected by the number of epistatically interacting genes involved in incompatibility, independent of the overall intensity of selection against hybrids. HILE mating preferences are clearly fundamen- ous. Evidence of reinforcement has, however, been W tal as isolating mechanisms in many groups of found in several detailed studies of geographical varia- animals, it is unclear whether they are the cause or tion in mating behavior within species, for example, in the effect of speciation. A common view is that mating frogs (Gerhardt 1994), ¯ies (Noor 1995), and birds preferences are an important cause of speciation. The (Saetre et al. 1997). Strong support for the widespread hypothesis here is that mating preferences diverge in operation of reinforcement comes from the work of isolated populations as a by-product of genetic change Coyne and Orr (1989b, 1997; see also Noor 1997). caused by either adaptation or genetic drift. This diver- Their review of studies on 171 species of Drosophila gence causes prezygotic isolation that results in spe- shows that sympatric pairs of species have far stronger ciation (Mayr 1963; Rice and Hostert 1993). The behavioral isolation than allopatric pairs that have been converse possibility, that speciation causes preference isolated for comparable amounts of time. evolution, was suggested by Dobzhansky (1940). Under Theoretical objections to the reinforcement hypothe- his idea of reinforcement, an important side-effect of sis have also been raised. Reinforcement involves two divergence in allopatry is partial postzygotic isolation. competing forces that act on a mating preference. The Crosses between individuals from different populations ®rst is indirect selection. Even if preferences do not produce offspring with reduced ®tness. When two popu- directly affect survival or the number of gametes pro- lations come into contact, there is a selective premium duced, preference alleles favoring heterotypic matings for individuals from each population to avoid mating are indirectly selected against because they are as- with individuals from the other. Consequently, mating sociated with low-®tness hybrid genotypes. This is the preferences evolve to reinforce the postzygotic isolation, engine that drives reinforcement. The countervailing accelerating the process of speciation. force is gene ¯ow: hybridization causes the preference Although intuitively appealing, the reinforcement hy- genes in the two populations to become homogenized. pothesis has a checkered history of support from evo- The most obvious theoretical problem for reinforce- lutionists (reviewed by Butlin 1987, 1989; Howard ment is that the force of gene ¯ow might overwhelm 1993). On the empirical side, weaknesses have been indirect selection and prevent reinforcement from suc- identi®ed in many early studies that were offered in ceeding (Moore 1957; Mayr 1963). Recombination support of the idea, making their interpretation ambigu- breaks down the genetic associations between prefer- ence genes and the loci selected against in hybrids (Felsenstein 1981; Barton and Hewitt 1985), which Corresponding author: Mark Kirkpatrick, Department of Zoology, Uni- versity of Texas, Austin, TX 78712. E-mail: [email protected] weakens the force of indirect selection favoring rein- 1 Present address: Section of Ecology and Systematics, Corson Hall, forcement. Cornell University, Ithaca, NY 14853. Several models have established that reinforcement Genetics 151: 865±884 (February 1999) 866 M. Kirkpatrick and M. R. Servedio of mating preferences can succeed, however, at least in speci®c model in which hybrid un®tness is caused by some circumstances. Sved (1981) considered the situa- epistatic interactions. Results there show how the ge- tion of complete hybrid inviability or sterility and de- netic basis of hybrid un®tness can affect the outcome rived analytic expressions for the reinforcement of a of reinforcement. speci®c type of mating preference. Three simulation There are four features of the model we emphasize studies since then have found that reinforcement of at the start. First, we assume that mating preference mating preferences succeeds in some but not all cases. genes are free of direct selection; that is, preference Spencer et al. (1986) developed a model that includes genes do not affect the survival or the number of ga- demography as well as evolution and tracked the fate metes produced by an individual. This allows us to look of a single population when hybrids are completely in- at the effects of reinforcement on preference evolution fertile or inviable. Liou and Price (1994) extended that in isolation from other evolutionary forces. In our model by allowing reciprocal introgression between a model, reinforcement results from genetic associations pair of species that have only partial postzygotic isola- (linkage disequilibrium) between preference alleles tion. Servedio and Kirkpatrick (1997) compared situ- and other genes that are directly selected, for example ations in which there is reciprocal introgression with those that cause hybrids to have low ®tness, as envi- situations involving one-way gene ¯ow. Because these sioned by Dobzhansky. Second, the model is quite gen- simulation models make quite restrictive assumptions eral in several respects regarding genetics (e.g., there about genetics and behavior, it is not known how gen- can be any number of genes and any linkage relations eral their qualitative conclusions might be or how the between the genes that affect hybrid ®tness, the prefer- results can be applied quantitatively to natural popula- ence, and the display) and behavior (any form of mating tions. preference is allowed). The model is therefore free of This article develops an analytic model for investigat- several assumptions that restrict the generality of earlier ing the reinforcement of mating preferences on an is- models. Third, the model treats the average value of land that receives immigrants from a continent. It con- the display trait as a known quantity, rather than ac- siders what happens when postzygotic isolation is weak counting for its evolution explicitly. This approach and so applies to the early phases of divergence. We makes the results general to all forms of natural and choose to focus on this situation for two reasons. First, sexual selection that might act on a display. Fourth, the islands are sites of rapid and profuse speciation (Mayr migration rate of continental individuals onto the island 1963), and it is of interest to see how reinforcement is also viewed as a known quantity. Again, this buys might play a role in these radiations. Second, it is simpler generality: no restrictive assumption is made about how to study a single island population than two or more the values of the mating preference and display trait populations in which the picture is complicated by the affect rates of hybridization. But another consequence effects of reciprocal gene ¯ow and spatial structure. is that our model does not describe how evolution might Our main aim is to determine if and how mating shut off introgression and lead to complete reproduc- preferences that discriminate against the continental tive isolation, as Dobzhansky suggested. Thus ours is a immigrants will evolve on an island. Major questions model for the reinforcement of mating preferences, but are: Can reinforcement of mating preferences occur, not for the reinforcement of prezygotic isolation. and if so how big of an impact will it have? Does the way in which hybrids are selected against determine if THE GENERAL MODEL reinforcement succeeds? How is reinforcement affected by genetic details such as the number of loci, their Our model considers the evolution of three kinds of linkage, and the distribution of their effects? When can characters: a female mating preference, a male display observable phenotypic characters be used to make pre- trait that the preference acts on,