SPECIATION BY REINFORCEMENT OF PREMATING ISOLATION

The generation of premating isolation given partial or complete postzygotic isolation between populations is termed reinforcement or, in the case of complete isolation, reproductive character displacement. In this study we use computer simulations and a multilocus genetic model to reevaluate the theory of reinforcement. We consider the evolution of female preferences for a male secondary sexual trait. If the populations differ in mean female preference, there is direct selection on the preference for further divergence, which may be augmented by a correlated response to sexual selection on males. Two factors prevent divergence. First, if postzygotic isolation is not complete, gene flow can prevent divergence and lead to a hybrid swarm. This is the usual outcome whenever the average number of breeding adult offspring produced by a hybrid mating is sufficient to replace the parents. Second, one or the other population may become extinct because of the large number of hybrid matings it is involved in. The likelihood of extinction is lowered if population growth rates are high, if hybrids are inviable rather than infertile, or under some conditions when allopatric populations provide immigrants into the contact zone. Provided hybrid fitness is sufficiently low, there is a wide range of genetic and ecological conditions under which reinforcement rather easily occurs, and also a range under which it may occur because of stochastic effects on both the inheritance parameters and the population sizes.     

GOOD GENES AND DIRECT SELECTION IN THE EVOLUTION OF MATING PREFERENCES

A model is used to study quantitatively the impact of a good genes process and direct natural selection on the evolution of a mating preference. The expression of a male display trait is proportional to genetic quality, which is determined by the number of deleterious mutations a male carries throughout his genome. Genetic variances and covariances, including the covariance between the preference and male trait that drives the good genes process, are allowed to evolve under an infinitesimal model. Results suggest that the good genes process generates only weak indirect selection on preferences, with an effective selection intensity of a few percent or less. If preferences are subject to direct natural selection of the intensity observed for other characters, the good genes process alone is not expected to exaggerate the male trait by more than a few phenotypic standard deviations, contrary to what is observed in highly sexually selected species. Good genes can, however, cause substantial exaggeration if preference genes are nearly selectively neutral. Alternatively, direct selection on preference genes, acting on mating behavior itself or on the genes' pleiotropic effects, can cause mating preferences and male display traits to be exaggerated by any degree. Direct selection of preference genes may therefore play an important role in species that show extreme sexual selection.     

THE EVOLUTION OF HYBRID INCOMPATIBILITIES ALONG A PHYLOGENY

The Dobzhansky–Muller model of speciation posits that defects in hybrids between species are the result of negative epistatic interactions between alleles that arose in independent genetic backgrounds. Tests of one important prediction from this model, that incompatibilities “snowball,” have relied on comparisons of the number of incompatibilities between closely related pairs of species separated by different divergence times. How incompatibilities accumulate along phylogenies, however, remains poorly understood. We extend the Dobzhansky–Muller model to multispecies clades to describe the mathematical relationship between tree topology and the number of shared incompatibilities among related pairs of species. We use these results to develop a statistical test that distinguishes between the snowball and alternative incompatibility accumulation models, including nonepistatic and multilocus incompatibility models, in a phylogenetic context. We further demonstrate that patterns of incompatibility sharing across species pairs can be used to estimate the relative frequencies of different types of incompatibilities, including derived–derived versus derived–ancestral incompatibilities. Our results and statistical methods should motivate comparative genetic mapping of hybrid incompatibilities to evaluate competing models of speciation.     

COMPARATIVE APPROACHES TO THE EVOLUTION OF REPRODUCTIVE ISOLATION: A COMMENT ON SCOPECE ET AL. 2007

Speciation can be driven by the evolution of many forms of reproductive isolation. Comparative study is a powerful approach for elucidating the relative importance of individual isolating barriers in the speciation process. A recent contribution by Scopece and colleagues provides comparative data for two groups of deceptive pollination orchids and aims to test hypotheses about which forms of isolation are most important in the two clades. The authors compare pollinator isolation and postmating isolation between the two orchid groups, and conclude that food-deceptive orchid species have less isolation by pollinator specificity than sexually deceptive species, and that postmating isolation is more important in the food-deceptive clade. Although we find this approach to be novel and potentially powerful, these conclusions are called into question by the methods used to define and select species and quantify pollinator isolation. Definition and selection of taxa were performed in a biased manner that undermines the ability to infer general patterns of speciation. Furthermore, pollinator isolation was calculated inconsistently for the two groups under study, effectively nullifying the comparison.     

ON THE COYNE AND ORR‐IGIN OF SPECIES: EFFECTS OF INTRINSIC POSTZYGOTIC ISOLATION,ECOLOGICAL DIFFERENTIATION,X CHROMOSOME SIZE,AND SYMPATRY ON DROSOPHILA SPECIATION

Coyne and Orr found that mating discrimination (premating isolation) evolves much faster between sympatric than allopatric Drosophila species pairs. Their meta‐analyses established that this pattern, expected under reinforcement, is common and that Haldane's rule is ubiquitous in Drosophila species divergence. We examine three possible contributors to the reinforcement pattern: intrinsic postzygotic isolation, dichotomized as to whether hybrid males show complete inviability/sterility; host‐plant divergence, as a surrogate for extrinsic postzygotic isolation; and X chromosome size, whether roughly 20% or 40% of the genome is X‐linked. We focus on “young” species pairs with overlapping ranges, contrasted with allopatric pairs. Using alternative criteria for “sympatry” and tests that compare either level of prezygotic isolation in sympatry or frequency of sympatry, we find no statistically significant effects associated with X chromosome size or our coarse quantifications of intrinsic postzygotic isolation or ecological differentiation. Although sympatric speciation seems very rare in animals, the pervasiveness of the reinforcement pattern and the commonness of range overlap for close relatives indicate that speciation in Drosophila is often not purely allopatric. It remains to determine whether increased premating isolation with sympatry results from secondary contact versus parapatric speciation and what drives this pattern.     

DISSECTING SELECTION ON FEMALE MATING PREFERENCES DURING SECONDARY CONTACT

Population-specific preferences involved in premating isolation may be based on several different types of mating cues. Here, we compare the rates of spread of 12 different mating preferences that reflect preferences for local adaptation, male condition, and reinforcement. We introduce methods to dissect the components of the rate of spread to determine why certain mating preferences spread more quickly than others. We confirm the result that female preferences based on population-specific markers alone always spread faster than female preferences based only on a single local adaptation locus, regardless of the strength of natural selection on hybrid incompatibility. However, we find that this occurs for different reasons depending on the strength of selection against hybrids. Female preferences based on total male condition also achieved high rates of spread, suggesting that preferences for condition-dependent male displays may evolve under reinforcement scenarios.     

THE EVOLUTION OF STRONG REPRODUCTIVE ISOLATION

Felsenstein distinguished two ways by which selection can directly strengthen isolation. First, a modifier that strengthens prezygotic isolation can be favored everywhere. This fits with the traditional view of reinforcement as an adaptation to reduce deleterious hybridization by strengthening assortative mating. Second, selection can favor association between different incompatibilities, despite recombination. We generalize this "two allele" model to follow associations among any number of incompatibilities, which may include both assortment and hybrid inviability. Our key argument is that this process, of coupling between incompatibilities, may be quite different from the usual view of reinforcement: strong isolation can evolve through the coupling of any kind of incompatibility, whether prezygotic or postzygotic. Single locus incompatibilities become coupled because associations between them increase the variance in compatibility, which in turn increases mean fitness if there is positive epistasis. Multiple incompatibilities, each maintained by epistasis, can become coupled in the same way. In contrast, a single-locus incompatibility can become coupled with loci that reduce the viability of haploid hybrids because this reduces harmful recombination. We obtain simple approximations for the limits of tight linkage, and strong assortment, and show how assortment alleles can invade through associations with other components of reproductive isolation.     

REINFORCEMENT OF STICKLEBACK MATE PREFERENCES: SYMPATRY BREEDS CONTEMPT

Detailed studies of reproductive isolation and how it varies among populations can provide valuable insight into the mechanisms of speciation. Here we investigate how the strength of premating isolation varies between sympatric and allopatric populations of threespine sticklebacks to test a prediction of the hypothesis of reinforcement: that interspecific mate discrimination should be stronger in sympatry than in allopatry. In conducting such tests, it is important to control for ecological character displacement between sympatric species because ecological character divergence may strengthen prezygotic isolation as a by-product. We control for ecological character displacement by comparing mate preferences of females from a sympatric population (benthics) with mate preferences of females from two allopatric populations that most closely resemble the sympatric benthic females in ecology and morphology. No-choice mating trials indicate that sympatric benthic females mate less readily with heterospecific (limnetic) than conspecific (benthic) males, whereas two different populations of allopatric females resembling benthics show no such discrimination. These differences demonstrate reproductive character displacement of benthic female mate choice. Previous studies have established that hybridization between sympatric species occurred in the past in the wild and that hybrid offspring have lower fitness than either parental species, thus providing conditions under which natural selection would favor individuals that do not hybridize. Results are therefore consistent with the hypothesis that female mate preferences have evolved as a response to reduced hybrid fitness (reinforcement), although direct effects of sympatry or a biased extinction process could also produce the pattern. Males of the other sympatric species (limnetics) showed a preference for smaller females, in contrast to the inferred ancestral preference for larger females, suggesting reproductive character displacement of limnetic male mate preferences as well.     

THE ROLES OF LIFE‐HISTORY SELECTION AND SEXUAL SELECTION IN THE ADAPTIVE EVOLUTION OF MATING BEHAVIOR IN A BEETLE

Although there is continuing debate about whether sexual selection promotes or impedes adaptation to novel environments, the role of mating behavior in such adaptation remains largely unexplored. We investigated the evolution of mating behavior (latency to mating, mating probability and duration) in replicate populations of seed beetles Callosobruchus maculatus subjected to selection on life‐history (“Young” vs. “Old” reproduction) under contrasting regimes of sexual selection (“Monogamy” vs. “Polygamy”). Life‐history selection is predicted to favor delayed mating in “Old” females, but sexual conflict under polygamy can potentially retard adaptive life‐history evolution. We found that life‐history selection yielded the predicted changes in mating behavior, but sexual selection regime had no net effect. In within‐line crosses, populations selected for late reproduction showed equally reduced early‐life mating probability regardless of mating system. In between‐line crosses, however, the effect of life‐history selection on early‐life mating probability was stronger in polygamous lines than in monogamous ones. Thus, although mating system influenced male–female coevolution, removal of sexual selection did not affect the adaptive evolution of mating behavior. Importantly, our study shows that the interaction between sexual selection and life‐history selection can result in either increased or decreased reproductive divergence depending on the ecological context.     

SIGNALING EFFICACY DRIVES THE EVOLUTION OF LARGER SEXUAL ORNAMENTS BY SEXUAL SELECTION

Why are there so few small secondary sexual characters? Theoretical models predict that sexual selection should lead to reduction as often as exaggeration, and yet we mainly associate secondary sexual ornaments with exaggerated features such as the peacock's tail. We review the literature on mate choice experiments for evidence of reduced sexual traits. This shows that reduced ornamentation is effectively impossible in certain types of ornamental traits (behavioral, pheromonal, or color‐based traits, and morphological ornaments for which the natural selection optimum is no trait), but that there are many examples of morphological traits that would permit reduction. Yet small sexual traits are very rarely seen. We analyze a simple mathematical model of Fisher's runaway process (the null model for sexual selection). Our analysis shows that the imbalance cannot be wholly explained by larger ornaments being less costly than smaller ornaments, nor by preferences for larger ornaments being less costly than preferences for smaller ornaments. Instead, we suggest that asymmetry in signaling efficacy limits runaway to trait exaggeration.     

ON EVOLUTION UNDER SEXUAL AND VIABILITY SELECTION: A TWO-LOCUS DIPLOID MODEL

A two-locus diploid model of sexual selection is presented in which the two loci govern, respectively, a trait limited in expression in one sex (generally male) and the mating preferences of the other sex (generally female). The viability of a male depends on its genotype at the trait locus. In contrast, all females are equally viable and all individuals are equally fertile with respect to the two loci. Near fixation at both loci, evolution at the mating locus is neutral and hence a new mating preference allele will increase only through random genetic drift or through a correlated response to the increase of a new advantageous trait allele. If, however, a polymorphism is already maintained at the trait locus through overdominance in fitness then the increase of a rare preference allele depends only on the recombination rate between the loci and not on the new preference scheme.     

SINGLE FOUNDER-FLUSH EVENTS AND THE EVOLUTION OF REPRODUCTIVE ISOLATION

By demonstrating the evolution of significant premating isolation, previous laboratory experiments have provided some evidence for the founder-flush model of speciation. However, these experiments are subject to a number of criticisms, including the use of hybrid populations recently collected from the wild and the use of multiple bottlenecks. Here we present the results of a test of founder-flush speciation using a single, well-adapted laboratory stock of Drosophila melanogaster subjected to one founder-flush event. The experiment was replicated at larger scale than previous studies, and results indicate that none of 50 independent founder-flush lines evolved significant assortative mating relative to the control (base) population. This suggests a diminished emphasis on population bottlenecks in speciation of D. melanogaster and perhaps in general.     

GENETIC ARCHITECTURE AND POSTZYGOTIC REPRODUCTIVE ISOLATION: EVOLUTION OF BATESON–DOBZHANSKY–MULLER INCOMPATIBILITIES IN A POLYGENIC MODEL

The Bateson–Dobzhansky–Muller model predicts that postzygotic isolation evolves due to the accumulation of incompatible epistatic interactions, but few studies have quantified the relationship between genetic architecture and patterns of reproductive divergence. We examined how the direction and magnitude of epistatic interactions in a polygenic trait under stabilizing selection influenced the evolution of hybrid incompatibilities. We found that populations evolving independently under stabilizing selection experienced suites of compensatory allelic changes that resulted in genetic divergence between populations despite the maintenance of a stable, high‐fitness phenotype. A small number of loci were then incompatible with multiple alleles in the genetic background of the hybrid and the identity of these incompatibility loci changed over the evolution of the populations. For F₁ hybrids, reduced fitness evolved in a window of intermediate strengths of epistatic interactions, but F₂ and backcross hybrids evolved reduced fitness across weak and moderate strengths of epistasis due to segregation variance. Strong epistatic interactions constrained the allelic divergence of parental populations and prevented the development of reproductive isolation. Because many traits with varying genetic architectures must be under stabilizing selection, our results indicate that polygenetic drift is a plausible hypothesis for the evolution of postzygotic reproductive isolation.     

DISRUPTIVE SELECTION ON HABITAT PREFERENCE AND THE EVOLUTION OF REPRODUCTIVE ISOLATION: AN EXPLORATORY EXPERIMENT

A. pair of replicate experiments was carried out to examine the role of habitat specialization in the process of sympatric speciation. The rationale of the experimental design was that disruptive selection for habitat preference can facilitate the process of sympatric speciation by reducing an antagonistic interaction between the processes of recombination and selection. Replicate populations of Drosophila melanogaster were subjected to disruptive selection for habitat preference and simultaneous selection for positive assortative mating, for a period of 46 generations. The experimental protocol simulated the introduction of a frugivorous fly population into a new environment that contained a mosaic of eight equally abundant habitats. Only two habitats were suitable to the flies, and these required opposite patterns of geotaxis, phototaxis, chemotaxis, and developmental time to be successfully located. At the beginning of each generation, flies were placed as pupae into the middle of a maze containing eight discrete habitats. To produce disruptive selection on habitat preference, only those flies that chose one or the other of two selected habitats were permitted to contribute gametes to the next generation. Flies from each of the selected habitats were cultured separately to simulate independent carrying capacities within each habitat. Because flies rarely mated until they assorted themselves into the available habitats, genes affecting habitat preference pleiotropically produced assortative mating between flies with similar habitat preference. A genetic marker was used to continuously monitor the level of potential gene flow between the flies derived from the two selected habitats. During the course of the experiment, there was a gradual increase in the philopatry of the flies, indicating the development of habitat specialization. The evolution of habitat specialization resulted in substantial reproductive isolation between the subpopulations utilizing each habitat resource.     

ADAPTIVE RADIATION DRIVEN BY THE INTERPLAY OF ECO‐EVOLUTIONARY AND LANDSCAPE DYNAMICS

We investigate an individual‐based model of adaptive radiation based on the biogeographical changes of the Great African Lakes where cichlid fishes radiated. In our model, the landscape consists of a mosaic of three habitat types which may or may not be separated by geographic barriers. We study the effect of the alternation between allopatry and sympatry called landscape dynamics. We show that landscape dynamics can generate a significantly higher diversity than allopatric or sympatric speciation alone. Diversification is mainly due to the joint action of allopatric, ecological divergence, and of disruptive selection increasing assortative mating and allowing for the coexistence in sympatry of species following reinforcement or character displacement. Landscape dynamics possibly increase diversity at each landscape change. The characteristics of the radiation depend on the speed of landscape dynamics and of the number of geographically isolated regions at steady state. Under fast dynamics of a landscape with many fragments, the model predicts a high diversity, possibly subject to the temporary collapse of all species into a hybrid swarm. When fast landscape dynamics induce the recurrent fusion of several sites, diversity is moderate but very stable over time. Under slow landscape dynamics, diversification proceeds similarly, although at a slower pace.     

ARE SPECIES REAL? THE SHAPE OF THE SPECIES BOUNDARY WITH EXPONENTIAL FAILURE,REINFORCEMENT, AND THE “MISSING SNOWBALL”

Under simple assumptions, the evolution of epistatic "Dobzhansky–Muller" incompatibilities between a pair of species should yield an accelerating decline of log overall reproductive compatibility—a "snowball" effect that might rapidly provide new species with "reality." Possible alternatives include: (1) simple exponential failure, giving a linear rate of log compatibility loss, and (2) "slowdown," likely during reinforcement in which mate choice evolves to prevent deleterious hybridization, yielding a decelerating log compatibility loss. In analyses of multiple datasets, we find little support for the snowball effect, except possibly in Lepidoptera hybrid viability. The snowball predicts a slow initial rate of incompatibility acquisition, with low initial variance; instead, highly variable compatibility is almost universally observed at low genetic distances. Another deviation from predictions is that reproductive isolation usually remains incomplete until long after speciation. These results do not disprove snowball compatibility decay, but can result if large deleterious effects are due to relatively few genetic changes, or if different types of incompatibility evolve at very different rates. On the other hand, data on Bacillus and Saccharomyces , as well as theories of chromosomal evolution, suggest that some kinds of incompatibility accumulate approximately linearly, without Dobzhansky–Muller effects. In microorganisms, linearity can result from direct negative effects of DNA sequence divergence on compatibility. Finally, a decelerating slowdown model is supported for sympatric Leptasterias starfish, and in Drosophila prezygotic isolation in sympatry but not allopatry, providing novel comparative evidence for reinforcement.     

PARALLEL EVOLUTION OF LOCAL ADAPTATION AND REPRODUCTIVE ISOLATION IN THE FACE OF GENE FLOW

Parallel evolution of similar phenotypes provides strong evidence for the operation of natural selection. Where these phenotypes contribute to reproductive isolation, they further support a role for divergent, habitat‐associated selection in speciation. However, the observation of pairs of divergent ecotypes currently occupying contrasting habitats in distinct geographical regions is not sufficient to infer parallel origins. Here we show striking parallel phenotypic divergence between populations of the rocky‐shore gastropod, Littorina saxatilis, occupying contrasting habitats exposed to either wave action or crab predation. This divergence is associated with barriers to gene exchange but, nevertheless, genetic variation is more strongly structured by geography than by ecotype. Using approximate Bayesian analysis of sequence data and amplified fragment length polymorphism markers, we show that the ecotypes are likely to have arisen in the face of continuous gene flow and that the demographic separation of ecotypes has occurred in parallel at both regional and local scales. Parameter estimates suggest a long delay between colonization of a locality and ecotype formation, perhaps because the postglacial spread of crab populations was slower than the spread of snails. Adaptive differentiation may not be fully genetically independent despite being demographically parallel. These results provide new insight into a major model of ecologically driven speciation.     

ARTIFICIAL SELECTION FOR DEVELOPMENTAL TIME IN DROSOPHILA MELANOGASTER IN RELATION TO THE EVOLUTION OF AGING: DIRECT AND CORRELATED RESPONSES

A wild-type strain of Drosophila melanogaster was successfully selected for both fast and slow larval development. The realized heritabilities (h²) ranged from 0.20 to 0.30 for the fast lines and 0.35 to 0.60 for the slow lines. The selection applied is relevant in relation to the evolution of aging. The longevity of adults, either virgin or mated, was not affected by selection for developmental time, indicating that developmental time is not a causal determinant of life span, thus confirming the results of the studies on environmental effects on aging (Zwaan et al. 1991, 1992). However, adult body weights were higher in the slow developmental lines and lower in the fast lines, relative to the control flies. Furthermore, slow females showed relatively high early fecundity and low late fecundity, as compared with control and fast females. Mated longevities and total lifetime progeny productions were not statistically different. Previous results obtained by other authors from selection experiments on age at reproduction either supported the mutation accumulation or the negative pleiotropy theory of aging (Luckinbill et al. 1984; Rose 1984b). The impact of the reported results on the interpretation of these studies is discussed, and it is noted that direct selection on adult longevity is needed to settle this issue.     

THE RATE TEST OF SPECIATION: ESTIMATING THE LIKELIHOOD OF NON‐ALLOPATRIC SPECIATION FROM REPRODUCTIVE ISOLATION RATES IN DROSOPHILA

Among the most debated subjects in speciation is the question of its mode. Although allopatric (geographical) speciation is assumed the null model, the importance of parapatric and sympatric speciation is extremely difficult to assess and remains controversial. Here I develop a novel approach to distinguish these modes of speciation by studying the evolution of reproductive isolation (RI) among taxa. I focus on the Drosophila genus, for which measures of RI are known. First, I incorporate RI into age‐range correlations. Plots show that almost all cases of weak RI are between allopatric taxa whereas sympatric taxa have strong RI. This either implies that most reproductive isolation (RI) was initiated in allopatry or that RI evolves too rapidly in sympatry to be captured at incipient stages. To distinguish between these explanations, I develop a new “rate test of speciation” that estimates the likelihood of non‐allopatric speciation given the distribution of RI rates in allopatry versus sympatry. Most sympatric taxa were found to have likely initiated RI in allopatry. However, two putative candidate species pairs for non‐allopatric speciation were identified (5% of known Drosophila). In total, this study shows how using RI measures can greatly inform us about the geographical mode of speciation in nature.