On the evolution of premating isolation after a founder event

We present a new simple model for the evolution of premating reproductive isolation. Using this model we first analyze the level of genetic variability maintained by mutation in a large stable population. Then we consider the plausibility of the evolution of strong premating reproductive isolation after a founder event. We demonstrate that after a founder event a new adaptive combination of genes may rise to high frequencies in the presence of an old combination of genes. We compare the probabilities of speciation after a founder event with those in a stable population and with those when reproductive isolation is due to viability selection against hybrids. We argue that premating reproductive isolation is more efficient than postmating reproductive isolation in maintaining the integrity of sympatric species. This might have contributed to the pattern of stronger premating isolation than postmating isolation between closely related pairs of sympatric species.     

Review. Specificity in pollination and consequences for postmating reproductive isolation in deceptive Mediterranean orchids

The type of reproductive isolation prevalent in the initial stages of species divergence can affect the nature and rate of emergence of additional reproductive barriers that subsequently strengthen isolation between species. Different groups of Mediterranean deceptive orchids are characterized by different levels of pollinator specificity. Whereas food-deceptive orchid species show weak pollinator specificity, the sexually deceptive Ophrys species display a more specialized pollination strategy. Comparative analyses reveal that orchids with high pollinator specificity mostly rely on premating reproductive barriers and have very little postmating isolation. In this group, a shift to a novel pollinator achieved by modifying the odour bouquet may represent the main isolation mechanism involved in speciation. By contrast, orchids with weak premating isolation, such as generalized food-deceptive orchids, show strong evidence for intrinsic postmating reproductive barriers, particularly for late-acting postzygotic barriers such as hybrid sterility. In such species, chromosomal differences may have played a key role in species isolation, although strong postmating-prezygotic isolation has also evolved in these orchids. Molecular analyses of hybrid zones indicate that the types and strength of reproductive barriers in deceptive orchids with contrasting premating isolation mechanisms directly affect the rate and evolutionary consequences of hybridization and the nature of species differentiation.     

Sexual selection and natural selection in bird speciation

The role of sexual selection in speciation is investigated, addressing two main issues. First, how do sexually selected traits become species recognition traits? Theory and empirical evidence suggest that female preferences often do not evolve as a correlated response to evolution of male traits. This implies that, contrary to runaway (Fisherian) models of sexual selection, premating isolation will not arise as an automatic side effect of divergence between populations in sexually selected traits. I evaluate premating isolating mechanisms in one group, the birds. In this group premating isolation is often a consequence of sexual imprinting, whereby young birds learn features of their parents and use these features in mate choice. Song, morphology and plumage are known recognition cues. I conclude that perhaps the main role for sexual selection in speciation is in generating differences between populations in traits. Sexual imprinting then leads to these traits being used as species recognition mechanisms. The second issue addressed in this paper is the role of sexual selection in adaptive radiation, again concentrating on birds. Ecological differences between species include large differences in size, which may in themselves be sufficient for species recognition, and differences in habitat, which seem to evolve frequently and at all stages of an adaptive radiation. Differences in habitat often cause song and plumage patterns to evolve as a result of sexual selection for efficient communication. Therefore sexual selection is likely to have an important role in generating premating isolating mechanisms throughout an adaptive radiation. It is also possible that sexual selection, by creating more allopatric species, creates more opportunity for ecological divergence to occur. The limited available evidence does not support this idea. A role for sexual selection in accelerating ecological diversification has yet to be demonstrated.     

Reproductive isolation caused by visual predation on migrants between divergent environments

In theory, natural selection can drive adaptation within species while simultaneously promoting the formation of new species by causing the evolution of reproductive isolation. Cryptic coloration is widespread in nature and is generally considered to be a clear visual example of adaptation. I provide evidence that population divergence in cryptic coloration can also cause reproductive isolation. First, a manipulative field experiment using walking-stick insects demonstrates that the relative survival of different colour-pattern morphs depends on the host-plant species on which they are resting, but only in the presence of avian predation. Second, natural populations adapted to different host plants have diverged in colour-pattern-morph frequencies such that between-host migrants are more likely to be the locally less-cryptic morph than are residents. Collectively, these data indicate that high rates of visual predation on less-cryptic migrants are likely to reduce encounters, and thus interbreeding, between host-associated populations. Comparison with previous estimates of sexual isolation reveals that the contribution of selection against between-host migrants to total premating isolation is as strong as, or stronger than, that of sexual isolation. These findings highlight the potential role of natural selection against migrants between divergent environments in the formation of new species.     

The evolution of premating isolation: local adaptation and natural and sexual selection against hybrids

Although reinforcement is ostensibly driven by selection against hybrids, there are often other components in empirical cases and theoretical models of reinforcement that may contribute to premating isolation. One of these components is local adaptation of a trait used in mate choice. I use several different comparisons to assess the roles that local adaptation and selection against hybrids may play in reinforcement models. Both numerical simulations of exact recursion equations and analytical weak selection approximations are employed. I find that selection against hybrids may play a small role in driving preference evolution in a reinforcement model where the mating cue is separate from loci causing hybrid incompatibilities. When females have preferences directly for purebreds of their own population, however, selection against hybrids can play a large role in premating isolation evolution. I present some situations in which this type of selection is likely to exist. This work also illustrates shortfalls of using a weak selection approach to address questions about reinforcement.     

Evolution of reproductive isolation in plants

Reproductive isolation is essential for the process of speciation and much has been learned in recent years about the ecology and underlying genetics of reproductive barriers. But plant species are typically isolated not by a single factor, but by a large number of different pre- and postzygotic barriers, and their potentially complex interactions. This phenomenon has often been ignored to date. Recent studies of the relative importance of different isolating barriers between plant species pairs concluded that prezygotic isolation is much stronger than postzygotic isolation. But studies of the patterns of reproductive isolation in plants did not find that prezygotic isolation evolves faster than postzygotic isolation, in contrast to most animals. This may be due to the multiple premating barriers that isolate most species pairs, some of which may be controlled by few genes of major effect and evolve rapidly, whereas others have a complex genetic architecture and evolve more slowly. Intrinsic postzygotic isolation in plants is correlated with genetic divergence, but some instrinsic postzygotic barriers evolve rapidly and are polymorphic within species. Extrinsic postzygotic barriers are rarely included in estimates of different components of reproductive isolation. Much remains to be learned about ecological and molecular interactions among isolating barriers. The role of reinforcement and reproductive character displacement in the evolution of premating barriers is an open topic that deserves further study. At the molecular level, chromosomal and genic isolation factors may be associated and act in concert to mediate reproductive isolation, but their interactions are only starting to be explored.     

Models of Evolution of Reproductive Isolation

Mathematical models are presented for the evolution of postmating and premating reproductive isolation. In the case of postmating isolation it is assumed that hybrid sterility or inviability is caused by incompatibility of alleles at one or two loci, and evolution of reproductive isolation occurs by random fixation of different incompatibility alleles in different populations. Mutations are assumed to occur following either the stepwise mutation model or the infinite-allele model. Computer simulations by using It?'s stochastic differential equations have shown that in the model used the reproductive isolation mechanism evolves faster in small populations than in large populations when the mutation rate remains the same. In populations of a given size it evolves faster when the number of loci involved is large than when this is small. In general, however, evolution of isolation mechanisms is a very slow process, and it would take thousands to millions of generations if the mutation rate is of the order of 10(-5) per generation. Since gene substitution occurs as a stochastic process, the time required for the establishment of reproductive isolation has a large variance. Although the average time of evolution of isolation mechanisms is very long, substitution of incompatibility genes in a population occurs rather quickly once it starts. The intrapopulational fertility or viability is always very high. In the model of premating isolation it is assumed that mating preference or compatibility is determined by male- and female-limited characters, each of which is controlled by a single locus with multiple alleles, and mating occurs only when the male and female characters are compatible with each other. Computer simulations have shown that the dynamics of evolution of premating isolation mechanism is very similar to that of postmating isolation mechanism, and the mean and variance of the time required for establishment of premating isolation are very large. Theoretical predictions obtained from the present study about the speed of evolution of reproductive isolation are consistent with empirical data available from vertebrate organisms.     

TROPICS ACCELERATE THE EVOLUTION OF HYBRID MALE STERILITY IN DROSOPHILA

Understanding the evolutionary mechanisms that facilitate speciation and explain global patterns of species diversity has remained a challenge for decades. The most general pattern of species biodiversity is the latitudinal gradient, whereby species richness increases toward the tropics. Although such a global pattern probably has a multitude of causes, recent attention has focused on the hypothesis that speciation and the evolution of reproductive isolation occur faster in the tropics. Here, I tested this prediction using a dataset on premating and postzygotic isolation between recently diverged Drosophila species. Results showed that while the evolution of premating isolation was not greater between tropical Drosophila relative to nontropical species, postzygotic isolation evolved faster in the tropics. In particular, hybrid male sterility was much greater among tropical Drosophila compared to nontropical species pairs of similar genetic age. Several testable explanations for the novel pattern are discussed, including greater role for sterility‐inducing bacterial endosymbionts in the tropics and more intense sperm–sperm competition or sperm–egg sexual conflict in the tropics. The results imply that processes of speciation in the tropics may evolve at different rates or may even be somewhat different from those at higher latitudes.     

Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. IV. Correlated responses in behavioral isolation to artificial selection on a life-history trait

Abstract Studies of behavioral isolation among geographically isolated populations of Drosophila mojavensis have provided an understanding of incipient speciation wherein phylogeny and ecology play a prominent role. Populations of D. mojavensis in mainland Mexico and southern Arizona exhibit low but significant premating isolation from Baja California populations in laboratory mate choice tests. These same populations have undergone considerable life-history evolution in response to use of different host plants, suggesting that behavioral isolation between populations is a pleiotropic consequence of adaptation to different environments, or Mayr's geographic speciation hypothesis. This hypothesis was tested using bidirectional artificial selection on egg-to-adult development time in replicate lines of a mainland and Baja population cultured on two host cacti for 13 generations. Response to selection was greatest in the slow lines cultured on one host, yet there was uneven response in some lines due to variation in cactus tissue quality. Realized heritabilities for development time ranged from 0.04 to 0.16, which is consistent with previous estimates from half-sib/full-sib analyses of genetic variation. In most lines that responded to selection, premating isolation decreased to near zero. Correlated responses in behavioral isolation suggest that adaptation to contrasting environments can cause secondary responses in mate recognition systems that can influence the formation of new species.     

Reproductive character displacement and speciation in periodical cicadas, with description of new species, 13-year Magicicada neotredecem

Abstract. Acoustic mate-attracting signals of related sympatric, synchronic species are always distinguishable, but those of related allopatric species sometimes are not, thus suggesting that such signals may evolve to "reinforce" premating species isolation when similar species become sympatric. This hypothesis predicts divergences restricted to regions of sympatry in partially overlapping species, but such "reproductive character displacement" has rarely been confirmed. We report such a case in the acoustic signals of a previously unrecognized 13-year periodical cicada species, Magicicada neotredecim , described here as a new species (see Appendix). Where M. neotredecim overlaps M. tredecim in the central United States, the dominant male call pitch (frequency) of M. neotredecim increases from approximately 1.4 kHz to 1.7 kHz, whereas that of M. tredecim remains comparatively stable. The average preferences of female M. neotredecim for call pitch show a similar geographic pattern, changing with the call pitch of conspecific males. Magicicada neotredecim differs from 13-year M. tredecim in abdomen coloration, mitochondrial DNA, and call pitch, but is not consistently distinguishable from 17-year M. septendecim ; thus, like other Magicicada species, M. neotredecim appears most closely related to a geographically adjacent counterpart with the alternative life cycle. Speciation in Magicicada may be facilitated by life-cycle changes that create temporal isolation, and reinforcement could play a role by fostering divergence in premating signals prior to speciation. We present two theories of Magicicada speciation by life-cycle evolution: "nurse-brood facilitation" and "life-cycle canalization."     

Ecological character displacement caused by reproductive interference

We carried out a theoretical investigation of whether ecological character displacement can be caused by reproductive interference. Our model assumes that a quantitative character is associated with both resource use and species recognition, and that heterospecific mating incurs costs. The model shows that ecological character displacement can occur as a consequence of evolution of premating isolation; this conclusion is based on the premise that resource competition is less intense between species than within species and that the ecological character also contributes to premating isolation. When resource competition between species is intense, extinction of either species may occur by competitive exclusion before ecological character divergence. Some observational studies have shown that character displacement in body size is associated with not only resources use but also species recognition. We propose that body size displacement can occur as a consequence of evolution of premating isolation. Our results suggest that ecological character displacement results from reproductive character displacement.     

Evidence for no sexual isolation between Drosophila albomicans and D. nasuta

Sexual isolation, the reduced tendency to mate, is one of the reproductive barriers that prevent gene flow between different species. Various species‐specific signals during courtship contribute to sexual isolation between species. Drosophila albomicans and D. nasuta are closely related species of the nasuta subgroup within the Drosophila immigrans group and are distributed in allopatry. We analyzed mating behavior and courtship as well as cuticular hydrocarbon profiles within and between species. Here, we report that these two species randomly mated with each other. We did not observe any sexual isolation between species or between strains within species by multiple‐choice tests. Significant difference in the courtship index was detected between these two species, but males and females of both species showed no discrimination against heterospecific partners. Significant quantitative variations in cuticular hydrocarbons between these two species were also found, but the cuticular hydrocarbons appear to play a negligible role in both courtship and sexual isolation between these two species. In contrast to the evident postzygotic isolation, the lack of sexual isolation between these two species suggests that the evolution of premating isolation may lag behind that of the intergenomic incompatibility, which might be driven by intragenomic conflicts.     

Existence of a pattern of reproductive character displacement in Homobasidiomycota but not in Ascomycota

Generally, stronger reproductive isolation is expected between sympatric than between allopatric sibling species. Such reproductive character displacement should predominantly affect premating reproductive isolation and can be due to several mechanisms, including population extinction, fusion of insufficiently isolated incipient species and reinforcement of reproductive isolation in response to low hybrid fitness. Experimental data on several taxa have confirmed these theoretical expectations on reproductive character displacement, but they are restricted to animals and a few plants. Using results reported in the literature on crossing experiments in fungi, we compared the degree and the nature of reproductive isolation between allopatric and sympatric species pairs. In accordance with theoretical expectations, we found a pattern of enhanced premating isolation among sympatric sibling species in Homobasidiomycota. By contrast, we did not find evidence for reproductive character displacement in Ascomycota at similar genetic distances. Both allopatric and sympatric species of Ascomycota had similarly low levels of reproductive isolation, being mostly post-zygotic. This suggests that some phylogeny-dependent life-history trait may strongly influence the evolution of reproductive isolation between closely related species. A significant correlation was found between degree of reproductive isolation and genetic divergence among allopatric species of Homobasidiomycota, but not among sympatric ones or among Ascomycota species.     

Cultural isolation is greater than genetic isolation across an avian hybrid zone

Elucidating the relationship between genetic and cultural evolution is important in understanding speciation, as learned premating barriers might be involved in maintaining species differences. Here, we test this relationship by examining a widely recognized premating barrier, bird song, in a hybrid zone between black‐throated green (Setophaga virens) and Townsend's warblers (S. townsendi). We use song analysis, genomic techniques and playback experiments to characterize the cultural and genetic backgrounds of individuals in this region, expecting that if song is an important reproductive barrier between these species, there should be a strong relationship between song and genotype. We show that songs in the hybrid zone correspond to the distinctly different songs found in allopatry but that song and genotype are not tightly coupled in sympatry. Allopatric individuals responded only to local songs, indicating that individuals may have learned to respond to songs they commonly hear. We observed discordance between song and genotype clines; a narrower cline suggests that cultural selection on song is stronger than natural selection on genotype. These findings indicate that song is unlikely to play a role in reproductive isolation between these species, and we suggest that spatial variation in song may nonetheless be maintained by frequency‐dependent cultural selection. This decoupling of genes and culture may contribute to hybridization in this region.     

Do allopatric male Calopteryx virgo damselflies learn species recognition?

There is a growing amount of empirical evidence that premating reproductive isolation of two closely related species can be reinforced by natural selection arising from avoidance of maladaptive hybridization. However, as an alternative for this popular reinforcement theory, it has been suggested that learning to prefer conspecifics or to discriminate heterospecifics could cause a similar pattern of reinforced premating isolation, but this possibility is much less studied. Here, we report results of a field experiment in which we examined (i) whether allopatric Calopteryx virgo damselfly males that have not encountered heterospecific females of the congener C. splendens initially show discrimination, and (ii) whether C. virgo males learn to discriminate heterospecifics or learn to associate with conspecifics during repeated experimental presentation of females. Our experiment revealed that there was a statistically nonsignificant tendency for C. virgo males to show initial discrimination against heterospecific females but because we did not use sexually naïve individuals in our experiment, we were not able to separate the effect of innate or associative learning. More importantly, however, our study revealed that species discrimination might be further strengthened by learning, especially so that C. virgo males increase their association with conspecific females during repeated presentation trials. The role of learning to discriminate C. splendens females was less clear. We conclude that learning might play a role in species recognition also when individuals are not naïve but have already encountered potential conspecific mates.     

BEYOND REINFORCEMENT: THE EVOLUTION OF PREMATING ISOLATION BY DIRECT SELECTION ON PREFERENCES AND POSTMATING, PREZYGOTIC INCOMPATIBILITIES

Abstract The evolution of premating isolation after secondary contact is primarily considered in the guise of reinforcement, which relies on low hybrid fitness as the driving force for mating preference divergence. Here I consider two additional forces that may play a substantial role in the adaptive evolution of premating isolation, direct selection on preferences and indirect selection against postmating, prezygotic incompatibilities. First, I argue that a combination of ecological character displacement and sensory bias can cause direct selection on preferences that results in the pattern of reproductive character displacement. Both analytical and numerical methods are then used to demonstrate that, as expected from work in single populations, such direct selection will easily overwhelm indirect selection due to low hybrid fitness as the primary determinant of preference evolution. Second, postmating, prezygotic incompatibilities are presented as a driving force in the evolution of premating isolation. Two classes of these mechanisms, those increasing female mortality after mating but before producing offspring and those reducing female fertility, are shown to be identical in their effects on preference divergence. Analytical and numerical techniques are then used to demonstrate that postmating, prezygotic factors may place strong selection on preference divergence. These selective forces are shown to be comparable if not greater than those produced by the low fitness of hybrids.     

Divergence and reproductive isolation in the early stages of speciation

To understand speciation we need to identify the factors causing divergence between natural populations. The traditional approach to gaining such insights has been to focus on a particular theory and ask whether observed patterns of reproductive isolation between populations or species are consistent with the hypothesis in question. However, such studies are few and they do not allow us to compare between hypotheses, so often we cannot determine the relative contribution to divergence of different potential factors. Here, I describe a study of patterns of phenotypic divergence and premating and postmating isolation between populations of the grasshopper Chorthippus parallelus. Information on the phylogeographic relationships of the populations means that a priori predictions from existing hypotheses for the evolution of reproductive isolation can be compared with observations. I assess the relative contributions to premating isolation, postmating isolation and phenotypic divergence of long periods of allopatry, adaptation to different environments and processes associated with colonisation (such as population bottlenecks). Likelihood analysis reveals that long periods of allopatry in glacial refugia are associated with postmating reproductive isolation, but not premating isolation, which is more strongly associated with colonisation. Neither premating nor postmating isolation is higher between populations differing in potential environmental selection pressures. There are only weak correlations between patterns of genetic divergence and phenotypic divergence and no correlation between premating and postmating isolation. This suggests that the potential of a taxon to exercise mate choice may affect the types of factor that promote speciation in that group. I discuss the advantages and disadvantages of the general approach of simultaneously testing competing hypotheses for the evolution of reproductive isolation.     

Phenotypic divergence but not genetic distance predicts assortative mating among species of a cichlid fish radiation

The hypothesis of ecological divergence giving rise to premating isolation in the face of gene flow is controversial. However, this may be an important mechanism to explain the rapid multiplication of species during adaptive radiation following the colonization of a new environment when geographical barriers to gene flow are largely absent but underutilized niche space is abundant. Using cichlid fish, we tested the prediction of ecological speciation that the strength of premating isolation among species is predicted by phenotypic rather than genetic distance. We conducted mate choice experiments between three closely related, sympatric species of a recent radiation in Lake Mweru (Zambia/DRC) that differ in habitat use and phenotype, and a distantly related population from Lake Bangweulu that resembles one of the species in Lake Mweru. We found significant assortative mating among all closely related, sympatric species that differed phenotypically, but none between the distantly related allopatric populations of more similar phenotype. Phenotypic distance between species was a good predictor of the strength of premating isolation, suggesting that assortative mating can evolve rapidly in association with ecological divergence during adaptive radiation. Our data also reveals that distantly related allopatric populations that have not diverged phenotypically, may hybridize when coming into secondary contact, e.g. upon river capture because of diversion of drainage systems.     

Mechanical reproductive isolation via divergent genital morphology between Carabus insulicola and C. esakii with implications in species coexistence

The mechanical isolation hypothesis predicts that physical incompatibility between divergent reproductive morphologies hinders hybridization between populations. However, evidence for this hypothesis remains scarce. We examined this hypothesis using two parapatric carabid beetles, Carabus insulicola and C. esakii, which are of the subgenus Ohomopterus and exhibit a species-specific genital lock-and-key system. Our interspecific crossing experiment revealed that incompatibility of genital morphologies served as a strong postmating-prezygotic isolation barrier. This isolation was asymmetric: a decrease in female fitness was more costly in the cross with greater genitalic incompatibility between a C. esakii female and a C. insulicola male. These two species share a limited sympatric area, but the mechanism responsible for their coexistence is unclear given no evidence of premating isolation via male mate choice. A comparison of the present results with those of previous studies that quantified reproductive isolation between Ohomopterus species suggest that strong mechanical isolation via genitalic incompatibility plays a major role in species isolation, but that it may be less important in species coexistence.     

Reinforcement and the genetics of nonrandom mating

Abstract.— The occurrence of reinforcement is compared when premating isolation is caused by the spread of a gene causing females to prefer to mate with males carrying a population-specific trait (a "preference" model) and by a gene that causes females to prefer to mate with males that share their own trait phenotype (an "assortative mating" model). Both two-island models, which have symmetric gene flow, and continent-island models, which have one-way gene flow, are explored. Reinforcement is found to occur much more easily in a two-island assortative mating model than in any of the other three models. This is due primarily to the fact that in this model the assortative mating allele will automatically become genetically associated in each population with the trait allele that is favored by natural selection on that island. In contrast, natural selection on the trait both favors and opposes the evolution of premating isolation in the two-island preference model, depending on the particular population. These results imply that species recognition in the context of mating may evolve particularly easily when it targets cues that are favored by natural selection in each population. In the continent-island models, reinforcement is found to occur more often under the preference model than the assortative mating model, thus reversing the trend from the two-island models. Patterns of population subdivision may therefore play a role in determining what types of premating isolation may evolve.