Sympatric speciation by sexual selection alone is unlikely

According to Darwin, sympatric speciation is driven by disruptive, frequency-dependent natural selection caused by competition for diverse resources. Recently, several authors have argued that disruptive sexual selection can also cause sympatric speciation. Here, we use hypergeometric phenotypic and individual-based genotypic models to explore sympatric speciation by sexual selection under a broad range of conditions. If variabilities of preference and display traits are each caused by more than one or two polymorphic loci, sympatric speciation requires rather strong sexual selection when females exert preferences for extreme male phenotypes. Under this kind of mate choice, speciation can occur only if initial distributions of preference and display are close to symmetric. Otherwise, the population rapidly loses variability. Thus, unless allele replacements at very few loci are enough for reproductive isolation, female preferences for extreme male displays are unlikely to drive sympatric speciation. By contrast, similarity-based female preferences that do not cause sexual selection are less destabilizing to the maintenance of genetic variability and may result in sympatric speciation across a broader range of initial conditions. Certain groups of African cichlids have served as the exclusive motivation for the hypothesis of sympatric speciation by sexual selection. Mate choice in these fishes appears to be driven by female preferences for extreme male phenotypes rather than similarity-based preferences, and the evolution of premating reproductive isolation commonly involves at least several genes. Therefore, differences in female preferences and male display in cichlids and other species of sympatric origin are more likely to have evolved as isolating mechanisms under disruptive natural selection.     

Does competitive divergence occur if assortative mating is costly?

Most models of sympatric speciation have assumed that assortative mating has no costs. A few studies, however, have shown that the costs for being choosy can prevent such speciation. Here, we investigate the role of the strength of assortment and of the costs for being choosy for a simple genetic model of a single ('magic') trait that mediates both intraspecific competition for a continuum of resources and assortative mating, which is induced by choosy females who preferentially mate with males of similar phenotype. Choosiness may be costly if it is difficult to find a mating partner. Such magic trait models are considered to be most conducive of sympatric speciation. We consider a sexually reproducing population of haploid individuals that is density regulated. The trait is determined by a single locus with multiple alleles. The strength of stabilizing selection (caused by a unimodal resource distribution), the strength of competition, the degree of assortment and the costs for being choosy are independent parameters. We investigate analytically and numerically how these parameters determine the equilibrium and stability structure. In particular, we identify conditions under which no polymorphism at all is maintained as well as conditions under which strong competitive divergence occurs, or the population even splits into two reproductively isolated classes of highly diverse phenotypes. If costs are absent or moderate, genetic variability tends to be minimized at intermediate strengths of assortment, and reproductively isolated classes of phenotypes are a likely result of evolution only for intermediate or strong competition and for very strong assortment. The likelihood of divergence depends relatively weakly on the costs as long as they are not high. With high costs, however, increasingly strong assortment rapidly depletes all genetic variation, and strong competitive divergence is prevented.     

Sexual selection's impacts on ecological specialization: an experimental test

In many species, individuals specialize on different resources, thereby reducing competition. Such ecological specialization can promote the evolution of alternative ecomorphs—distinct phenotypes adapted for particular resources. Elucidating whether and how this process is influenced by sexual selection is crucial for understanding how ecological specialization promotes the evolution of novel traits and, potentially, speciation between ecomorphs. We evaluated the population-level effects of sexual selection (as mediated by mate choice) on ecological specialization in spadefoot toad tadpoles that express alternative ecomorphs. We manipulated whether sexual selection was present or reversed by mating females to their preferred versus non-preferred males, respectively. We then exposed their tadpoles to resource competition in experimental mesocosms. The resulting distribution of ecomorphs was similar between treatments, but sexual selection generated poorer trait integration in, and lower fitness of, the more specialized carnivore morph. Moreover, disruptive and directional natural selection were weaker in the sexual selection present treatment. Nevertheless, this effect on disruptive selection was smaller than previously documented effects of ecological opportunity and competitor density. Thus, sexual selection can inhibit adaptation to resource competition and thereby hinder ecological specialization, particularly when females obtain fitness benefits from mate choice that offset the cost of producing competitively inferior offspring.     

Male-male competition and speciation: aggression bias towards differently coloured rivals varies between stages of speciation in a Lake Victoria cichlid species complex

Sympatric speciation driven by sexual selection by female mate choice on a male trait is a much debated topic. The process is problematic because of the lack of negative frequency-dependent selection that can facilitate the invasion of a novel colour phenotype and stabilize trait polymorphism. It has recently been proposed that male-male competition for mating territories can generate frequency-dependent selection on male colouration. Rare male cichlid fish would enjoy a fitness advantage if territorial defenders bias aggression towards male cichlid fish of their own colour. We used blue (ancestral type) and red phenotypes of the Lake Victoria cichlid species complex Pundamilia. We tested the aggression bias of wild-caught territorial blue male cichlid fish from five separate populations for blue vs. red rival male cichlid fish using simulated intruder choice tests. The different populations vary in the frequency of red male cichlid fish, and in the degree of reproductive isolation between red and blue, reflecting different stages of speciation. Blue male cichlid fish from a population that lack red phenotypes biased aggression towards blue stimulus male cichlid fish. The same was found in two populations where blue and red are reproductively isolated sister species. This aggression bias may facilitate the invasion of a novel colour phenotype and species coexistence. Blue male cichlid fish from two populations where red and blue are hybridizing incipient species biased aggression towards red stimulus male cichlid fish. Thus, after a successful invasion of red, aggression bias alone is not likely to generate frequency dependence required to stabilize the coexistence of phenotypes. The findings show that aggression bias varies between stages of speciation, but is not enough to stabilize the process of speciation.     

The genetic basis for fruit odor discrimination in Rhagoletis flies and its significance for sympatric host shifts

Rhagoletis pomonella (Diptera: Tephritidae) use volatile compounds emitted from the surface of ripening fruit as important chemosensory cues for recognizing and distinguishing among alternative host plants. Host choice is of evolutionary significance in Rhagoletis because these flies mate on or near the fruit of their respective host plants. Differences in host choice based on fruit odor discrimination therefore result in differential mate choice and prezygotic reproductive isolation, facilitating sympatric speciation in the absence of geographic isolation. We test for a genetic basis for host fruit odor discrimination through an analysis of F2 and backcross hybrids constructed between apple-, hawthorn-, and flowering dogwood-infesting Rhagoletis flies. We recovered a significant proportion (30-65%) of parental apple, hawthorn, and dogwood fly response phenotypes in F2 hybrids, despite the general failure of F1 hybrids to reach odor source spheres. Segregation patterns in F2 and backcross hybrids suggest that only a modest number of allelic differences at a few loci may underlie host fruit odor discrimination. In addition, a strong bias was observed for F2 and backcross flies to orient to the natal fruit blend of their maternal grandmother, implying the existence of cytonuclear gene interactions. We explore the implications of our findings for the evolutionary dynamics of sympatric host race formation and speciation.     

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.     

Patterns of speciation in endemic Mexican Goodeid fish: sexual conflict or early radiation?

Currently there is much interest in the potential for sexual selection or conflict to drive speciation. Theory proposes that speciation will be accelerated where sexual conflict is strong, particularly if females are ahead because mate choice will accentuate divergence by limiting gene flow. The Goodeinae are a monophyletic group of endemic Mexican fishes with an origin at least as old as the Miocene. Sexual selection is important in the Goodeinae and there is substantial interspecific variability in body morphology, which influences mate choice, allowing inference of the importance of female mate choice. We therefore used this group to test the relationship between sexual dimorphism and speciation rate. We quantified interspecific variation in sexual dimorphism amongst 25 species using a multivariate measure of total morphological differentiation between the sexes that accurately reflects sexual dimorphism driven by female mate choice and also used a mtDNA-based phylogeny to examine speciation rates. Comparative analyses failed to support a significant association between sexual dimorphism and speciation rate. In addition, variation in the time course of speciation throughout the whole clade was also examined using a similar tree containing 34 extant species. A constant rates model for the growth of this clade was rejected, but analyses instead indicated a decline in the rate of speciation over time. These results support the hypothesis of an early expansion of the group, perhaps due to an early radiation influenced by the key innovation of live bearing, or the prevalence of Miocene volcanism. In general, support for the role of sexual selection in generating patterns of speciation is proving equivocal and we argue that vicariance biogeography and adaptive radiations remain the most likely determinants of major patterns of diversification of continental organisms.     

Competitive environments induce shifts in host fidelity

Recent models support the idea of sympatric speciation as a result of the joint effects of disruptive selection and assortative mating. We present experimental data, testing models of speciation through frequency‐dependent selection. We show that under high competition on a mixture of resources/hosts, strains of the Seed beetle, Callosobruchus maculatus, change their host fidelity and evolve a more generalistic behaviour in resource utilization among females. The change in host fidelity did not result in disruptive selection and was not followed by assortative mating. This means that only one of three fundamental prerequisites for sympatric speciation evolved as a result of the frequency‐dependent selection. We conclude that for this process to work, a shift to a novel food resource as a result of selection must also lead to a loss of preference for the original resource such that individuals are only able to use either one of the two.     

Female mate-choice behavior and sympatric speciation

Many models have investigated how the process of speciation may occur in sympatry. In these models, individuals are either asexual or mate choice is determined by very simple rules. Females, for example, may be assumed either to compare their phenotype to that of a potential mate, preferring to mate with similar males (phenotype matching), or to possess preference genes that determine which male phenotype they prefer. These rules often do not reflect the mate-choice rules found in empirical studies. In this paper, we compare these two modes of female choice with various types of sexual imprinting. We examine the efficacy of different mate-choice behavior in causing divergence in male traits under simple deterministic one-locus population genetic models as well as under polygenic, individual-based simulations based on the models of Dieckmann and Doebeli (1999). We find that the inheritance mechanism of mate choice can have a large effect on the ease of sympatric speciation. When females imprint on their mothers, the result of the model is similar to phenotype matching, where speciation can occur fairly easily. When females imprint on their fathers or imprint obliquely, speciation becomes considerably less likely. Finally, when females rely on preference genes, male trait evolution occurs easily, but the correlation between trait and preference can be weak, and interpreting these results as speciation may be suspect.     

被子植物同域物种形成研究进展

同域物种形成是指在缺少地理隔离的情况下分化出新种,相比异域物种形成更为罕见,存在较多的研究空白.该文分析了近十年来与被子植物同域物种形成相关的国内外研究,着重论述同域物种形成的影响因素和种对间的生殖隔离.考虑到历史上的地理隔离难以确定,加之种对间亲缘关系很近,同域物种的判定容易引发争议.其成因可分为生态因素和突变因素:...     

Host choice promotes reproductive isolation between host races of the larch budmoth Zeiraphera diniana

The chances for sympatric speciation are improved if ecological divergence leads to assortative mating as a by-product. This effect is known in parasites that find mates using host cues, but studies of larch- and pine-feeding races of the larch budmoth (Zeiraphera diniana, Lepidoptera: Tortricidae) suggest it may also occur when mate attraction is via sex pheromones that are independent of habitat. We have previously shown that females releasing pheromones on or near their own host attract more males of their own race than if placed on the alternative host. This host effect would enhance assortative mating provided adults preferentially alight on their native hosts. Here we investigate alighting preferences in natural mixed forest using a novel likelihood analysis of genotypic clusters based on three semidiagnostic allozyme loci. Both larch and pine females show a realized alighting preference for their own host of 86%. The equivalent preferences of males were 79% for the larch race and 85% for the pine race. These preferences are also detectable in small-scale laboratory experiments, where alighting preferences of larch and pine races towards their own hosts were, respectively, 67 and 66% in females and 69 and 63% in males. Pure larch race moths reared in the laboratory had alighting choice similar to moths from natural populations, while hybrids were intermediate, showing that alighting preferences were heritable and approximately additive. The field estimates of alighting preference, coupled with earlier work on mate choice, yield an estimated rate of natural hybridization between sympatric host races of 2.2-3.8% per generation. Divergent alighting choice enhances pheromone-mediated assortative mating today, and is likely to have been an important cause of assortative mating during initial divergence in host use. Because resources are normally 'coarse-grained' in space and time, assortative mating due to ecological divergence may be a more important catalyst of sympatric speciation than generally realized.     

The interaction of resource use and gene flow on the phenotypic divergence of benthic and pelagic morphs of Icelandic Arctic charr (Salvelinus alpinus)

Conceptual models of adaptive divergence and ecological speciation in sympatry predict differential resource use, phenotype–environment correlations, and reduced gene flow among diverging phenotypes. While these predictions have been assessed in past studies, connections among them have rarely been assessed collectively. We examined relationships among phenotypic, ecological, and genetic variation in Arctic charr (Salvelinus alpinus) from six Icelandic localities that have undergone varying degrees of divergence into sympatric benthic and pelagic morphs. We characterized morphological variation with geometric morphometrics, tested for differential resource use between morphs using stable isotopes, and inferred the amount of gene flow from single nucleotide polymorphisms. Analysis of stable isotopic signatures indicated that sympatric morphs showed similar difference in resource use across populations, likely arising from the common utilization of niche space within each population. Carbon isotopic signature was also a significant predictor of individual variation in body shape and size, suggesting that variation in benthic and pelagic resource use is associated with phenotypic variation. The estimated percentage of hybrids between sympatric morphs varied across populations (from 0% to 15.6%) but the majority of fish had genotypes (ancestry coefficients) characteristic of pure morphs. Despite evidence of reduced gene flow between sympatric morphs, we did not detect the expected negative relationship between divergence in resource use and gene flow. Three lakes showed the expected pattern, but morphs in the fourth showed no detectable hybridization and had relatively low differences in resource use between them. This coupled with the finding that resource use and genetic differentiation had differential effects on body shape variation across populations suggests that reproductive isolation maintains phenotypic divergence between benthic and pelagic morphs when the effects of resource use are relatively low. Our ability to assess relationships between phenotype, ecology, and genetics deepens our understanding of the processes underlying adaptive divergence in sympatry.     

The genetics and ecology of sympatric speciation: A case study

Mating occurs on the larval host plant in allRhagoletis species (Diptera: Tephritidae). We show how this attribute, when coupled with certain differences in other biological traits, strongly influences the mode of speciation. In species of thesuavis species group, host shifts have never occurred during speciation, and larvae feed in the husks of any walnut species(Juglans spp.), which are highly toxic. Taxa are allopatric or parapatric and exhibit deep phylogenetic nodes suggesting relatively ancient speciation events. Traits responsible for species and mate recognition, particularly in parapatric species, are morphologically distinct and strongly sexually dimorphic. All aspects of their biology, genetics and distribution are consistent with a slow rate of allopatric speciation followed by morphological divergence in secondary contact. In contrast, speciation in thepomonella species group has always involved a shift to a new, usually unrelated, non-toxic host, and all taxa within these groups are sympatric, monophagous and morphologically indistinguishable from one another. Phylogenetic nodes are very shallow, indicating recent sympatric speciation. Sympatric divergence is promoted by genetic variation which allows a portion of the original species to shift to a new habitat or host. Evidence suggests that changes in a few key loci responsible for host selection and fitness on a new host may initiate host shifts. By exploiting different habitats, competition for resources between diverging populations is reduced or avoided. We provide evidence that in phytophagous and parasitic insects sufficient intrinsic barriers to gene flow can evolve between sister populations as they adapt to different habitats or hosts to allow each population to establish independent evolutionary lineages in sympatry.     

Combining Biogeographic and Phylogenetic Data to Examine Primate Speciation: An Example Using Cercopithecin Monkeys

We combined phylogenetic and biogeographic data to examine the mode of speciation in a group of African monkeys, the Cercopithecini. If allopatric speciation is the major force producing species, then there should be a positive relationship between the relative divergence time of taxa and their degree of geographic range overlap. Alternatively, an opposite relationship between divergence time and geographic range overlap is consistent with sympatric speciation as the main mechanism underlying the cercopithecin radiation. We collected biogeographic and phylogenetic data for 19 guenon species from the literature. We digitized geographic range maps and utilized three different phylogenetic hypotheses based on Y chromosome, X chromosome, and mitochondrial (mtDNA) data. We used regressions with Monte Carlo simulation to examine the relationship between the relative time since divergence of taxa and their degree of geographic range overlap. We found that there was a positive relationship between relative divergence time and the proportion of geographic range overlap between taxa using all three molecular data sets. Our findings provide evidence for allopatric speciation being the common mode of diversification in the cercopithecin clade. Because most of these primates are forest adapted mammals, the cyclical contraction and expansion of African forests from the late Miocene to the present has likely been an important factor driving allopatric speciation. In addition, geographic barriers such as the Congo and Sanaga rivers have probably played a complementary role in producing new species within the clade.     

Testing for mating isolation between ecotypes: laboratory experiments with lake, stream and hybrid stickleback

Mating isolation is a frequent contributor to ecological speciation – but how consistently does it evolve as a result of divergent selection? We tested for genetically based mating isolation between lake and stream threespine stickleback (Gasterosteus aculeatus L.) from the Misty watershed, Vancouver Island, British Columbia. We combined several design elements that are uncommon in the studies of stickleback mate choice: (i) we used second‐generation laboratory‐reared fish (to reduce environmental and maternal effects), (ii) we allowed for male–male competitive interactions (instead of the typical no‐choice trials) and (iii) we included hybrids along with pure types. Males of different types (Lake, Inlet, hybrid) were paired in aquaria, allowed to build nests and then exposed sequentially to females of all three types. We found that Lake and Inlet males differed in behaviours thought to influence stickleback mate choice (inter‐ and intra‐sexual aggression, display and nest activities), whereas hybrids were either intermediate or apparently ‘inferior’ in these behaviours. Despite these differences, Lake and Inlet fish did not mate assortatively and hybrid males did not have a mating disadvantage. Our study reinforces the noninevitability of mating isolation evolving in response to ecological differences and highlights the need to further investigate the factors promoting and constraining progress towards ecological speciation.     

Sexual selection can constrain sympatric speciation

Recent theory has suggested that sympatric speciation can occur quite easily when individuals that are ecologically similar mate assortatively. Although many of these models have assumed that individuals have equal mating success, in nature rare phenotypes may often suffer decreased mating success. Consequently, assortative mating may often generate stabilizing sexual selection. We show that this effect can substantially impede sympatric speciation. Our results emphasize the need for data on the strength of the stabilizing component of selection generated by mating in natural populations.     

Synergistic selection between ecological niche and mate preference primes diversification

The ecological niche and mate preferences have independently been shown to be important for the process of speciation. Here, we articulate a novel mechanism by which ecological niche use and mate preference can be linked to promote speciation. The degree to which individual niches are narrow and clustered affects the strength of divergent natural selection and population splitting. Similarly, the degree to which individual mate preferences are narrow and clustered affects the strength of divergent sexual selection and assortative mating between diverging forms. This novel perspective is inspired by the literature on ecological niches; it also explores mate preferences and how they may contribute to speciation. Unlike much comparative work, we do not search for evolutionary patterns using proxies for adaptation and sexual selection, but rather we elucidate how ideas from niche theory relate to mate preference, and how this relationship can foster speciation. Recognizing that individual and population niches are conceptually and ecologically linked to individual and population mate preference functions will significantly increase our understanding of rapid evolutionary diversification in nature. It has potential to help solve the difficult challenge of testing the role of sexual selection in the speciation process. We also identify ecological factors that are likely to affect individual niche and individual mate preference in synergistic ways and as a consequence to promote speciation. The ecological niche an individual occupies can directly affect its mate preference. Clusters of individuals with narrow, differentiated niches are likely to have narrow, differentiated mate preference functions. Our approach integrates ecological and sexual selection research to further our understanding of diversification processes. Such integration may be necessary for progress because these processes seem inextricably linked in the natural world.     

Inheritance of female mating preference in a sympatric sibling species pair of Lake Victoria cichlids: implications for speciation

Female mate choice has often been proposed to play an important role in cases of rapid speciation, in particular in the explosively evolved haplochromine cichlid species flocks of the Great Lakes of East Africa. Little, if anything, is known in cichlid radiations about the heritability of female mating preferences. Entirely sympatric distribution, large ecological overlap and conspicuous differences in male nuptial coloration, and female preferences for these, make the sister species Pundamilia pundamilia and P. nyererei from Lake Victoria an ideally suited species pair to test assumptions on the genetics of mating preferences made in models of sympatric speciation. Female mate choice is necessary and sufficient to maintain reproductive isolation between these species, and it is perhaps not unlikely therefore, that female mate choice has been important during speciation. A prerequisite for this, which had remained untested in African cichlid fish, is that variation in female mating preferences is heritable. We investigated mating preferences of females of these sister species and their hybrids to test this assumption of most sympatric speciation models, and to further test the assumption of some models of sympatric speciation by sexual selection that female preference is a single-gene trait. We find that the differences in female mating preferences between the sister species are heritable, possibly with quite high heritabilities, and that few but probably more than one genetic loci contribute to this behavioural speciation trait with no apparent dominance. We discuss these results in the light of speciation models and the debate about the explosive radiation of cichlid fishes in Lake Victoria.     

Integrating QTL mapping and genome scans towards the characterization of candidate loci under parallel selection in the lake whitefish (Coregonus clupeaformis)

As natural selection must act on underlying genetic variation, discovering the number and location of loci under the influence of selection is imperative towards understanding adaptive divergence in evolving populations. Studies employing genome scans have hypothesized that the action of divergent selection should reduce gene flow at the genomic locations implicated in adaptation and speciation among natural populations, yet once 'outlier' patterns of variation have been identified the function and role of such loci needs to be confirmed. We integrated adaptive QTL mapping and genomic scans among diverging sympatric pairs of the lake whitefish (Coregonus clupeaformis) species complex in order to test the hypothesis that differentiation between dwarf and normal ecotypes at growth-associated QTL was maintained by directional selection. We found evidence of significantly high levels of molecular divergence among eight growth QTL where two of the strongest candidate loci under the influence of directional selection exhibited parallel reductions of gene flow over multiple populations.     

Coevolution of male mating signal and female preference during early lineage divergence of the Hawaiian cricket, Laupala cerasina

Sexual selection is a powerful evolutionary force shaping mate choice phenotypes, initiating phenotypic shifts resulting in (or reinforcing) population divergence and speciation when such shifts reduce mating probabilities among divergent populations. In the Hawaiian cricket genus Laupala, pulse rate of male calling song, a conspicuous mating signal, differs among species, potentially behaving as a speciation phenotype. Populations of the widespread species Laupala cerasina show variation in pulse rate. We document the degree of population differentiation in three features of calling song: pulse rate, pulse duration, and carrier frequency. All show significant population differentiation, with pulse rate showing the greatest heterogeneity. A Mantel test found no relationship between geographic distance and pulse rate divergence, indicating that a simple model of greater divergence with increasing distance cannot explain the observed pattern of differentiation. We demonstrate that female preference functions for pulse rate are unimodal, and that preference means show significant differentiation among populations. Furthermore, estimates of pulse rate preference correlate significantly with mean pulse rates across populations, indicating song and preference coevolve in a stepwise manner. This correlated divergence between signal and preference suggests that sexual selection facilitates the establishment of sexual isolation, reduced gene flow, and population differentiation, prerequisites for speciation.