Sexual selection and speciation

The power of sexual selection to drive changes in mate recognition traits gives it the potential to be a potent force in speciation. Much of the evidence to support this possibility comes from comparative studies that examine differences in the number of species between clades that apparently differ in the intensity of sexual selection. We argue that more detailed studies are needed, examining extinction rates and other sources of variation in species richness. Typically, investigations of extant natural populations have been too indirect to convincingly conclude speciation by sexual selection. Recent empirical work, however, is beginning to take a more direct approach and rule out confounding variables.     

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.     

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.     

Sexual selection research on spiders: progress and biases

The renaissance of interest in sexual selection during the last decades has fuelled an extraordinary increase of scientific papers on the subject in spiders. Research has focused both on the process of sexual selection itself, for example on the signals and various modalities involved, and on the patterns, that is the outcome of mate choice and competition depending on certain parameters. Sexual selection has most clearly been demonstrated in cases involving visual and acoustical signals but most spiders are myopic and mute, relying rather on vibrations, chemical and tactile stimuli. This review argues that research has been biased towards modalities that are relatively easily accessible to the human observer. Circumstantial and comparative evidence indicates that sexual selection working via substrate-borne vibrations and tactile as well as chemical stimuli may be common and widespread in spiders. Pattern-oriented research has focused on several phenomena for which spiders offer excellent model objects, like sexual size dimorphism, nuptial feeding, sexual cannibalism, and sperm competition. The accumulating evidence argues for a highly complex set of explanations for seemingly uniform patterns like size dimorphism and sexual cannibalism. Sexual selection appears involved as well as natural selection and mechanisms that are adaptive in other contexts only. Sperm competition has resulted in a plethora of morphological and behavioural adaptations, and simplistic models like those linking reproductive morphology with behaviour and sperm priority patterns in a straightforward way are being replaced by complex models involving an array of parameters. Male mating costs are increasingly being documented in spiders, and sexual selection by male mate choice is discussed as a potential result. Research on sexual selection in spiders has come a long way since Darwin, whose spider examples are reanalysed in the context of contemporary knowledge, but the same biases and methodological constraints have persisted almost unchanged through the current boom of research.     

Sexual selection drives speciation in an Amazonian frog

One proposed mechanism of speciation is divergent sexual selection, whereby divergence in female preferences and male signals results in behavioural isolation. Despite the appeal of this hypothesis, evidence for it remains inconclusive. Here, we present several lines of evidence that sexual selection is driving behavioural isolation and speciation among populations of an Amazonian frog (Physalaemus petersi). First, sexual selection has promoted divergence in male mating calls and female preferences for calls between neighbouring populations, resulting in strong behavioural isolation. Second, phylogenetic analysis indicates that populations have become fixed for alternative call types several times throughout the species' range, and coalescent analysis rejects genetic drift as a cause for this pattern, suggesting that this divergence is due to selection. Finally, gene flow estimated with microsatellite loci is an average of 30 times lower between populations with different call types than between populations separated by a similar geographical distance with the same call type, demonstrating genetic divergence and incipient speciation. Taken together, these data provide strong evidence that sexual selection is driving behavioural isolation and speciation, supporting sexual selection as a cause for speciation in the wild.     

Sexual selection and the risk of extinction in mammals

Sexual selection is commonly envisaged as a force working in opposition to natural selection, because extravagant or exaggerated traits could apparently have never evolved via natural selection alone. There is good evidence that a selection load imposed by sexual selection may be eased experimentally by restricting the opportunity for it to operate. Sexual selection could therefore potentially play an important role in influencing the risk of extinction that a population faces, thereby contributing to the apparent selectivity of extinctions. Conversely, recent theory predicts that the likelihood of extinction may decrease when sexual selection is operating because it could accelerate the rate of adaptation in concert with natural selection. So far, comparative evidence (coming mostly from birds) has generally indicated support for the former scenario, but the question remains open. The aim of this study was therefore to examine whether the level of sexual selection (measured as residual testes mass and sexual size dimorphism) was related to the risk of extinction that mammals are currently experiencing. We found no evidence for a relationship between these factors, although our analyses may have been confounded by the possible dominating effect of contemporary anthropogenic factors.     

Sexual selection,speciation and constraints on geographical range overlap in birds

The role of sexual selection as a driver of speciation remains unresolved, not least because we lack a clear empirical understanding of its influence on different phases of the speciation process. Here, using data from 1306 recent avian speciation events, we show that plumage dichromatism (a proxy for sexual selection) does not predict diversification rates, but instead explains the rate at which young lineages achieve geographical range overlap. Importantly, this effect is only significant when range overlap is narrow (< 20%). These findings are consistent with a ‘differential fusion’ model wherein sexual selection reduces rates of fusion among lineages undergoing secondary contact, facilitating parapatry or limited co‐existence, whereas more extensive sympatry is contingent on additional factors such as ecological differentiation. Our results provide a more mechanistic explanation for why sexual selection appears to drive early stages of speciation while playing a seemingly limited role in determining broad‐scale patterns of diversification.     

Sexual selection drives the evolution of antiaphrodisiac pheromones in butterflies

Competition for mates has resulted in sophisticated mechanisms of male control over female reproduction. Antiaphrodisiacs are pheromones transferred from males to females during mating that reduce attractiveness of females to subsequent courting males. Antiaphrodisiacs generally help unreceptive females reduce male harassment. However, lack of control over pheromone release by females and male control over the amount transferred provides males an opportunity to use antiaphrodisiacs to delay remating by females that have returned to a receptive state. We propose a model for the evolution of antiaphrodisiacs under the influence of intrasexual selection, and determine whether changes in this signal in 11 species of Heliconius butterflies are consistent with two predictions of the model. First, we find that as predicted, male-contributed chemical mixtures are complex and highly variable across species, with limited phylogenetic signal. Second, differences in rates of evolution in pheromone composition between two major clades of Heliconius are as expected: the clade with a greater potential for male-male competition (polyandrous) shows a faster rate of divergence than the one with typically monoandrous mating system. Taken together, our results provide evidence that for females, antiaphrodisiacs can be both honest signals of receptivity (helping reduce harassment) and chastity belts (a male-imposed reduction in remating).     

Sexual selection accelerates signal evolution during speciation in birds

Sexual selection is proposed to be an important driver of diversification in animal systems, yet previous tests of this hypothesis have produced mixed results and the mechanisms involved remain unclear. Here, we use a novel phylogenetic approach to assess the influence of sexual selection on patterns of evolutionary change during 84 recent speciation events across 23 passerine bird families. We show that elevated levels of sexual selection are associated with more rapid phenotypic divergence between related lineages, and that this effect is restricted to male plumage traits proposed to function in mate choice and species recognition. Conversely, we found no evidence that sexual selection promoted divergence in female plumage traits, or in male traits related to foraging and locomotion. These results provide strong evidence that female choice and male–male competition are dominant mechanisms driving divergence during speciation in birds, potentially linking sexual selection to the accelerated evolution of pre-mating reproductive isolation.     

Sexual selection and speciation: the comparative evidence revisited

The spectacular diversity in sexually selected traits in the animal kingdom has inspired the hypothesis that sexual selection can promote species divergence. In recent years, several studies have attempted to test this idea by correlating species richness with estimates of sexual selection across phylogenies. These studies have yielded mixed results and it remains unclear whether the comparative evidence can be taken as generally supportive. Here, we conduct a meta‐analysis of the comparative evidence and find a small but significant positive overall correlation between sexual selection and speciation rate. However, we also find that effect size estimates are influenced by methodological choices. Analyses that included deeper phylogenetic nodes yielded weaker correlations, and different proxies for sexual selection showed different relationships with species richness. We discuss the biological and methodological implications of these findings. We argue that progress requires more representative sampling and justification of chosen proxies for sexual selection and speciation rate, as well as more mechanistic approaches.     

Sexual selection and speciation: Issues raised by Hawaiian Drosophila

The Drosophila fauna of Hawaii is extraordinarily diverse, representing about 25% of the world's described species. The most notable characteristics which differentiate the species in Hawaii are morphological and behavioral ones used in courtship and mating. These flies are excellent model species for investigating the evolution of sexually selected traits. Hypotheses regarding the associations between species formation and mating behaviour have been formulated as a result of work on this group, leading to further empirical and theoretical research.     

Sexual selection and peripatric speciation: the Kaneshiro model revisited

The Kaneshiro model proposes a role for sexual selection in peripatric speciation. During population bottlenecks, derived males lose attractive traits and become discriminated against by ancestral females, whereas derived females are selected to be less choosy. This permits novel mate choice cues to evolve in derived populations. In a quantitative analysis of laboratory experiments, we show that bottlenecked males have indeed become less attractive, but females have not lost their ancestral preferences. Contrary to the model, mating asymmetries were not limited to bottlenecks, but regularly occurred between derived and ancestral populations. The simplest explanation for the observed mating asymmetries is loss of genetic variation and inbreeding in the derived populations. The Kaneshiro process is unlikely to isolate small daughter populations from their ancestor but with slight modifications it may become a strong candidate for speciation in allopatry manifested as isolation between daughter populations in secondary contact.     

ZSL Scientific Meetings: short reports Sexual selection, genetic variation and speciation

Rudyard Kipling was able to explain "How the Leopard got its Spots" and "How the Rhino got its Skin", but he did not offer any clue as to "How the Peacock got its Tail", which is an issue that has long taxed the minds of evolutionary biologists. In fact, the males of many animal species produce extravagant ornaments that appear to serve no really useful purpose. We know that, at least in some cases, these flamboyant displays are to do with sexual selection; they are used by females in making their choice of mates. However, we do not understand the consequences of such behaviour for other evolutionary topics.     

Karyotypic diversity and speciation in Agrodiaetus butterflies

That chromosomal rearrangements may play an important role in maintaining postzygotic isolation between well-established species is part of the standard theory of speciation. However, little evidence exists on the role of karyotypic change in speciation itself--in the establishment of reproductive barriers between previously interbreeding populations. The large genus Agrodiaetus (Lepidoptera: Lycaenidae) provides a model system to study this question. Agrodiaetus butterflies exhibit unusual interspecific diversity in chromosome number, from n= 10 to n= 134; in contrast, the majority of lycaenid butterflies have n= 23/24. We analyzed the evolution of karyotypic diversity by mapping chromosome numbers on a thoroughly sampled mitochondrial phylogeny of the genus. Karyotypic differences accumulate gradually between allopatric sister taxa, but more rapidly between sympatric sister taxa. Overall, sympatric sister taxa have a higher average karyotypic diversity than allopatric sister taxa. Differential fusion of diverged populations may account for this pattern because the degree of karyotypic difference acquired between allopatric populations may determine whether they will persist as nascent biological species in secondary sympatry. This study therefore finds evidence of a direct role for chromosomal rearrangements in the final stages of animal speciation. Rapid karyotypic diversification is likely to have contributed to the explosive speciation rate observed in Agrodiaetus, 1.6 species per million years.     

Hybridization promotes speciation in Coenonympha butterflies

Hybridization has become a central element in theories of animal evolution during the last decade. New methods in population genomics and statistical model testing now allow the disentangling of the complexity that hybridization brings into key evolutionary processes such as local adaptation, colonization of new environments, species diversification and extinction. We evaluated the consequences of hybridization in a complex of three alpine butterflies in the genus Coenonympha, by combining morphological, genetic and ecological analyses. A series of approximate Bayesian computation procedures based on a large SNP data set strongly suggest that the Darwin's Heath (Coenonympha darwiniana) originated through hybridization between the Pearly Heath (Coenonympha arcania) and the Alpine Heath (Coenonympha gardetta) with different parental contributions. As a result of hybridization, the Darwin's Heath presents an intermediate morphology between the parental species, while its climatic niche seems more similar to the Alpine Heath. Our results also reveal a substantial genetic and morphologic differentiation between the two geographically disjoint Darwin's Heath lineages leading us to propose the splitting of this taxon into two different species.     

Hybrid zones and the speciation continuum in Heliconius butterflies

Tropical butterflies in the genus Heliconius have long been models in the study of the stages of speciation. Heliconius are unpalatable to predators, and many species are notable for multiple geographic populations with striking warning colour pattern differences associated with Müllerian mimicry. A speciation continuum is evident in Heliconius hybrid zones. Examples range from hybrid zones across which (a) there is little genetic differentiation other than at mimicry loci, but where hybrids are common, (b) to ‘bimodal‘ hybrid zones with strong genetic divergence and few hybrids, (c) through to ‘good’ sympatric species, with hybridization extremely rare or absent. Now, in this issue of Molecular Ecology, Arias et al. ( 2012 ) have found an intermediate case in Colombian Heliconius cydno showing evidence for assortative mating and molecular differences, but where hybrids are abundant.     

Ecology, sexual selection and speciation

The spectacular diversity in sexually selected traits among animal taxa has inspired the hypothesis that divergent sexual selection can drive speciation. Unfortunately, speciation biologists often consider sexual selection in isolation from natural selection, even though sexually selected traits evolve in an ecological context: both preferences and traits are often subject to natural selection. Conversely, while behavioural ecologists may address ecological effects on sexual communication, they rarely measure the consequences for population divergence. Herein, we review the empirical literature addressing the mechanisms by which natural selection and sexual selection can interact during speciation. We find that convincing evidence for any of these scenarios is thin. However, the available data strongly support various diversifying effects that emerge from interactions between sexual selection and environmental heterogeneity. We suggest that evaluating the evolutionary consequences of these effects requires a better integration of behavioural, ecological and evolutionary research.     

Review. Hybrid trait speciation and Heliconius butterflies

Homoploid hybrid speciation (HHS) is the establishment of a novel species through introgressive hybridization without a change in chromosome number. We discuss different routes by which this might occur and propose a novel term, 'hybrid trait speciation', which combines the idea that hybridization can generate adaptive novelty with the 'magic trait' model of ecological speciation. Heliconius butterflies contain many putative examples of hybrid colour patterns, but only recently has the HHS hypothesis been tested explicitly in this group. Molecular data has shown evidence for gene flow between many distinct species. Furthermore, the colour pattern of Heliconius heurippa can be recreated in laboratory crosses between Heliconius melpomene and Heliconius cydno and, crucially, plays a role in assortative mating between the three species. Nonetheless, although the genome of H. heurippa shows evidence for hybridization, it is not a mosaic of the two parental species. Instead, ongoing hybridization has likely blurred any signal of the original speciation event. We argue that where hybridization leads to novel adaptive traits that also cause reproductive isolation, it is likely to trigger speciation.     

Sexual attractivity,proceptivity, and receptivity in female mammals

Special definitions are proposed for three concepts representing characteristics of female mammals when they are in estrus. Attractivity refers to the female's stimulus value in evoking sexual responses by the male. Proceptivity connotes various reactions by the female toward the male which constitute her assumption of initiative in establishing or maintaining sexual interaction. Receptivity is defined in terms of female responses necessary and sufficient for the male's success in achieving intravaginal ejaculation. Attempts are made to measure each variable in the S-R paradigm and to identify the causal agents determining each aspect of the estrous female's behavioral characteristics.