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 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.     

Role of sexual selection in speciation in Drosophila

The power of sexual selection to drive changes in the mate recognition system through divergence in sexually selected traits gives it the potential to be a potent force in speciation. To know how sexual selection can bring such type of divergence in the genus Drosophila, comparative studies based on intra- and inter-sexual selection are documented in this review. The studies provide evidence that both mate choice and male–male competition can cause selection of trait and preference which thereby leads to divergence among species. In the case of intrasexual selection, various kinds of signals play significant role in affecting the species mate recognition system and hence causing divergence between the species. However, intrasexual selection can bring the intraspecific divergence at the level of pre- and post-copulatory stage. This has been better explained through Hawaiian Drosophila which has been suggested a wonderful model system in explaining the events of speciation via sexual selection. This is due to their elaborate mating displays and some kind of ethological isolation persisting among them. Similarly, the genetic basis of sexually selected variations can provide yet another path in understanding the speciation genetics via sexual selection more closely.     

Sexual selection and magic traits in speciation with gene flow

The extent to which sexual selection is involved in speciation with gene flow remains an open question and the subject of much research.Here,we propose that some insight can be gained from considering the concept of magic traits (i.e.,traits involved in both reproductive isolation and ecological divergence).Both magic traits and other,“non-magic”,traits can contribute to speciation via a number of specific mechanisms.We argue that many of these mechanisms are likely to differ widely in the extent to which they involve sexual selection.Furthermore,in some cases where sexual selection is present,it may be prone to inhibit rather than drive speciation.Finally,there are a priori reasons to believe that certain categories of traits are much more effective than others in driving speciation.The combination of these points suggests a classification of traits that may shed light on the broader role of sexual selection in speciation with gene flow.In particular,we suggest that sexual selection can act as a driver of speciation in some scenarios,but may play a negligible role in potentially common categories of magic traits,and may be likely to inhibit speeiation in common categories of non-magic traits.     

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.     

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.     

Sexual selection on color and behavior within and between cichlid populations: Implications for speciation

Sexual selection is widely viewed as playing a central role in hapiochromine cichlid speciation.Hypothetically,once divergent mate preferences evolve among populations of these fishes,reproductive isolation follows and the populations begin to behave as different species.Various studies have examined patterns of assortative mating among species and sometimes populations,but few have examined variation in directional preferences,especially among populations of the same species.We investigated mate choice behavior in two populations of Labeotropheus fuelleborni,a Lake Malawi endemic.We test whether mating.preferences between populations are based on the same traits and in the same direction as preferences within populations.We examine the potential contributions of two classes of trait,color patterns and behaviors,to reproductive isolation.When females chose between either two males of their own population,or two from another,female preferences were generally similar (for the female population) across the two contexts.Mate choice patterns differed between (female) populations for a measure of color,but only modestly for male behavior.In a separate experiment we simultaneously offered females a male of their own population and a male from a different population.In these trials,females consistently preferred males from their own population,which were also the males that displayed more frequently than their opponents,but not necessarily those with color traits suggested to be most attractive in the previous experiment.Thus directional preferences for chroma and related aspects of color may be important when females are presented with males of otherwise similar phenotypes,but may play little role in mediating assortative mating among populations with substantially different color patterns.A preference for male behavior could play some role in speciation if males preferentially court same-population females,as we have observed for the populations studied herein.     

Sexual conflict and speciation.

We review the significance of two forms of sexual conflict (different evolutionary interests of the two sexes) for genetic differentiation of populations and the evolution of reproductive isolation. Conflicting selection on the alleles at a single locus can occur in males and females if the sexes have different optima for a trait, and there are pleiotropic genetic correlations between the sexes for it. There will then be selection for sex limitation and hence sexual dimorphism. This sex limitation could break down in hybrids and reduce their fitness. Pleiotropic genetic correlations between the sexes could also affect the likelihood of mating in interpopulation encounters. Conflict can also occur between (sex-limited) loci that determine behaviour in males and those that determine behaviour in females. Reproductive isolation may occur by rapid coevolution of male trait and female mating preference. This would tend to generate assortative mating on secondary contact, hence promoting speciation. Sexual conflict resulting from sensory exploitation, polyspermy and the cost of mating could result in high levels of interpopulation mating. If females evolve resistance to make pre- and postmating manipulation, males from one population could be more successful with females from the other, because females would have evolved resistance to their own (but not to the allopatric) males. Between-locus sexual conflict could also occur as a result of conflict between males and females of different populations over the production of unfit hybrids. We develop models which show that females are in general selected to resist such matings and males to persist, and this could have a bearing on both the initial level of interpopulation matings and the likelihood that reinforcement will occur. In effect, selection on males usually acts to promote gene flow and to restrict premating isolation, whereas selection on females usually acts in the reverse direction. We review theoretical models relevant to resolution of this conflict. The winning role depends on a balance between the ''value of winning'' and ''power'' (relating to contest or armament costs): the winning role is likely to correlate with high value of winning and low costs. Sperm-ovum (or sperm-female tract) conflicts (and their plant parallels) are likely to obey the same principles. Males may typically have higher values of winning, but it is difficult to quantify ''power'', and females may often be able to resist mating more cheaply than males can force it. We tentatively predict that sexual conflict will typically result in a higher rate of speciation in ''female-win'' clades, that females will be responsible for premating isolation through reinforcement, and that ''female-win'' populations will be less genetically diverse.     

Sympatric speciation by sexual selection: a critical reevaluation

Several empirical studies put forward sexual selection as an important driving force of sympatric speciation. This idea agrees with recent models suggesting that speciation may proceed by means of divergent Fisherian runaway processes within a single population. Notwithstanding this, the models so far have not been able to demonstrate that sympatric speciation can unfold as a fully adaptive process driven by sexual selection alone. Implicitly or explicitly, most models rely on nonselective factors to initiate speciation. In fact, they do not provide a selective explanation for the considerable variation in female preferences required to trigger divergent runaway processes. We argue that such variation can arise by disruptive selection but only when selection on female preferences is frequency dependent. Adaptive speciation is therefore unattainable in traditional female choice models, which assume selection on female preferences to be frequency independent. However, when frequency-dependent sexual selection processes act alongside mate choice, truly adaptive sympatric speciation becomes feasible. Speciation is then initiated independently of nonadaptive processes and does not suffer from the theoretical weaknesses associated with the current Fisherian runaway model of speciation. However, adaptive speciation requires the simultaneous action of multiple mechanisms, and therefore it occurs under conditions far more restrictive than earlier models of sympatric speciation by sexual selection appear to suggest.     

Sexual isolation and speciation in bacteria

Like organisms from all other walks of life, bacteria are capable of sexual recombination. However, unlike most plants and animals, bacteria recombine only rarely, and when they do they are extremely promiscuous in their choice of sexual partners. There may be no absolute constraints on the evolutionary distances that can be traversed through recombination in the bacterial world, but interspecies recombination is reduced by a variety of factors, including ecological isolation, behavioral isolation, obstacles to DNA entry, restriction endonuclease activity, resistance to integration of divergent DNA sequences, reversal of recombination by mismatch repair, and functional incompatibility of recombined segments. Typically, individual bacterial species are genetically variable for most of these factors. Therefore, natural selection can modulate levels of sexual isolation, to increase the transfer of genes useful to the recipient while minimizing the transfer of harmful genes. Interspecies recombination is optimized when recombination involves short segments that are just long enough to transfer an adaptation, without co-transferring potentially harmful DNA flanking the adaptation. Natural selection has apparently acted to reduce sexual isolation between bacterial species. Evolution of sexual isolation is not a milestone toward speciation in bacteria, since bacterial recombination is too rare to oppose adaptive divergence between incipient species. Ironically, recombination between incipient bacterial species may actually foster the speciation process, by prohibiting one incipient species from out-competing the other to extinction. Interspecific recombination may also foster speciation by introducing novel gene loci from divergent species, allowing invasion of new niches.     

Interspecific genetics of speciation phenotypes: song and preference coevolution in Hawaiian crickets

Understanding the genetic architecture of traits involved in premating isolation between recently diverged lineages can provide valuable insight regarding the mode and tempo of speciation. The repeated coevolution of male courtship song and female preference across the species radiation of Laupala crickets presents an unusual opportunity to compare the genetic basis of divergence across independent evolutionary histories. Previous studies of one pair of species revealed a polygenic basis (including a significant X chromosome contribution) to quantitative differences in male song and female acoustic preference. Here, we studied interspecific crosses between two phenotypically less-diverged species that represents a phylogenetically independent occurrence of intersexual signalling evolution. We found patterns consistent with an additive polygenic basis to differentiation in both song and preference (n(E) = 5.3 and 5.1 genetic factors, respectively), and estimate a moderate contribution of the X chromosome (7.6%) of similar magnitude to that observed for Laupala species with nearly twice the phenotypic divergence. Together, these findings suggest a similar genetic architecture underlying the repeated evolution of sexual characters in this genus and provide a counterexample to prevailing theory predicting an association between early lineage divergence and sex-linked 'major genes'.     

Sex chromosomes and speciation in Drosophila

Two empirical rules suggest that sex chromosomes play a special role in speciation. The first is Haldane's rule - the preferential sterility and inviability of species hybrids of the heterogametic (XY) sex. The second is the disproportionately large effect of the X chromosome in genetic analyses of hybrid sterility. Whereas the causes of Haldane's rule are well established, the causes of the 'large X-effect' have remained controversial. New genetic analyses in Drosophila confirm that the X is a hotspot for hybrid male sterility factors, providing a proximate explanation for the large X-effect. Several other new findings -- on faster X evolution, X chromosome meiotic drive and the regulation of the X chromosome in the male-germline -- provide plausible evolutionary explanations for the large X-effect.     

Sympatric speciation and extinction driven by environment dependent sexual selection

A theoretical model is studied to investigate the possibility of sympatric speciation driven by sexual selection and ecological diversification. In particular we focus on the rock-dwelling haplochromine cichlid species in Lake Victoria. The high speciation rate in these cichlids has been explained by their apparent ability to specialize rapidly to a large diversity of feeding niches. Seehausen and colleagues however, demonstrated the importance of sexual selection in maintaining reproductive barriers between species. Our individual-orientated model integrates both niche differentiation and a Fisherian runaway process, which is limited by visibility constraints. The model shows rapid sympatric speciation or extinction of species, depending on the strength of sexual selection.     

Sexual selection on song and cuticular hydrocarbons in two distinct populations of Drosophila montana

Sexual selection has the potential to contribute to population divergence and speciation. Most studies of sexual selection in Drosophila have concentrated on a single signaling modality, usually either courtship song or cuticular hydrocarbons (CHCs), which can act as contact pheromones. We have examined the relationship between both signal types and reproductive success using F(1-3) offspring of wild-collected flies, raised in the lab. We used two populations of the Holarctic species Drosophila montana that represent different phylogeographic clades that have been separate for ca. 0.5 million years (MY), and differ to some extent in both traits. Here, we characterize the nature and identify the targets of sexual selection on song, CHCs, and both traits combined within the populations. Three measures of courtship outcome were used as fitness proxies. They were the probability of mating, mating latency, and the production of rejection song by females, and showed patterns of association with different traits that included both linear and quadratic selection. Courtship song predicted courtship outcome better than CHCs and the signal modalities acted in an additive rather than synergistic manner. Selection was generally consistent in direction and strength between the two populations and favored males that sang more vigorously. Sexual selection differed in the extent, strength, and nature on some of the traits between populations. However, the differences in the directionality of selection detected were not a good predictor of population differences. In addition, a character previously shown to be important for species recognition, interpulse interval, was found to be under sexual selection. Our results highlight the complexity of understanding the relationship between within-population sexual selection and population differences. Sexual selection alone cannot predict differences between populations.