The evolution of reproductive isolation through sexual conflict

Classical population-genetics theory suggests that reproductive isolation will evolve fastest in small isolated populations. In contrast, recent theory suggests that divergence should occur fastest in larger allopatric populations. The rationale behind this is that sexual conflict, potentially the strongest driver of speciation, is greater in larger, higher-density populations. This idea is highly controversial and has little experimental support. Here we show, using replicate fly populations with varying levels of sexual conflict, that larger, more dense populations with more sexual conflict diverged to a greater degree than small populations with relaxed conflict. This result strongly suggests that speciation can occur rapidly in large populations through increased sexual conflict.     

Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism.

The origin and maintenance of polymorphism in major histocompatibility complex (MHC) genes in natural populations is still unresolved. Sexual selection, frequency-dependent selection by parasites and pathogens, and heterozygote advantage have been suggested to explain the maintenance of high allele diversity at MHC genes. Here we argue that there are two (non-exclusive) strategies for MHC-related sexual selection, representing solutions to two different problems: inbreeding avoidance and parasite resistance. In species prone to inadvertent inbreeding, partners should prefer dissimilar MHC genotypes to similar ones. But if the goal is to maximize the resistance of offspring towards potential infections, the choosing sex should prefer mates with a higher diversity of MHC alleles. This latter strategy should apply when there are several MHC loci, as is the case in most vertebrates. We tested the relative importance of an 'allele counting' strategy compared to a disassortative mating strategy using wild-caught three-spined sticklebacks (Gasterosteus aculeatus) from an interconnected system of lakes. Here we show that gravid female fish preferred the odour of males with a large number of MHC class-IIB alleles to that of males with fewer alleles. Females did not prefer male genotypes dissimilar to their own.     

Sympatric speciation by sexual selection

There is increasing evidence for the process of sympatric speciation, in which reproductive isolation of species occurs without physical isolation. Theoretical models have focused on disruptive natural selection as the crucial pressure for splitting a species. Here we report the theoretical finding that sympatric speciation may be caused by sexual selection even without disruptive natural selection. Specifically, we show that variation in a male secondary sexual character with two conspicuous extremes and the corresponding variance in female mating preference around no preference may jointly evolve into bimodal distributions with increasing modal divergence of the male and female traits, pulling a population apart into two prezygotically isolated populations. This mode of speciation, driven by two runaway processes in different directions, is promoted by an increase in the efficiency of females in discriminating among males or a decrease in the cost of male conspicuousness, indicating that sympatric speciation may occur more readily if barrier-free or predator-free conditions arise. Although even a slight cost of female preference would cancel the runaway process of sexual selection, it would not cancel the divergent runaway processes of sympatric speciation.     

Intrasexual competition and sexual selection in cooperative mammals

In most animals, the sex that invests least in its offspring competes more intensely for access to the opposite sex and shows greater development of secondary sexual characters than the sex that invests most. However, in some mammals where females are the primary care-givers, females compete more frequently or intensely with each other than males. A possible explanation is that, in these species, the resources necessary for successful female reproduction are heavily concentrated and intrasexual competition for breeding opportunities is more intense among females than among males. Intrasexual competition between females is likely to be particularly intense in cooperative breeders where a single female monopolizes reproduction in each group. Here, we use data from a twelve-year study of wild meerkats (Suricata suricatta), where females show high levels of reproductive skew, to show that females gain greater benefits from acquiring dominant status than males and traits that increase competitive ability exert a stronger influence on their breeding success. Females that acquire dominant status also develop a suite of morphological, physiological and behavioural characteristics that help them to control other group members. Our results show that sex differences in parental investment are not the only mechanism capable of generating sex differences in reproductive competition and emphasize the extent to which competition for breeding opportunities between females can affect the evolution of sex differences and the operation of sexual selection.     

Genetic selection for reproductive photoresponsiveness in deer mice

Seasonal breeding is common in mammals, particularly in habitats outside the tropics. Climate and availability of food are the ultimate factors that usually dictate the optimal time of year for a mammal to breed; however, day length (photoperiod) often serves as the proximal cue to signal the onset or cessation of seasonal reproduction. Some individuals in some populations of deer mice are reproductively responsive to photoperiod, while other individuals in the same population are not. As shown here, selection can dramatically alter the frequency of photoresponsiveness in a laboratory population in only two generations. To our knowledge this is the first demonstration of selection for reproductive photoresponsiveness in any mammal. By implication, some wild populations of deer mice must use multiple, genetic-based reproductive strategies, and the degree to which each such strategy is exhibited must be subject to rapid change in response to both seasonally and momentarily changing climatic and dietary conditions.     

Disposable-soma senescence mediated by sexual selection in an ungulate

Senescence may result from an optimal balance between current reproductive investment and bodily repair processes required for future reproduction, a theoretical prediction difficult to prove especially in large, long-lived animals. Here we propose that teeth that have fixed dimensions early in life, but that wear during chewing, can be taken as a measure of total lifetime 'repair', and their wear rate as a measure of current expenditure in performance. Our approach also considers the sexual selection process to investigate the advance of senescence in males compared with females, when selection favouring competition over mates reduces the reproductive lifespan of males. We studied carcasses of 2,141 male and 739 female red deer (Cervus elaphus) of different ages, finding that male molariform teeth emerged at a far smaller size than expected from body size dimorphism. This led to higher workload, steeper wear rate and earlier depletion of male teeth than in females, in concordance with sex-specific patterns of lifetime performance and reproduction. These findings provide the empirical support for the disposable-soma hypothesis of senescence, which predicts that investment in bodily repair will decrease when the return from this investment may not be realized as a result of other causes that limit survival or reproduction.     

Host-plant adaptation drives the parallel evolution of reproductive isolation

Parallel evolution of similar traits in independent populations that inhabit ecologically similar environments strongly implicates natural selection as the cause of evolution. Parallel speciation is a special form of parallel evolution where traits that determine reproductive isolation evolve repeatedly, in closely related populations, as by-products of adaptation to ecological conditions. The outcome of such parallel evolution is that ecologically divergent pairs of populations exhibit greater levels of reproductive isolation than ecologically similar pairs of populations of a similar or younger age. The parallel evolution of reproductive isolation provides strong evidence for natural selection in the process of speciation, but only one conclusive example from nature is known. Populations of the walking-stick insect Timema cristinae that use different host-plant species have diverged in body size and shape, host preference, behaviour and the relative frequency of two highly cryptic colour-pattern morphs. Here we report that divergent selection for host adaptation, and not genetic drift, has promoted the parallel evolution of sexual isolation in this species. Our findings represent a clear demonstration that host-plant adaptation can play a crucial and repeatable role in the early stages of speciation.     

Rapid evolution of reproductive barriers driven by sexual conflict

A growing amount of experimental data indicates extremely rapid evolution of traits and proteins related to fertilization in many diverging taxa. These data come from studies of sperm or pollen competition between closely related species, and from molecular studies of fertilization proteins. The positive selection for evolutionary novelty that appears to be acting on fertilization systems seems paradoxical because successful reproduction requires the close matching of female and male traits. It has been suggested that perpetual coevolution between the sexes can result from sexual conflict in mating. Sexual conflict occurs when characteristics that enhance the reproductive success of one sex reduce the fitness of the other sex. Numerous examples of sexual conflict resulting from sensory exploitation, polyspermy and the cost of mating have been discussed in detail. The potential for coevolution due to such conflict has been evaluated experimentally. Here I develop a simple mathematical model describing coevolutionary dynamics of male and female traits involved in reproduction. The model shows that continual change in such traits at a constant speed is expected whenever females (or eggs) experience fitness loss from having too many compatible males (or sperms). The plausibility of runaway coevolution increases with increasing population size. Rapid evolution of reproductive barriers driven by sexual conflict may explain increased speciation rates after colonization of new habitats ('adaptive radiation') and high species richness in resource-rich environments.     

Genetic linkage of ecological specialization and reproductive isolation in pea aphids

The evolution of ecological specialization generates biological diversity and may lead to speciation. Genetic architecture can either speed or retard this process. If resource use and mate choice have a common genetic basis through pleiotropy or close linkage, the resulting genetic correlations can promote the joint evolution of specialization and reproductive isolation, facilitating speciation. Here we present a model of the role of genetic correlations in specialization and speciation, and test it by analysing the genetic architecture of key traits in two highly specialized host races of the pea aphid (Acyrthosiphon pisum pisum; Hemiptera : Aphididae). We found several complexes of pleiotropic or closely linked quantitative trait loci (QTL) that affect key traits in ways that would promote speciation: QTL with antagonistic effects on performance on the two hosts are linked to QTL that produce asortative mating (through habitat choice). This type of genetic architecture may be common in taxa that have speciated under divergent natural selection.     

Directional postcopulatory sexual selection revealed by artificial insemination

Postcopulatory sexual selection comprises both sperm competition, where the sperm from different males compete for fertilization, and cryptic female choice, where females bias sperm use in favour of particular males. Despite intense current interest in both processes as potential agents of directional sexual selection, few studies have attributed the success of attractive males to events that occur exclusively after insemination. This is because the interactions between pre- and post-insemination episodes of sexual selection can be important sources of variation in paternity. The use of artificial insemination overcomes this difficulty because it controls for variation in male fertilization success attributable to the female's perception of male quality, as well as effects due to mating order and the relative contribution of sperm from competing males. Here, we adopt this technique and show that in guppies, when equal numbers of sperm from two males compete for fertilization, relatively colourful individuals achieve greater parentage than their less ornamented counterparts. This finding indicates that precopulatory female mating preferences can be reinforced exclusively through postcopulatory processes occurring at a physiological level. Our analysis also revealed that relatively small individuals were advantaged in sperm competition, suggesting a possible trade-off between sperm competitive ability and body growth.     

Intensity of sexual selection along the anisogamy-isogamy continuum

Research into the evolution of giant sperm has uncovered a paradox within the foundations of sexual selection theory. Postcopulatory sexual selection on males (that is, sperm competition and cryptic female choice) can lead to decreased sperm numbers by favouring the production of larger sperm. However, a decline in sperm numbers is predicted to weaken selection on males and increase selection on females. As isogamy is approached (that is, as investment per gamete by males approaches that by females), sperm become less abundant, ova become relatively less rare, and competition between males for fertilization success is predicted to weaken. Sexual selection for longer sperm, therefore, is expected to be self limiting. Here we examine this paradox in Drosophila along the anisogamy-isogamy continuum using intraspecific experimental evolution techniques and interspecific comparative techniques. Our results confirm the big-sperm paradox by showing that the sex difference in sexual selection gradients decreases as sperm size increases. However, a resolution to the paradox is provided when this finding is interpreted in concert with the 'opportunity for selection' and the 'opportunity for sexual selection'. Furthermore, we show that most of the variation in measures of selection intensity is explained by sperm length and relative investment in sperm production.     

Mating advantage of rare males in models of sexual selection

Models of sexual selection in polygynous species of animals have been derived on the assumption that some females have preferences to mate with males with particular genotypes. The mating advantage gained by the males is always frequency-dependent because the preferred males take part in the same number of preferential matings when they are rare as when they are common; individually therefore, they mate more often when they are rare. Frequency-dependent sexual selection has been demonstrated in many experiments with Drosophila: rare males take part in a higher proportion of matings than their frequency as available mates. Ehrman and Spiess explained this phenomenon by frequency-dependence either in female preference or in male courtship. This explanation, which is difficult to interpret in behavioural terms, may not be necessary, however, because constant female preferences would entail frequency-dependent selection among the males. I show here that a simple model of constant preferences for particular phenotypes or genotypes is sufficient to explain a large body of data on frequency-dependent sexual selection in Drosophila.     

Disruptive sexual selection for plumage coloration in a passerine bird

The theory of sexual selection was developed to explain the evolution of highly exaggerated sexual ornaments. Now supported by vast empirical evidence, sexual selection is generally considered to favour individuals with the most extreme trait expression. Here we describe disruptive selection on a sexual ornament, plumage coloration, in yearling male lazuli buntings (Passerina amoena). In habitats with limited good-quality nesting cover, the dullest and the brightest yearlings were more successful in obtaining high-quality territories, pairing with females and siring offspring, than yearlings with intermediate plumage. This pattern reflects the way that territorial adult males vary levels of aggression to influence the structure of their social neighbourhood. Adult males showed less aggression towards dull yearlings than intermediate and bright ones, permitting the dull yearlings to settle on good territories nearby. Fitness comparisons based on paternity analyses showed that both the adults and dull yearlings benefited genetically from this arrangement, revealing a rare example of sexually selected male-male cooperation.     

Sexual selection and the maintenance of sexual reproduction

The maintenance of sexual reproduction is a problem in evolutionary theory because, all else being equal, asexual populations have a twofold fitness advantage over their sexual counterparts and should rapidly outnumber a sexual population because every individual has the potential to reproduce. The twofold cost of sex exists because of anisogamy or gamete dimorphism-egg-producing females make a larger contribution to the zygote compared with the small contribution made by the sperm of males, but both males and females contribute 50% of the genes. Anisogamy also generates the conditions for sexual selection, a powerful evolutionary force that does not exist in asexual populations. The continued prevalence of sexual reproduction indicates that the 'all else being equal' assumption is incorrect. Here I show that sexual selection can mitigate or even eliminate the cost of sex. If sexual selection causes deleterious mutations to be more deleterious in males than females, then deleterious mutations are maintained at lower equilibrium frequency in sexual populations relative to asexual populations. The fitness of sexual females is higher than asexuals because there is no difference in the fecundity of sexual females and asexuals of the same genotype, but the equilibrium frequency of deleterious mutations is lower in sexual populations. The results are not altered by synergistic epistasis in males.     

Ecological opportunity and sexual selection together predict adaptive radiation

A fundamental challenge to our understanding of biodiversity is to explain why some groups of species undergo adaptive radiations, diversifying extensively into many and varied species, whereas others do not. Both extrinsic environmental factors (for example, resource availability, climate) and intrinsic lineage-specific traits (for example, behavioural or morphological traits, genetic architecture) influence diversification, but few studies have addressed how such factors interact. Radiations of cichlid fishes in the African Great Lakes provide some of the most dramatic cases of species diversification. However, most cichlid lineages in African lakes have not undergone adaptive radiations. Here we compile data on cichlid colonization and diversification in 46 African lakes, along with lake environmental features and information about the traits of colonizing cichlid lineages, to investigate why adaptive radiation does and does not occur. We find that extrinsic environmental factors related to ecological opportunity and intrinsic lineage-specific traits related to sexual selection both strongly influence whether cichlids radiate. Cichlids are more likely to radiate in deep lakes, in regions with more incident solar radiation and in lakes where there has been more time for diversification. Weak or negative associations between diversification and lake surface area indicate that cichlid speciation is not constrained by area, in contrast to diversification in many terrestrial taxa. Among the suite of intrinsic traits that we investigate, sexual dichromatism, a surrogate for the intensity of sexual selection, is consistently positively associated with diversification. Thus, for cichlids, it is the coincidence between ecological opportunity and sexual selection that best predicts whether adaptive radiation will occur. These findings suggest that adaptive radiation is predictable, but only when species traits and environmental factors are jointly considered.     

Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild

Females often mate with several males before producing offspring. Field studies of vertebrates suggest, and laboratory experiments on invertebrates confirm, that even when males provide no material benefits, polyandry can enhance offspring survival. This enhancement is widely attributed to genetic benefits that arise whenever paternity is biased towards males that sire more viable offspring. Field studies suggest that post-mating sexual selection biases fertilization towards genetically more compatible males and one controlled experiment has shown that, when females mate with close kin, polyandry reduces the relative number of inbred offspring. Another potential genetic benefit of polyandry is that it increases offspring survival because males with more competitive ejaculates sire more viable offspring. Surprisingly, however, there is no unequivocal evidence for this process. Here, by experimentally assigning mates to females, we show that polyandry greatly increases offspring survival in the Australian marsupial Antechinus stuartii. DNA profiling shows that males that gain high paternity under sperm competition sire offspring that are more viable. This beneficial effect occurs in both the laboratory and the wild. Crucially, there are no confounding non-genetic maternal effects that could arise if polyandry increases female investment in a particular reproductive event because A. stuartii is effectively semelparous. Our results therefore show that polyandry improves female lifetime fitness in nature. The threefold increase in offspring survival is not negated by a decline in maternal lifespan and is too large to be offset by an equivalent decline in the reproductive performance of surviving offspring.     

Microorganisms associated with chromosome destruction and reproductive isolation between two insect species

Microorganisms have been implicated in causing cytoplasmic incompatibility in a variety of insect species, including mosquitoes, fruitflies, beetles and wasps. The effect is typically unidirectional: incompatible crosses produce no progeny or sterile males, whereas the reciprocal crosses produce normal progeny. The parasitic wasp Nasonia vitripennis is one of the few species in which the cytogenetic mechanism of incompatibility is known. In this species the paternal chromosome set forms a tangled mass in a fertilized egg and is eventually lost. Here we report that cytoplasmic microorganisms are associated with complete bidirectional incompatibility between N. vitripennis and a closely related sympatric species, N. giraulti. Microorganisms can be seen in the eggs of both species. Hybrid offspring are normally not produced in crosses between the two species, but do occur after elimination of the microorganisms by antibiotic treatment. A cytogenetic and genetic study shows that bidirectional interspecific incompatibility is due to improper condensation of the paternal chromosomes. Microorganism-mediated reproductive isolation is of interest because it could provide a rapid mode of speciation. The mechanism of incompatibility in Nasonia is also of interest as a potential tool for studying chromosome imprinting and chromosome condensation.     

The genomic basis of adaptive evolution in threespine sticklebacks

Marine stickleback fish have colonized and adapted to thousands of streams and lakes formed since the last ice age, providing an exceptional opportunity to characterize genomic mechanisms underlying repeated ecological adaptation in nature. Here we develop a high-quality reference genome assembly for threespine sticklebacks. By sequencing the genomes of twenty additional individuals from a global set of marine and freshwater populations, we identify a genome-wide set of loci that are consistently associated with marine-freshwater divergence. Our results indicate that reuse of globally shared standing genetic variation, including chromosomal inversions, has an important role in repeated evolution of distinct marine and freshwater sticklebacks, and in the maintenance of divergent ecotypes during early stages of reproductive isolation. Both coding and regulatory changes occur in the set of loci underlying marine-freshwater evolution, but regulatory changes appear to predominate in this well known example of repeated adaptive evolution in nature.