Male mating preferences pre-date the origin of a female trait polymorphism in an incipient species complex of Lake Victoria cichlids

Disruptive sexual selection on colour patterns has been suggested as a major cause of diversification in the cichlid species flock of Lake Victoria. In Neochromis omnicaeruleus, a colour and sex determination polymorphism is associated with a polymorphism in male and female mating preferences. Theoretical work on this incipient species complex found conditions for rapid sympatric speciation by selection on sex determination and sexual selection on male and female colour patterns, under restrictive assumptions. Here we test the biological plausibility of a key assumption of such models, namely, the existence of a male preference against a novel female colour morph before its appearance in the population. We show that most males in a population that lacks the colour polymorphism exhibit a strong mating preference against the novel female colour morph and that reinforcement is not a likely explanation for the origin of such male preferences. Our results show that a specific condition required for the combined action of selection on sex determination and sexual selection to drive sympatric speciation is biologically justified. Finally, we suggest that Lake Victoria cichlids might share an ancestral female recognition scheme, predisposing colour monomorphic populations/species to similar evolutionary pathways leading to divergence of colour morphs in sympatry.     

Disruptive sexual selection on male nuptial coloration in an experimental hybrid population of cichlid fish

Theory suggests that genetic polymorphisms in female mating preferences may cause disruptive selection on male traits, facilitating phenotypic differentiation despite gene flow, as in reinforcement or other models of speciation with gene flow. Very little experimental data have been published to test the assumptions regarding the genetics of mate choice that such theory relies on. We generated a population segregating for female mating preferences and male colour dissociated from other species differences by breeding hybrids between species of the cichlid fish genus Pundamilia. We measured male mating success as a function of male colour. First, we demonstrate that non-hybrid females of both species use male nuptial coloration for choosing mates, but with inversed preferences. Second, we show that variation in female mating preferences in an F2 hybrid population generates a quadratic fitness function for male coloration suggestive of disruptive selection: intermediate males obtained fewer matings than males at either extreme of the colour range. If the genetics of female mate choice in Pundamilia are representative for those in other species of Lake Victoria cichlid fish, it may help explain the origin and maintenance of phenotypic diversity despite some gene flow.     

Sympatric colour polymorphisms associated with nonrandom gene flow in cichlid fish of Lake Victoria

Colour polymorphisms have fascinated evolutionary ecologists for a long time. Yet, knowledge on the mechanisms that allow their persistence is restricted to a handful of well‐studied cases. We studied two species of Lake Victoria cichlid fish, Neochromis omnicaeruleus and Neochromis greenwoodi, exhibiting very similar sex‐linked colour polymorphisms. The ecology and behaviour of one of these species is well studied, with colour‐based mating and aggression preferences. Here, we ask whether the selection potentially resulting from female and male mating preferences and aggression biases reduces gene flow between the colour morphs and permits differentiation in traits other than colour. Over the past 14 years, the frequencies of colour morphs have somewhat oscillated, but there is no evidence for directional change, suggesting the colour polymorphism is persistent on an ecological timescale. We find limited evidence of eco‐morphological differentiation between sympatric ancestral (plain) and derived (blotched) colour morphs. We also find significantly nonrandom genotypic assignment and an excess of linkage disequilibrium in the plain morph, which together with previous information on mating preferences suggests nonrandom mating between colour morphs. This, together with negative frequency‐dependent sexual selection, found in previous studies, may facilitate maintenance of these polymorphisms in sympatry.     

Reinforcement shapes clines in female mate discrimination in Drosophila subquinaria

Reinforcement of species boundaries may alter mate recognition in a way that also affects patterns of mate preference among conspecific populations. In the fly Drosophila subquinaria, females sympatric with the closely related species D. recens reject mating with heterospecific males as well as with conspecific males from allopatric populations. Here, we assess geographic variation in behavioral isolation within and among populations of D. subquinaria and use cline theory to understand patterns of selection on reinforced discrimination and its consequences for sexual isolation within species. We find that selection has fixed rejection of D. recens males in sympatry, while significant genetic variation in this behavior occurs within allopatric populations. In conspecific matings sexual isolation is also asymmetric and stronger in populations that are sympatric with D. recens. The clines in behavioral discrimination within and between species are similar in shape and are maintained by strong selection in the face of gene flow, and we show that some of their genetic basis may be either shared or linked. Thus, while reinforcement can drive extremely strong phenotypic divergence, the long‐term consequences for incipient speciation depend on gene flow, genetic linkage of discrimination traits, and the cost of these behaviors in allopatry.     

Colour pattern as a single trait driving speciation in Hypoplectrus coral reef fishes?

Theory shows that speciation in the presence of gene flow occurs only under narrow conditions. One of the most favourable scenarios for speciation with gene flow is established when a single trait is both under disruptive natural selection and used to cue assortative mating. Here, we demonstrate the potential for a single trait, colour pattern, to drive incipient speciation in the genus Hypoplectrus (Serranidae), coral reef fishes known for their striking colour polymorphism. We provide data demonstrating that sympatric Hypoplectrus colour morphs mate assortatively and are genetically distinct. Furthermore, we identify ecological conditions conducive to disruptive selection on colour pattern by presenting behavioural evidence of aggressive mimicry, whereby predatory Hypoplectrus colour morphs mimic the colour patterns of non-predatory reef fish species to increase their success approaching and attacking prey. We propose that colour-based assortative mating, combined with disruptive selection on colour pattern, is driving speciation in Hypoplectrus coral reef fishes.     

Strong cryptic prezygotic isolation despite lack of behavioral isolation between sympatric host races of the leaf beetle Lochmaea capreae

One of the major goals in speciation research is to understand which isolation mechanisms form the first barriers to gene flow. This requires examining lineages that are still in the process of divergence or incipient species. Here, we investigate the presence of behavioral and several cryptic barriers between the sympatric willow and birch host races of Lochmaea capreae. Behavioral isolation did not have any profound effect on preventing gene flow. Yet despite pairs mating indiscriminately, no offspring were produced from the heterospecific matings between birch females and willow males due to the inability of males to transfer sperm to females. We found evidence for differences in genital morphology that may contribute to failed insemination attempts during copulation. The heterospecific matings between willow females and birch males resulted in viable offspring. Yet fecundity and hatchability was remarkably reduced, which is likely the result of lower efficiency in sperm transportation and storage and lower survival of sperm in the foreign reproductive tract. Our results provide evidence for the contribution of several postmating‐prezygotic barriers that predate behavioral isolation and act as primary inhibitors of gene flow in this system. This is a surprising, yet perhaps often overlooked feature of barriers acting early in sympatric speciation process.     

Mate choice and the genetic basis for colour variation in a polymorphic dart frog: inferences from a wild pedigree

Understanding how reproductive barriers evolve during speciation remains an important question in evolution. Divergence in mating preferences may be a common first step in this process. The striking colour pattern diversity of strawberry dart frog (Dendrobates pumilio) populations has likely been shaped by sexual selection. Previous laboratory studies have shown that females attend to male coloration and prefer to court with males of their own colour, suggesting that divergent morphs may be reproductively isolated. To test this hypothesis, we used molecular data to estimate pedigree relationships from a polymorphic population. Whereas in the laboratory both red and yellow females preferred to court with males of their own phenotype, our pedigree shows a pattern of assortative mating only for red females. In the wild, yellow females appear to be less choosy about their mates, perhaps because they incur higher costs associated with searching than females of the more common red phenotype. We also used our pedigree to investigate the genetic basis for colour-pattern variation. The phenotype frequencies we observed were consistent with those expected if dorsal background coloration is controlled by a single locus, with complete dominance of red over yellow. Our results not only help clarify the role of sexual selection in reducing gene flow, but also shed light on the mechanisms underlying colour-pattern variation among sympatric colour morphs. The difference we observed between mating preferences measured under laboratory conditions and the pattern of mate choice observed in the wild highlight the importance of field studies for understanding behavioural reproductive isolation.     

No barriers to fertilization between sympatric colour morphs in the marine species flock Hypoplectrus (Serranidae)

Assortative mate choice is, so far, the only demonstrated isolating barrier between colour morphs in fish species flocks, such as freshwater cichlids and marine hamlets, suggesting an important role for sexual selection in speciation. However, there has been little consideration of post-copulatory mechanisms that are known to influence reproductive isolation in other taxa. Selective pressures through a cost to hybrid matings, or genetic drift, may lead to the evolution of fertilization barriers through gamete incompatability. In cases of incipient speciation, such as the hamlets, complete fertilization blocks may not have evolved. Instead, differential fertilization between species may reduce the success of interspecific fertilizations. We examined the fertilization dynamics of sympatric Hypoplectrus nigricans (black hamlet) and Hypoplectrus puella (barred hamlet). Experimental crosses were performed to score fertilization success in within-morph and between-morph crosses. Fertilization success did not differ between self-fertilized, within-morph or between-morph crosses. We therefore found no evidence of post-mating barriers through sperm:egg incompatibilities and potential for self-fertilization. Our results are consistent with a mechanism of colour morph divergence based on sexually selected morph mating preferences.     

Similar preferences for ornamentation in opposite‐ and same‐sex choice experiments

Selection due to social interactions comprises competition over matings (sexual selection stricto sensu) plus other forms of social competition and cooperation. Sexual selection explains sex differences in ornamentation and in various other phenotypes, but does not easily explain cases where those phenotypes are similar in males and females. Understanding such similarities requires knowing how phenotypes influence nonsexual social interactions as well, which can be very important in gregarious animals, but whose role for phenotypic evolution has been overlooked. For example, ‘mate choice’ experiments often found preferences for ornamentation, but have not assessed whether those are strictly sexual or are general social preferences. Using choice experiments with a gregarious and mutually ornamented finch, the common waxbill (Estrilda astrild), we show that preferences for ornamentation in the opposite‐sex also extend to same‐sex interactions. Waxbills discriminated between opposite‐ and same‐sex individuals, but most preferences for colour traits were similar when interacting with either sex. Similar preferences in sexual and nonsexual associations may be widespread in nature, either as social adaptations or as by‐product of mate preferences. In either case, such preferences may set the stage for the evolution of mutual ornamentation and of various other similarities between the sexes.     

Interaction between female mating preferences and predation may explain the maintenance of rare males in the pentamorphic fish Poecilia parae

Variation in mating preferences coupled with selective predation may allow for the maintenance of alternative mating strategies. Males of the South American live‐bearing fish Poecilia parae fall in one of five discrete morphs: red, yellow, blue, stripe‐coloured tail (parae) and female mimic (immaculata). Field surveys indicate that the red and yellow morphs are the rarest and that their rarity is consistent across years. We explored the role of variable female mating preference and selective predation by visual predators in explaining the rarity of red and yellow males, and more generally, the maintenance of this extreme colour polymorphism. We presented wild‐caught P. parae females and Aequidens tetramerus, the most common cichlid predator, with the five male colour morphs in separate trials to determine mating and prey preferences, respectively. We found that a large proportion of females shared a strong preference for the rare carotenoid‐based red and yellow males, but a distinct group also preferred the blue and parae morphs. The cichlid predator strongly preferred red and yellow males as prey. Together, these results suggest that the interaction between premating sexual selection favouring and predation acting against the red and yellow morphs may explain their rarity in the wild. The trade‐off between sexual and natural selection, accompanied by variation in female mating preferences, may therefore facilitate the maintenance of the striking colour polymorphism in P. parae.     

Trade-off between warning signal efficacy and mating success in the wood tiger moth

The coloration of species can have multiple functions, such as predator avoidance and sexual signalling, that directly affect fitness. As selection should favour traits that positively affect fitness, the genes underlying the trait should reach fixation, thereby preventing the evolution of polymorphisms. This is particularly true for aposematic species that rely on coloration as a warning signal to advertise their unprofitability to predators. Nonetheless, there are numerous examples of aposematic species showing remarkable colour polymorphisms. We examined whether colour polymorphism in the wood tiger moth is maintained by trade-offs between different functions of coloration. In Finland, males of this species have two distinct colour morphs: white and yellow. The efficacy of the warning signal of these morphs was tested by offering them to blue tits in the laboratory. Birds hesitated significantly longer to attack yellow than white males. In a field experiment, the survival of the yellow males was also higher than white males. However, mating experiments in the laboratory revealed that yellow males had lower mating success than white males. Our results offer an explanation for the maintenance of polymorphism via trade-off between survival selection and mating success.     

Sexual selection and non-random mating for shell colour in a natural population of the marine snailLittorina mariae (Gastropoda: Prosobranchia)

In order to estimate the three independent components of mating behaviour, sexual selection in females, sexual selection in males and mating pattern, we studied the distribution of shell colour morphs among mating pairs and between copulating and non-copulating snails in four subsamples of a natural population ofL. mariae. The colour of the shell, the sex and a qualitative estimate of age was recorded for every snail. We found sexual selection acting against one of the two commonest colours (yellow) among the young females. However, in males none of the eight shell colour morphs was favoured during matings. Male sexual choice or differences in female sexual activity may cause the sexual fitness disadvantage of yellow females. Moreover, individuals of different colour morphs did not mate at random, rather dissasortatively. A behavioural choice among shell colour morphs or a non-random microdistribution of the morphs may cause the departure from random mating in this population.     

Linking intra‐ and interspecific assortative mating: Consequences for asymmetric sexual isolation

Assortative mating is of interest because of its role in speciation and the maintenance of species boundaries. However, we know little about how within‐species assortment is related to interspecific sexual isolation. Most previous studies of assortative mating have focused on a single trait in males and females, rather than utilizing multivariate trait information. Here, we investigate how intraspecific assortative mating relates to sexual isolation in two sympatric and congeneric damselfly species (genus Calopteryx). We connect intraspecific assortment to interspecific sexual isolation by combining field observations, mate preference experiments, and enforced copulation experiments. Using canonical correlation analysis, we demonstrate multivariate intraspecific assortment for body size and body shape. Males of the smaller species mate more frequently with heterospecific females than males of the larger species, which showed less attraction to small heterospecific females. Field experiments suggest that sexual isolation asymmetry is caused by male preferences for large heterospecific females, rather than by mechanical isolation due to interspecific size differences or female preferences for large males. Male preferences for large females and male–male competition for high quality females can therefore counteract sexual isolation. This sexual isolation asymmetry indicates that sexual selection currently opposes a species boundary.     

The evolution of male mate choice in insects: a synthesis of ideas and evidence

Mate choice by males has been recognized at least since Darwin's time, but its phylogenetic distribution and effect on the evolution of female phenotypes remain poorly known. Moreover, the relative importance of factors thought to underlie the evolution of male mate choice (especially parental investment and mate quality variance) is still unresolved. Here I synthesize the empirical evidence and theory pertaining to the evolution of male mate choice and sex role reversal in insects, and examine the potential for male mating preferences to generate sexual selection on female phenotypes. Although male mate choice has received relatively little empirical study, the available evidence suggests that it is widespread among insects (and other animals). In addition to 'precopulatory' male mate choice, some insects exhibit 'cryptic' male mate choice, varying the amount of resources allocated to mating on the basis of female mate quality. As predicted by theory, the most commonly observed male mating preferences are those that tend to maximize a male's expected fertilization success from each mating. Such preferences tend to favour female phenotypes associated with high fecundity or reduced sperm competition intensity. Among insect species there is wide variation in mechanisms used by males to assess female mate quality, some of which (e.g. probing, antennating or repeatedly mounting the female) may be difficult to distinguish from copulatory courtship. According to theory, selection for male choosiness is an increasing function of mate quality variance and those reproductive costs that reduce, with each mating, the number of subsequent matings that a male can perform ('mating investment') Conversely, choosiness is constrained by the costs of mate search and assessment, in combination with the accuracy of assessment of potential mates and of the distribution of mate qualities. Stronger selection for male choosiness may also be expected in systems where female fitness increases with each copulation than in systems where female fitness peaks at a small number of matings. This theoretical framework is consistent with most of the empirical evidence. Furthermore, a variety of observed male mating preferences have the potential to exert sexual selection on female phenotypes. However, because male insects typically choose females based on phenotypic indicators of fecundity such as body size, and these are usually amenable to direct visual or tactile assessment, male mate choice often tends to reinforce stronger vectors of fecundity or viability selection, and seldom results in the evolution of female display traits. Research on orthopterans has shown that complete sex role reversal (i.e. males choosy, females competitive) can occur when male parental investment limits female fecundity and reduces the potential rate of reproduction of males sufficiently to produce a female-biased operational sex ratio. By contrast, many systems exhibiting partial sex role reversal (i.e. males choosy and competitive) are not associated with elevated levels of male parental investment, reduced male reproductive rates, or reduced male bias in the operational sex ratio. Instead, large female mate quality variance resulting from factors such as strong last-male sperm precedence or large variance in female fecundity may select for both male choosiness and competitiveness in such systems. Thus, partial and complete sex role reversal do not merely represent different points along a continuum of increasing male parental investment, but may evolve via different evolutionary pathways.     

Common Wall Lizard Females (Podarcis muralis) do not Actively Choose Males Based on their Colour Morph

Identifying the processes that lead to the evolution and maintenance of links between colour morphs and behavioural strategies has implications for the evolution of reproductive isolation and sympatric speciation. Sexual selection may play a significant role in the evolution of colour pattern complexity in reptiles, particularly when there are fitness consequences associated with mating with males of different colour morphs. In this article, we explored if common wall lizard females (Podarcis muralis) actively select males according to their morph in a colour‐assortative pattern using a multiple‐choice experiment with both visual and chemical cues. We failed to identify female active mate choice, as females did not choose males based on male colouration or femoral pore secretions. Indeed, females equally entered the three preference compartments and spent nearly the same amount of time within them, irrespective of both colour and odour of males. Consequently, our results do not support the hypothesis that colour polymorphism in this species may be driven by colour‐assortative mating promoted by females. However, we cannot exclude the possibility that females may choose males according to their colour following a flexible choice strategy, nor the possibility that females actively discriminate among males according to qualities that are not directly related to morph‐specific strategies.     

Limited male dispersal in a social spider with extreme inbreeding

Cooperatively breeding animals commonly avoid incestuous mating through pre-mating dispersal. However, a few group-living organisms, including the social spiders, have low pre-mating dispersal, intra-colony mating, and inbreeding. This results in limited gene flow among colonies and sub-structured populations. The social spiders also exhibit female-biased sex ratios because survival benefits to large colonies favour high group productivity, which selects against 1 : 1 sex ratios. Although propagule dispersal of mated females may occasionally bring about limited gene flow, little is known about the role of male dispersal. We assessed the extent of male movement between colonies in natural populations both experimentally and by studying colony sex ratios over the mating season. We show that males frequently move to neighbouring colonies, whereas only 4% of incipient nests were visited by dispersing males. Neighbouring colonies are genetically similar and movement within colony clusters does not contribute to gene flow. Post-mating sex ratio bias was high early in the mating season due to protandry, and also in colonies at the end of the season, suggesting that males remain in the colony when mated females have dispersed. Thus, male dispersal is unlikely to facilitate gene flow between different matrilineages. This is consistent with models of non-Fisherian group-level selection for the maintenance of female biased sex ratios, which predict the elimination of male dispersal.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society 2009, 97 , 227–234.     

The Midas cichlid species complex: incipient sympatric speciation in Nicaraguan cichlid fishes?

Abstract Sympatric speciation is a contentious concept, although theoretical models as well as empirical evidence support its relevance in evolutionary biology. The Midas cichlid species complex (Amphilophus citrinellus, labiatus, zaliosus) from several crater lakes in Nicaragua fits several of the key characteristics of a sympatric speciation model. In particular, in A. citrinellus (i) strong assortative mating on the basis of colour polymorphism and (ii) ecological differentiation based on morphological polymorphisms involving the feeding apparatus and body shape might both be mechanisms of incipient speciation. Seven microsatellite markers and mtDNA control region sequences [836 base pairs (bp)] were used to study the population genetic structure of 519 specimens of Midas cichlid populations from the two Great Lakes Managua and Nicaragua, and three crater lakes in Nicaragua, Central America. The three named species of the species complex occupy different ecological niches, are morphologically distinct and can be distinguished genetically. We uncovered allopatric genetic differentiation of populations of A. citrinellus from different lakes and distant locations within Lake Managua and, more interestingly, incipient genetic differentiation of several sympatric populations based on colouration (in A. citrinellus and A. labiatus) but not on the morphology of the pharyngeal jaws (in A. citrinellus). Sexual selection and assortative mating might be the driven forces of diversification within named species. The Midas cichlid species complex in Nicaragua is an excellent model system for the study of the incipient stages of adaptation, speciation and the formation of species flocks.     

COLOR ASSORTATIVE MATING CONTRIBUTES TO SYMPATRIC DIVERGENCE OF NEOTROPICAL CICHLID FISH

It is still debated vigorously whether sexual selection can result in speciation without physical barriers to gene flow. In this study, we used field data and molecular methods to investigate the gold–normal color polymorphism in two endemic cichlid fish species of crater lake Xiloá, Nicaragua. We found significant assortative mating by color in both Amphilophus xiloaensis and A. sagittae . Focusing on A. xiloaensis , microsatellite allele frequencies, an assignment test, and model-based cluster analysis demonstrates significant and clear genetic differentiation ( F _ST= 0.03) between gold and normal individuals in sympatry. In addition, we find genetic differentiation between all three sympatric and ecologically distinct Midas cichlid species of Lake Xiloá, A. amarillo , A. sagittae , and A. xiloaensis ( F _ST= 0.03 – 0.19), and clear genetic isolation of these species from their closest relative ( A. citrinellus ) in the neighboring great lake Managua. The A. xiloaensis gold morph is genetically more distinct from the lake's other two Midas cichlid species than is A. xiloaensis -normal. Thus, we have identified sexual isolation based on color that is evident in population genetics and mate choice. Our results suggest that sexual selection through color assortative mating may play an important role in incipient sympatric speciation in Midas cichlids of Nicaragua.     

The evolution of reproductive character displacement conflicts with how sexual selection operates within a species

Processes that affect the evolution of female preferences or male display traits involved in mating decisions in different geographic areas have the potential to result in within-species divergence. This could occur via reinforcement of mate recognition in species using the same traits for species recognition and sexual selection. Sympatric individuals experience reinforcement of female preferences and male display traits, whereas allopatric individuals do not, creating the potential for divergent sexual selection in sympatric and allopatric populations. Sexual selection operates on the cuticular hydrocarbons (CHCs) of Drosophila serrata, and reinforcement on the CHCs of populations sympatric with D. birchii. Here, we manipulate sexual selection in D. serrata populations generated by hybridizing natural sympatric and allopatric populations. Under the influence of sexual selection, male CHCs evolved from an intermediate phenotype to resemble an allopatric phenotype, which was driven by female choice. Additionally, female choice resulted in evolution of an allopatric female preference, so that allopatric males were preferred to sympatric males. Allopatric CHCs and preferences represent a sexual selection optimum via female choice. Sympatric populations display suboptimal phenotypes relative to their allopatric conspecifics. The combination of reinforcement and sexual selection can therefore generate divergence in female preferences and male display traits.     

The evolution of female‐limited polymorphisms in damselflies: a signal detection model

Female‐limited intraspecific colour variation is a widely distributed trait within damselflies. Typically, one morph resembles the male (the andromorph) whereas one, or sometimes more, do not [the heteromorph(s)]. While several selective explanations have been offered, such as decreased harassment by males balanced by predation or lack of mating success, field data indicate that andromorphs and heteromorphs mate at equal frequencies in the field, and survive equally well. In this paper, I use a signal detection model to characterize the properties of a new male‐mimicry hypothesis, in which andromorphs are not only more similar to males, but are also encountered more by males. I show that this combination of frequency‐dependent and frequency‐independent factors readily combine to generate a balanced polymorphism. The model explains why morphs have similar mean mating frequencies, why the experimentally observed mating preferences of males vary between ponds, and why the frequency of andromorphs tends to rise with sex ratio.