Female mating preference functions predict sexual selection against hybrids between sibling species of cichlid fish

The evolutionary outcome of interspecific hybridization, i.e. collapse of species into a hybrid swarm, persistence or even divergence with reinforcement, depends on the balance between gene flow and selection against hybrids. If female mating preferences are open-ended but sign-inversed between species, they can theoretically be a source of such selection. Cichlid fish in African lakes have sustained high rates of speciation despite evidence for widespread hybridization, and sexual selection by female choice has been proposed as important in the origin and maintenance of species boundaries. However, it had never been tested whether hybridizing species have open-ended preference rules. Here we report the first experimental test using Pundamilia pundamilia, Pundamilia nyererei and their hybrids in three-way choice experiments. Hybrid males are phenotypically intermediate. Wild-caught females of both species have strong preferences for conspecific over heterospecific males. Their responses to F1 hybrid males are intermediate, but more similar to responses to conspecifics in one species and more similar to responses to heterospecifics in the other. We suggest that their mate choice mechanism may predispose haplochromine cichlids to maintain and perhaps undergo phenotypic diversification despite hybridization, and that species differences in female preference functions may predict the potential for adaptive trait transfer between hybridizing species.     

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

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

Cross-fostering Does Not Influence the Mate Preferences and Territorial Behaviour of Males in Lake Victoria Cichlids

The ability to recognise conspecifics in contexts of mate choice and territorial defence may have large effects on an individual's fitness. Understanding the development of assortative behaviour may shed light on how species assortative behaviour evolves and how it may influence reproductive isolation. This is the case not only for female mate preferences, but also for male mate preferences and male territorial behaviour. Here we test with a cross-fostering experiment whether early learning influences male mate preferences and male–male aggression biases in two closely related, sympatrically occurring cichlid species Pundamilia pundamilia and Pundamilia nyererei from Lake Victoria. Males that had been fostered, either by a conspecific female or by a heterospecific female, were tested for their aggression bias, as well as for their mate preferences, in two-way choice tests. Males cross-fostered with conspecific and heterospecific foster mothers selectively directed their aggression towards conspecific intruders. The cross-fostering treatment also did not affect male mate preferences. These results are in striking contrast with the finding that females of these species show a sexual preference for males of the foster species.     

Fitness correlates of male coloration in a Lake Victoria cichlid fish

Sexual selection by female choice has contributed to the rapidevolution of phenotypic diversity in the cichlid fish speciesflocks of East Africa. Yet, very little is known about the ecologicalmechanisms that drive the evolution of female mating preferences.We studied fitness correlates of male nuptial coloration ina member of a diverse Lake Victoria cichlid lineage, Pundamilianyererei. In this species, male red coloration is subject tointraspecific sexual selection by female mate choice. Male nuptialcoloration plays a critical role also in reproductive isolationbetween this species and the closely related sympatric speciesP. pundamilia. Here, we show that P. nyererei male colorationis carotenoid based, illustrating the potential for honest signalingof individual quality. In a wild population, we found that variationin male coloration was not associated with variation in a setof strongly intercorrelated indicators of male dominance: malesize, territory size, and territory location. Instead, the 2male characters that predominantly determine female choice,territory size and red coloration, may be independent predictorsof male quality: males with bright red coloration and largeterritories had lower parasite infestation rates. As a result,female preferences tended to select against heavily parasitizedmales. Consistent with parasite-mediated sexual selection, maleshad higher and more variable parasite loads than females.     

Female mating preferences and male coloration covary with water transparency in a Lake Victoria cichlid fish

Rapid speciation in Lake Victoria cichlid fish of the genus Pundamilia may be facilitated by sexual selection: female mate choice exerts sexual selection on male nuptial coloration within species and maintains reproductive isolation between species. However, declining water transparency coincides with increasingly dull coloration and increasing hybridization. In the present study, we investigated the mechanism underlying this pattern in Pundamilia nyererei, a species that interbreeds with a sister species in turbid but not in clear water. We compared measures of intraspecific sexual selection between two populations from locations that differ in water transparency. First, in laboratory mate‐choice experiments, conducted in clear water and under broad‐spectrum illumination, we found that females originating from turbid water have significantly weaker preferences for male coloration than females originating from clear water. Second, both the hue and body coverage of male coloration differ between populations, which is consistent with adaptation to different photic habitats. These findings suggest that the observed relationship between male coloration and water transparency is not mediated by environmental variation alone. Rather, female mating preferences are indicated to have changed in response to this variation, constituting the first evidence for intraspecific preference‐trait co‐evolution in cichlid fish. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 398–406.     

Quantification of sexual dimorphism in Asellus aquaticus (Crustacea: Isopoda) using outline approaches

A marked sexual dimorphism is often observed in arthropods species in which males perform precopulatory mate guarding. It is generally thought to reflect the influence of sexual selection. Until now, sexual dimorphisms associated with mate guarding have mainly been qualitatively described. However, assessing the effects of sexual selection on sexual dimorphims requires a preliminary quantitative assessment of differences in morphology between sexes. Using Fourier analyses, we tested if morphological dimorphisms could be quantitatively assessed in the isopod Asellus aquaticus . In addition, we checked whether sexual dimorphism in shape was exclusively related to mate guarding through considering characters that are not, a priori , implicated in mating behaviour. To assess the potential role of sexual selection in shaping morphology, we then examined how dimorphic characters could influence males' pairing success. Three characters (pleotelson, paraeopods 4 and 5) differed significantly in shape between males and females. In addition, two characters (pleotelson and paraeopods 4) differed in shape between guarding males and non-guarding males, with the latter being closer in shape to females. This suggests that sexual selection may be partly responsible for the observed morphological divergence between sexes in A. aquaticus .  © 2002 The Linnean Society of London, Biological Society of the Linnean Society , 2002, 77 , 523–533.     

Developmental effects of visual environment on species‐assortative mating preferences in Lake Victoria cichlid fish

Local adaptation can be a potent force in speciation, with environmental heterogeneity leading to niche specialization and population divergence. However, local adaption often requires nonrandom mating to generate reproductive isolation. Population divergence in sensory properties can be particularly consequential in speciation, affecting both ecological adaptation and sexual communication. Pundamilia pundamila and Pundamilia nyererei are two closely related African cichlid species that differ in male coloration, blue vs. red. They co‐occur at rocky islands in southern Lake Victoria, but inhabit different depth ranges with different light environments. The species differ in colour vision properties, and females exert species‐specific preferences for blue vs. red males. Here, we investigated the mechanistic link between colour vision and preference, which could provide a rapid route to reproductive isolation. We tested the behavioural components of this link by experimentally manipulating colour perception – we raised both species and their hybrids under light conditions mimicking shallow and deep habitats – and tested female preference for blue and red males under both conditions. We found that rearing light significantly affected female preference: shallow‐reared females responded more strongly to P. pundamilia males and deep‐reared females favoured P. nyererei males – implying that visual development causally affects mate choice. These results are consistent with sensory drive predictions, suggesting that the visual environment is key to behavioural isolation of these species. However, the observed plasticity could also make the species barrier vulnerable to environmental change: species‐assortative preferences were weaker in females that were reared in the other species’ light condition.     

Preference polymorphism for coloration but no speciation in a population of Lake Victoria cichlids

Female mating preference based on male nuptial coloration hasbeen suggested to be an important source of diversifying selectionin the radiation of Lake Victoria cichlid fish. Initial variationin female preference is a prerequisite for diversifying selection;however, it is rarely studied in natural populations. In clearwater areas of Lake Victoria, the sibling species Pundamiliapundamilia with blue males and Pundamilia nyererei with redmales coexist, intermediate phenotypes are rare, and most femaleshave species-assortative mating preferences. Here, we studya population of Pundamilia that inhabits turbid water wheremale coloration is variable from reddish to blue with most malesintermediate. We investigated male phenotype distribution andfemale mating preferences. Male phenotype was unimodally distributedwith a mode on intermediate color in 1 year and more blue-shiftedin 2 other years. In mate choice experiments with females ofthe turbid water population and males from a clearer water population,we found females with a significant and consistent preferencefor P. pundamilia (blue) males, females with such preferencesfor P. nyererei (red) males, and many females without a preference.Hence, female mating preferences in this population could causedisruptive selection on male coloration that is probably constrainedby the low signal transduction of the turbid water environment.We suggest that if environmental signal transduction was improvedand the preference/color polymorphism was stabilized by negativefrequency-dependent selection, divergent sexual selection mightseparate the 2 morphs into reproductively isolated species resemblingthe clear water species P. pundamilia and P. nyererei.     

Mechanisms of species divergence through visual adaptation and sexual selection: Perspectives from a cichlid model sys-tem

The theory of ecological speciation suggests that assortative mating evolves most easily when mating preferences are directly linked to ecological traits that are subject to divergent selection. Sensory adaptation can play a major role in this process, because selective mating is often mediated by sexual signals: bright colours, complex song, pheromone blends and so on. When divergent sensory adaptation affects the perception of such signals, mating patterns may change as an immediate consequence. Alternatively, mating preferences can diverge as a result of indirect effects: assortative mating may be promoted by selection against intermediate phenotypes that are maladapted to their (sensory) environment. For Lake Victoria cichlids, the visual envi-ronment constitutes an important selective force that is heterogeneous across geographical and water depth gradients. We investi-gate the direct and indirect effects of this heterogeneity on the evolution of female preferences for alternative male nuptial colours (red and blue) in the genus Pundamilia. Here, we review the current evidence for divergent sensory drive in this system, extract general principles, and discuss future perspectives.     

Divergent host plant adaptation drives the evolution of sexual isolation in the grasshopper Hesperotettix viridis (Orthoptera: Acrididae) in the absence of reinforcement

Early stages of lineage divergence in insect herbivores are often related to shifts in host plant use and divergence in mating capabilities, which may lead to sexual isolation of populations of herbivorous insects. We examined host preferences, degree of differentiation in mate choice, and divergence in cuticular morphology using near‐infrared spectroscopy in the grasshopper Hesperotettix viridis aiming to understand lineage divergence. In Kansas (USA), H. viridis is an oligophagous species feeding on Gutierrezia and Solidago host species. To identify incipient mechanisms of lineage divergence and isolation, we compared host choice, mate choice, and phenotypic divergence among natural grasshopper populations in zones of contact with populations encountering only one of the host species. A significant host‐based preference from the two host groups was detected in host‐paired feeding preference studies. No‐choice mate selection experiments revealed a preference for individuals collected from the same host species independent of geographic location, and little mating was observed between individuals collected from different host species. Female mate choice tests between males from the two host species resulted in 100% fidelity with respect to host use. Significant differentiation in colour and cuticular composition of individuals from different host plants was observed, which correlated positively with host choice and mate choice. No evidence for reinforcement in the zone of contact was detected, suggesting that divergent selection for host plant use promotes sexual isolation in this species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 866–878.     

Divergent hormonal responses to social competition in closely related species of haplochromine cichlid fish

The diverse cichlid species flocks of the East African lakes provide a classical example of adaptive radiation. Territorial aggression is thought to influence the evolution of phenotypic diversity in this system. Most vertebrates mount hormonal (androgen, glucocorticoid) responses to a territorial challenge. These hormones, in turn, influence behavior and multiple aspects of physiology and morphology. Examining variation in competition-induced hormone secretion patterns is thus fundamental to an understanding of the mechanisms of phenotypic diversification. We test here the hypothesis that diversification in male aggression has been accompanied by differentiation in steroid hormone levels. We studied two pairs of sibling species from Lake Victoria belonging to the genera Pundamilia and Mbipia. The two genera are ecologically differentiated, while sibling species pairs differ mainly in male color patterns. We found that aggression directed toward conspecific males varied between species and across genera: Pundamilia nyererei males were more aggressive than Pundamilia pundamilia males, and Mbipia mbipi males were more aggressive than Mbipia lutea males. Males of both genera exhibited comparable attack rates during acute exposure to a novel conspecific intruder, while Mbipia males were more aggressive than Pundamilia males during continuous exposure to a conspecific rival, consistent with the genus difference in feeding ecology. Variation in aggressiveness between genera, but not between sibling species, was reflected in androgen levels. We further found that M. mbipi displayed lower levels of cortisol than M. lutea. Our results suggest that concerted divergence in hormones and behavior might play an important role in the rapid speciation of cichlid fishes.     

Sensory drive in cichlid speciation

The role of selection in speciation is a central yet poorly understood problem in evolutionary biology. The rapid radiations of extremely colorful cichlid fish in African lakes have fueled the hypothesis that sexual selection can drive species divergence without geographical isolation. Here we present experimental evidence for a mechanism by which sexual selection becomes divergent: in two sibling species from Lake Victoria, female mating preferences for red and blue male nuptial coloration coincide with their context-independent sensitivities to red and blue light, which in turn correspond to a difference in ambient light in the natural habitat of the species. These results suggest that natural selection on visual performance, favoring different visual properties in different spectral environments, may lead to divergent sexual selection on male nuptial coloration. This interplay of ecological and sexual selection along a light gradient may provide a mechanism of rapid speciation through divergent sensory drive.     

The role of physiology in the divergence of two incipient cichlid species

Sexual selection on male coloration has been implicated in the evolution of colourful species flocks of East African cichlid fish. During adaptive radiations, animals diverge in multiple phenotypic traits, but the role of physiology has received limited attention. Here, we report how divergence in physiology may contribute to the stable coexistence of two hybridizing incipient species of cichlid fish from Lake Victoria. Males of Pundamilia nyererei (males are red) tend to defeat those of Pundamilia pundamilia (males are blue), yet the two sibling species coexist in nature. It has been suggested that red males bear a physiological cost that might offset their dominance advantage. We tested the hypothesis that the two species differ in oxidative stress levels and immune function and that this difference is correlated with differences in circulating steroid levels. We manipulated the social context and found red males experienced significantly higher oxidative stress levels than blue males, but only in a territorial context when colour and aggression are maximally expressed. Red males exhibited greater aggression levels and lower humoral immune response than blue males, but no detectable difference in steroid levels. Red males appear to trade off increased aggressiveness with physiological costs, contributing to the coexistence of the two species. Correlated divergence in colour, behaviour and physiology might be widespread in the dramatically diverse cichlid radiations in East African lakes and may play a crucial role in the remarkably rapid speciation of these fish.     

Stifled sex in sympatry: patterns of sexual incompatibility among desmognathine salamanders

Sexual incompatibility due to differences in mate-recognition systems can be an important factor in preventing hybridization and gene flow between animal populations in sympatry. We tested in the laboratory for sexual incompatibility between populations of two species of desmognathine salamanders that occur in sympatry in south-eastern Kentucky, North America, Desmognathus monticola and D. welteri (Caudata: Plethodontidae: Desmognathinae). Spermatophore deposition and insemination (two related measures of sexual success) were frequent in intraspecific encounters, but interspecific encounters never resulted in the deposition of spermatophores by males (Experiment 1). The sexual behaviour patterns of these two species are similar qualitatively, but all encounters staged between them failed to progress beyond the most preliminary of courtship interactions (Experiment 2), perhaps due to species differences in chemosensory communication. Our data on sexual incompatibility between D. monticola and D. welteri are similar to those available for other desmognathine taxa that occur in sympatry. Review of a broader data-set on patterns of sexual incompatibility both within and between species, and in allopatry and in sympatry, provides evidence for both divergence of mate-recognition systems in allopatry and enhancement of sexual incompatibility in sympatry for desmognathine salamanders. We hypothesize that diversification in allopatry may be a consequence of natural and/or sexual selection acting to promote sexual success within populations. Enhancement in sympatry may be a consequence of subsequent selection for accurate species recognition under the threat of hybridization or gene flow between species.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 367–375.     

Limited mitochondrial DNA introgression in a Bombina hybrid zone

We analysed the variation at mitochondrial DNA (mtDNA) and six allozyme loci in two transects across a hybrid zone between the fire-bellied toads Bombina bombina and Bombina variegata in southern Poland. The mtDNA cline was narrower than allozyme clines in one transect (Przemyśl, β = 0.435, w  = 3.42 km) and shifted to the B .  bombina side in both (near Kraków by 1.32 km, α = 0.437, and near Przemyśl by 0.97 km, α = 0.319). Cytonuclear associations were weak. Narrowed mtDNA clines could be a by-product of female demography and lowered effective population size of mtDNA. Alternatively, restricted mtDNA introgression is a likely result of negative epistasis in recombinants augmented by environment-dependent selection because divergence of Bombina mitochondrial and nuclear genomes is large. The shift of the mtDNA cline, contrary to expectations from initial mating preferences and fecundity differences between the species, suggests that on the B .  bombina side of the zone hybrid females with B .  variegata mtDNA have a higher chance of leaving progeny.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 295–306.     

SEXUALLY TRANSMITTED DISEASE AND PARASITE-MEDIATED SEXUAL SELECTION

Few studies have investigated the consequences of parasite-mediated sexual selection on the parasites involved. In some cases parasite-mediated sexual selection could lead to increased virulence, but I develop a simple model that shows that, if a parasite is sexually transmitted (i.e., is a sexually transmitted disease, or STD) and if mating success of the host is adversely affected by the parasite, then less virulent STDs will be selected for because transmission of the STD depends on the mating success of the host. This selection for reduced virulence could have important consequences for the role of STDs in sexual selection.     

Sexual selection as a promoter of population divergence in male phenotypic characters: a study on mainland and islet lizard populations

Sexual selection is often viewed as a promoter of population divergence, although some forms of sexual selection could rather hamper divergence. In the present study, we investigated whether sexual selection promotes divergence in sexually‐selected traits. We studied population variation in sexual selection in relation to colour morph and body size in islet and mainland populations of the Skyros wall lizard (Podarcis gaigeae). Females were most likely to mate with orange‐throated males with small body sizes, and male body size and coloration were therefore subject to correlational sexual selection. By contrast, male mating probabilities were not affected by any female phenotypic character. We also found variation in a female resistance trait (escape propensity), with females being more prone to escape when exposed to males from other habitats. Sexual selection could potentially affect the frequencies of throat colour morphs in this species by favouring orange‐throated males of small body size, although there was no evidence of sexual selection for local mates or rare phenotypes. The results obtained in the present study thus do not support a role for sexual selection as a promoter of population divergence in this species. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 374–389.     

Feeding innovations and parasitism in birds

The rate of behavioural innovation, such as opportunistic feeding innovation, may facilitate adaptation to novel environments. Because parasites may affect how their hosts adopt novel means of resource acquisition, or because opportunistic behaviours may involve the risk of being exposed to a large parasite fauna, we hypothesize an evolutionary link between the rate of feeding innovations and parasitism. We investigated the phylogenetic relationship between relative frequency of feeding innovations (adjusted for research effort and population size) and relative size of immune defense organs (as a relative measure of parasite-mediated selection) and the prevalence of blood parasites in birds. Using generalized least squares models, we found that species with relatively large bursa of Fabricius, thymus, and spleen had higher rates of feeding innovations than species with small immune defense organs. Similarly, there was a positive interspecific association between feeding innovation and haematozoa prevalence. These relationships were not confounded by migration, relative brain size, geographical distribution, and male plumage brightness. Analyses of causality relying on evolutionary modelling of discrete variables and path analysis suggest that increasing rate of feeding innovation may place species under intense selection due to parasitism. Therefore, behavioural adaptation by feeding innovation seems to have consequences for the coevolutionary arm race between parasites and hosts.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 441–455.     

EFFECT OF ECTOPARASITIC MITES ON SEXUAL SELECTION IN A SONORAN DESERT FRUIT FLY

We conducted a field study and a laboratory experiment to test whether ectoparasitic mites, Macrocheles subbadius, generate parasite-mediated sexual selection in the Sonoran desert endemic fruit fly, Drosophila nigrospiracula. Male flies gather on the outer surfaces of necrotic saguaro cacti where they engage in male–male competitive interactions and vigorous female-directed courtship. At these sites, operational sex ratios were significantly skewed toward males. The degree to which mites were aggregated among flies varied across the 25 fly populations sampled. The degree of mite aggregation across fly populations was strongly positively related to the mean number of mites per fly (intensity of infestation). Both the intensity and prevalence of infestation (fraction of flies infested) increased with the age of the cactus necrosis. Infested flies of both sexes were significantly less likely to be found in copula than uninfested flies, and mean intensity of infestation was significantly more pronounced in noncopulating than in copulating flies. The effect of attached mites on copulatory success exhibited dose-dependency, and this effect was more stringent in males: males or females with more than two and four mites, respectively, were never found in copula. The magnitude of parasite-mediated sexual selection was estimated for 12 fly populations by calculating selection differentials for each sex separately. The relation between intensity of infestation and magnitude of parasite-mediated sexual selection was stronger in males but significant for both sexes. We also assayed copulatory success of field-caught males in the laboratory, both during infestation and after experimental removal of mites. Males infested with two mites copulated less frequently than uninfested individuals, and in mating trials after mites had been removed, previously infested males copulated as many times as flies with no history of infestation. These findings, and the lack of difference in the number of mite-induced scars on copulating and single individuals in nature, strongly suggest that the reduced copulatory success of infested flies is attributable to an effect of mites per se, rather than to a character correlated with parasitism or previous parasite infestation.     

Hierarchical comparative analysis of genetic and genitalic geographical structure: testing patterns of male and female genital evolution in the scarab beetle Phyllophaga hirticula (Coleoptera: Scarabaeidae)

It is generally accepted that genitalia are among the fastest evolving characters in insects and that selection on these structures may increase speciation rates in groups with polygamous mating systems. If selection is causing genitalic divergence between or among populations of a species, one prediction is that geographical structure of genitalic morphology would be in place before genetic structure of a rapidly evolving neutral marker. The current study tests this hypothesis in the geographically widespread scarab beetle Phyllophaga hirticula by evaluating whether standing variation in male and female genitalia is more or less geographically structured than a mitochondrial genetic marker. Geographical structure of mitochondrial (mt)DNA and male and female genitalic shape were analysed using analysis of variance, multivariate analysis of variance, Mantel tests, and tests of spatial autocorrelation. The results show that, although female genitalia are more geographically structured than mtDNA, male genitalia are not. This pattern suggests that selection on female genitalic variation may be causing divergence of these structures among populations.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 135–149.