Invasion and fixation of sex-reversal genes

We simulated a meta-population with random dispersal among demes but local mating within demes to investigate conditions under which a dominant female-determining gene W, with no individual selection advantage, can invade and become fixed in females, changing the population from male to female heterogamety. Starting with one mutant W in a single deme, the interaction of sex ratio selection and random genetic drift causes W to be fixed among females more often than a comparable neutral mutation with no influence on sex determination, even when YY males have slightly reduced viability. Meta-population structure and interdeme selection can also favour the fixation of W. The reverse transition from female to male heterogamety can also occur with higher probability than for a comparable neutral mutation. These results help to explain the involvement of sex-determining genes in the evolution of sex chromosomes and in sexual selection and speciation.

Carotenoid-based plumage colors and immune function: Is there a trade-off for rare carotenoids?

Theory suggests that carotenoid-based signals are used in animal communication because they contain specific information about parasite resistance or immunocompetence. This implies that honesty of carotenoid-based signals is maintained by a trade-off between pigmentation and immune function for carotenoids, assuming that the carotenoids used for coloration are also immunoenhancing. We tested this hypothesis by altering the diets of nestling great tits (Paris major) with supplementary beadlets containing the carotenoids that are naturally ingested with food or beadlets containing the carotenoids that are incorporated into the feathers; a control group received beadlets containing no carotenoids. We simultaneously immune challenged half of the nestlings of each supplementation group, using a two-factorial design. Activatior of the immune system led to reduced color expression. However, only nestlings fed with the naturally ingested carotenoids and not with the carotenoids deposited in the feathers showed an increased cellular immune response. This shows that the carotenoids used for ornamentation do not promote the immune function, which conflicts with the trade-off hypothesis. Our results indicate that honesty of carotenoid-based signals is maintained by an individual's physiological limitation to absorb and/or transport carotenoids and by access to carotenoids, indicating that preferences for carotenoid-based traits in sexual selection or parent-offspring interactions select for competitive individuals, rather than specifically for immune function.

Parallel evolution of facial stripe patterns in the Neolamprologus brichardilpulcher species complex endemic to Lake Tanganyika

Colour pattern diversity can be due to random processes or to natural or sexual selection. Consequently, similarities in colour patterns are not always correlated with common ancestry, but may result from convergent evolution under shared selection pressures or drift. Neolamprologus brichardi and Neolamprologus pulcher have been described as two distinct species based on differences in the arrangement of two dark bars on the operculum. Our study uses DNA sequences of the mitochondrial control region to show that relatedness of haplotypes disagrees with species assignment based on head colour pattern. This suggests repeated parallel evolution of particular stripe patterns. The complete lack of shared haplotypes between populations of the same or different phenotypes reflects strong philopatric behaviour, possibly induced by the cooperative breeding mode in which offspring remain in their natal territory and serve as helpers until they disperse to nearby territories or take over a breeding position. Concordant phylogeographic patterns between N. brichardi/N. pulcher populations and other rock-dwelling cichlids suggest that the same colonization routes have been taken by sympatric species and that these routes were affected by lake level fluctuations in the past. (C) 2007 Elsevier Inc. All rights reserved.

Reproductive parasitism: male and female responses to conspecific and heterospecific intrusions at spawning in a mouth-brooding cichlid Ophthalmotilapia ventralis

A rare form of alternative reproductive behaviour without simultaneous parasitic spawning was observed in Ophthalmotilapia ventralis, a lekking mouth-brooding cichlid from Lake Tanganyika. Floater males attempted to sneak opportunistically into the territory to actively court the female, while the owner (bourgeois male) defended the territory against other potential intruders. Floater males had more body fat than territory owners and generally higher condition factors. In field experiments, the response of bourgeois males and courted females was tested towards floaters and egg predators (a catfish Synodontis multipunctatus) present in the territories. Territory owners responded aggressively particularly to floaters, and female responsiveness to bourgeois male courtship tended to decline when floaters were present. The potential influence of reproductive parasitism on sexual selection in mouth-brooding cichlids is discussed.

Mapping Individual Variation in Male Mating Preference Space: Multiple Choice in a Color Polymorphic Cichlid Fish

Sexual selection theory largely rests on the assumption that populations contain individual variation in mating preferences and that individuals are consistent in their preferences. However, there are few empirical studies of within-population variation and even fewer have examined individual male mating preferences. Here, we studied a color polymorphic population of the Lake Victoria cichlid fish Neochromis omnicaeruleus, a species in which color morphs are associated with different sex-determining factors. Wild-caught males were tested in three-way choice trials with multiple combinations of different females belonging to the three color morphs. Compositional log-ratio techniques were applied to analyze individual male mating preferences. Large individual variation in consistency, strength, and direction of male mating preferences for female color morphs was found and hierarchical clustering of the compositional data revealed the presence of four distinct preference groups corresponding to the three color morphs in addition to a no-preference class. Consistency of individual male mating preferences was higher in males with strongest preferences. We discuss the implications of these findings for our understanding of the mechanisms underlying polymorphism in mating preferences.

Sex-specific clines support incipient speciation in a common European mammal

Hybrid zones provide excellent opportunities to study processes and mechanisms underlying reproductive isolation and speciation. Here we investigated sex-specific clines of molecular markers in hybrid zones of morphologically cryptic yet genetically highly-diverged evolutionary lineages of the European common vole (Microtus arvalis). We analyzed the position and width of four secondary contact zones along three independent transects in the region of the Alps using maternally (mitochondrial DNA) and paternally (Y-chromosome) inherited genetic markers. Given male-biased dispersal in the common vole, a selectively neutral secondary contact would show broader paternal marker clines than maternal ones. In a selective case, for example, involving a form of Haldane’s rule, Y-chromosomal clines would not be expected to be broader than maternal markers because they are transmitted by the heterogametic sex and thus gene flow would be restricted. Consistent with the selective case, paternal clines were significantly narrower or at most equal in width to maternal clines in all contact zones. In addition, analyses using maximum likelihood cline-fitting detected a shift of paternal relative to maternal clines in three of four contact zones. These patterns suggest that processes at the contact zones in the common vole are not selectively neutral, and that partial reproductive isolation is already established between these evolutionary lineages. We conclude that hybrid zone movement, sexual selection and/or genetic incompatibilities are likely associated with an unusual unidirectional manifestation of Haldane’s rule in this common European mammal.

Direct male-male competition can facilitate invasion of new colour types in Lake Victoria cichlids

The possibility that disruptive sexual selection alone can cause sympatric speciation is currently a subject of much debate. The initial difficulty for new and rare ornament phenotypes to invade a population, and the stabilisation of the resulting polymorphism in trait and preference make this hypothesis problematic. Recent theoretical work indicates that the invasion is facilitated if males with the new phenotype have an initial advantage in male-male competition. We studied a pair of sympatric incipient species of cichlids from Lake Victoria, in which the red (Pundamilia nyererei) and blue males (P. pundamilia) vigorously defend territories. Other studies suggested that red phenotypes may have repeatedly invaded blue populations in independent episodes of speciation. We hypothesised that red coloration confers an advantage in male-male competition, assisting red phenotypes to invade. To test this hypothesis, we staged contests between red and blue males from a population where the phenotypes are interbreeding morphs or incipient species. We staged contests under both white and green light condition. Green light effectively masks the difference between red and blue coloration. Red males dominated blue males under white light, but their competitive advantage was significantly diminished under green light. Contests were shorter when colour differences were visible. Experience of blue males with red males did not affect the outcome of a contest. The advantage of red over blue in combats may assist the red phenotype to invade blue populations. The apparently stable co-existence of red and blue incipient species in many populations of Lake Victoria cichlids is discussed.

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.

EVOLUTION OF DOMINANCE UNDER FREQUENCY-DEPENDENT INTRASPECIFIC COMPETITION IN AN ASSORTATIVELY MATING POPULATION

We study the evolution of higher levels of dominance as a response to negative frequency-dependent selection. In contrast to previous studies, we focus on the effect of assortative mating on the evolution of dominance under frequency-dependent intraspecific competition. We analyze a two-locus two-allele model, in which the primary locus has a major effect on a quantitative trait that is under a mixture of frequency-independent stabilizing selection, density-dependent selection, and frequency-dependent selection caused by intraspecific competition for a continuum of resources. The second (modifier) locus determines the degree of dominance at the trait level. Additionally, the population mates assortatively with respect to similarities in the ecological trait. Our analysis shows that the parameter region in which dominance can be established decreases if small levels of assortment are introduced. In addition, the degree of dominance that can be established also decreases. In contrast, if assortment is intermediate, sexual selection for extreme types can be established, which leads to evolution of higher levels of dominance than under random mating. For modifiers with large effects, intermediate levels of assortative mating are most favorable for the evolution of dominance. For large modifiers, the speed of fixation can even be higher for intermediate levels of assortative mating than for random mating.

The Underwater Photic Environment of Cape Maclear, Lake Malawi: Comparison Between Rock- and Sand-Bottom Habitats and Implications for Cichlid Fish Vision

Lake Malawi boasts the highest diversity of freshwater fishes in the world. Nearshore sites are categorized according to their bottom substrate, rock or sand, and these habitats host divergent assemblages of cichlid fishes. Sexual selection driven by mate choice in cichlids led to spectacular diversification in male nuptial coloration. This suggests that the spectral radiance contrast of fish, the main determinant of visibility under water, plays a crucial role in cichlid visual communication. This study provides the first detailed description of underwater irradiance, radiance and beam attenuation at selected sites representing two major habitats in Lake Malawi. These quantities are essential for estimating radiance contrast and, thus, the constraints imposed on fish body coloration. Irradiance spectra in the sand habitat were shifted to longer wavelengths compared with those in the rock habitat. Beam attenuation in the sand habitat was higher than in the rock habitat. The effects of water depth, bottom depth and proximity to the lake bottom on radiometric quantities are discussed. The radiance contrast of targets exhibiting diffused and spectrally uniform reflectance depended on habitat type in deep water but not in shallow water. In deep water, radiance contrast of such targets was maximal at long wavelengths in the sand habitat and at short wavelengths in the rock habitat. Thus, to achieve conspicuousness, color patterns of rock-and sand-dwelling cichlids would be restricted to short and long wavelengths, respectively. This study provides a useful platform for the examination of cichlid visual communication.

Evolution of colour patterns in East African cichlid fish

African cichlid fishes have undergone outbursts of explosive speciation in several lakes, accompanied by rapid radiations in coloration and ecology. Little is known about the evolutionary forces that triggered these events but a hypothesis, published by Wallace Dominey in 1984, has figured prominently. It states that the evolution of colour patterns is driven by sexual selection and that these colour patterns are important in interspecific mate choice, a combination which holds the potential for rapid speciation. Here we present phylogenetic analyses that describe major events in colour evolution and test predictions yielded by Dominey's hypothesis. We assembled information on stripe patterns and the presence or absence of nuptial coloration from more than 700 cichlid species representing more than 90 taxa for which molecular phylogenetic hypotheses were available. We show that sexual selection is most likely the selection force that made male nuptial coloration arise and evolve quickly. In contrast, stripe patterns, though phylogenetically not conserved either, are constrained ecologically. The evolution of vertical bar patterns is associated with structurally complex habitats, such as rocky substrates or vegetation. The evolution of a horizontal stripe is associated with a piscivorous feeding mode. Horizontal stripes are also associated with shoaling behaviour. Strength of sexual selection, measured in terms of the mating system (weak in monogamous, strong in promiscuous species), has no detectable effects on stripe pattern evolution. In promiscuous species the frequency of difference between sister species in nuptial hue is higher than in pair bonding and harem forming species, but the frequency of difference in stripe pattern is lower. We argue that differences between the two components of coloration in their exposure to natural selection explain their very different evolutionary behaviour. Finally, we suggest that habitat-mediated selection upon chromomotor flexibility, a special form of phenotypic plasticity found in the river-dwelling outgroups of the lake-dwelling cichlids, explains the rapid and recurrent ecology-associated radiation of stripe patterns in lake environments, a new hypothesis that yields experimentally testable predictions.

The effect of male coloration on female mate choice in closely related Lake Victoria cichlids (Haplochromis nyererei complex)

We studied the effect of male coloration on interspeciÆc female mate choice in two closely related species of haplochromine cichlids from Lake Victoria. The species differ primarily in male coloration. Males of one species are red, those of the other are blue. We re- corded the behavioral responses of females to males of both species in paired male trials under white light and under monochromatic light, under which the interspecific differences in coloration were masked. Females of both species exhibited species-assortative mate choice when colour differences were visible, but chose non-assortatively when colour differences were masked by light conditions. Neither male behaviour nor overall female response frequencies differed between light treatments. That female preferences could be altered by manipulating the perceived colour pattern implies that the colour itself is used in interspecific mate choice, rather than other characters. Hence, male coloration in haplochromine cichlids does underlie sexual selection by direct mate choice, involving the capacity for individual assessment of potential mates by the female. Females of both species responded more frequently to blue males under monochromatic light. Blue males were larger and displayed more than red males. This implies a hierarchy of choice criteria. Females may use male display rates, size, or both when colour is unavailable. Where available, colour has gained dominance over other criteria. This may explain rapid speciation by sexual selection on male coloration, as proposed in a recent mathematical model.

Genomics of Rapid Incipient Speciation in Sympatric Threespine Stickleback

Ecological speciation is the process by which reproductively isolated populations emerge as a consequence of divergent natural or ecologically-mediated sexual selection. Most genomic studies of ecological speciation have investigated allopatric populations, making it difficult to infer reproductive isolation. The few studies on sympatric ecotypes have focused on advanced stages of the speciation process after thousands of generations of divergence. As a consequence, we still do not know what genomic signatures of the early onset of ecological speciation look like. Here, we examined genomic differentiation among migratory lake and resident stream ecotypes of threespine stickleback reproducing in sympatry in one stream, and in parapatry in another stream. Importantly, these ecotypes started diverging less than 150 years ago. We obtained 34,756 SNPs with restriction-site associated DNA sequencing and identified genomic islands of differentiation using a Hidden Markov Model approach. Consistent with incipient ecological speciation, we found significant genomic differentiation between ecotypes both in sympatry and parapatry. Of 19 islands of differentiation resisting gene flow in sympatry, all were also differentiated in parapatry and were thus likely driven by divergent selection among habitats. These islands clustered in quantitative trait loci controlling divergent traits among the ecotypes, many of them concentrated in one region with low to intermediate recombination. Our findings suggest that adaptive genomic differentiation at many genetic loci can arise and persist in sympatry at the very early stage of ecotype divergence, and that the genomic architecture of adaptation may facilitate this.

Female preference for swords in Xiphophorus helleri reflects a bias for large apparent size

Swordtail fish (Poeciliidae: genus Xiphophorus) are a paradigmatic case of sexual selection by sensory exploitation. Female preference for males with a conspicuous “sword” ornament is ancestral, suggesting that male morphology has evolved in response to a preexisting bias. The perceptual mechanisms underlying female mate choice have not been identified, complicating efforts to understand the selection pressures acting on ornament design. We consider two alternative models of receiver behavior, each consistent with previous results. Females could respond either to specific characteristics of the sword or to more general cues, such as the apparent size of potential mates. We showed female swordtails a series of computer-altered video sequences depicting a courting male. Footage of an intact male was preferred strongly to otherwise identical sequences in which portions of the sword had been deleted selectively, but a disembodied courting sword was less attractive than an intact male. There was no difference between responses to an isolated sword and to a swordless male of comparable length, or between an isolated sword and a homogenous background. Female preference for a sworded male was abolished by enlarging the image of a swordless male to compensate for the reduction in length caused by removing the ornament. This pattern of results is consistent with mate choice being mediated by a general preference for large males rather than by specific characters. Similar processes may account for the evolution of exaggerated traits in other systems.

Ultraviolet plumage colors predict mate preferences in starlings

Avian plumage has long been used to test theories of sexual selection, with humans assessing the colors. However, many birds see in the ultraviolet (<400 nm), to which humans are blind. Consequently, it is important to know whether natural variation in UV reflectance from plumage functions in sexual signaling. We show that female starlings rank males differently when UV wavelengths are present or absent. Principal component analysis of ≈1300 reflectance spectra (300–700 nm) taken from sexually dimorphic plumage regions of males predicted preference under the UV+ treatment. Under UV− conditions, females ranked males in a different and nonrandom order, but plumage reflectance in the human visible spectrum did not predict choice. Natural variation in UV reflectance is thus important in avian mate assessment, and the prevailing light environment can have profound effects on observed mating preferences.