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 and male visually based mate preferences are consistent with reproductive isolation between populations of the Lake Malawi endemic Labeotropheus fuelleborni

Sexual selection via female mate choice is thought to have played a key role in the speciation of haplochromine cichlids, but a dominant role for visual signals in such processes has lately been called into question. In addition, the possible role of male mating preferences in haplochromine speciation has been little studied. We studied patterns of both female and male mate choice, based exclusively on visual signals, in order to evaluate potential reproductive isolation between two populations of the Lake Malawi haplochromine Labeotropheus fuelleborni. In the first experiment, females were allowed to choose between two males, one from the same population and the other allopatric with respect to the female. Females in this experiment responded more frequently to males from their own population. Similarly, the males in these trials displayed more frequently when presented with females of their own population. In the second experiment, a female was allowed to choose between two males, either both from her own population or both allopatric. In these trials, both males and females from the Katale population interacted significantly more frequently in settings in which all three individuals were from the same population (same-population trios), and those from the Chipoka population showed a similar trend. Thus, patterns in both male and female courtship behavior suggest that visual signals contribute to at least incipient reproductive isolation between populations of L. fuelleborni [Current Zoology 56 (1): 65-72 2010].     

Sequential search and the influence of male quality on female mating decisions

 The patterns of phenotypic association between mated males and females depend on the decision rules that individuals employ during search for a mate. We generalize the sequential search rule and examine how the shape of the function that relates a male character to the benefit of a mating decision influences the threshold value of the male trait that induces females to terminate search. If the fitness function is linear the optimal threshold value of a male character increases with the slope of the function. The phenotypic threshold criterion declines, all else being equal, if the fitness function is made more concave (or less convex) by an increase of the risk of the function. The expression of the trait in females has no effect on the optimal threshold value of a male character if the fitness function is linear and phenotypic values combine additively to influence the benefit of a mating decision; the phenotypic threshold criterion is ubiquitous among females. A convex fitness function induces females with high trait values to adopt a relatively high phenotypic threshold criterion, whereas a concave fitness function induces such females to adopt a low threshold value for the male trait. Thus, linear, convex and concave fitness functions effect random, assortative and disassortative combinations of phenotypes among mated individuals, respectively. Changes of female search behavior induced by changes of the distribution of a male character similarly depend on the shape of the fitness function. A variance-preserving increase of male trait values produces a relatively small increase of the threshold criterion for the male character if the fitness function is concave, relative to conditions in which the fitness function is either linear or convex. Our results suggest that a sequential search rule can in principle induce the kinds of mating patterns observed in nature and that the phenotypic association between mated individuals is likely to depend on how a male character translates into fitness, the distribution of the trait among males and attributes of searching females. Received: 20 September 1997 / Revised version: 13 August 1998     

Intrasexual competition among females and the stabilization of a conspicuous colour polymorphism in a Lake Victoria cichlid fish

The maintenance of colour polymorphisms within populations has been a long-standing interest in evolutionary ecology. African cichlid fish contain some of the most striking known cases of this phenomenon. Intrasexual selection can be negative frequency dependent when males bias aggression towards phenotypically similar rivals, stabilizing male colour polymorphisms. We propose that where females are territorial and competitive, aggression biases in females may also promote coexistence of female morphs. We studied a polymorphic population of the cichlid fish Neochromis omnicaeruleus from Lake Victoria, in which three distinct female colour morphs coexist: one plain brown and two blotched morphs. Using simulated intruder choice tests in the laboratory, we show that wild-caught females of each morph bias aggression towards females of their own morph, suggesting that females of all three morphs may have an advantage when their morph is locally the least abundant. This mechanism may contribute to the establishment and stabilization of colour polymorphisms. Next, by crossing the morphs, we generated sisters belonging to different colour morphs. We find no sign of aggression bias in these sisters, making pleiotropy unlikely to explain the association between colour and aggression bias in wild fish, which is maintained in the face of gene flow. We conclude that female-female aggression may be one important force for stabilizing colour polymorphism in cichlid fish.     

Runaway sexual selection with paternal transmission of the male trait and gene-culture determination of the female preference

Sexual selection is modeled with a male viability-reducing trait and a female mating preference for that trait both of which are culturally transmitted. Both the male trait and the female preference are transmitted only between same-sex individuals, so that non-random association between the trait and the preference, which would give rise to a Fisherian runaway process, cannot arise. Inclusion of an autosomal gene that confers a female predisposition to acquire a certain preference is shown to allow the coevolution of the male trait and the female preference by a Fisherian process. This holds true even when the female preference has a slight viability cost, provided the male cultural transmission is not perfect. It is also suggested that a Fisherian process can be more easily initiated in these models than in the conventional genetic models. Furthermore, a Fisherian process may cause cultural transmission of female preference to evolve. Additionally, polymorphism can be maintained at the predisposition locus if heterozygous females have a stronger predisposition to acquire the preference than homozygotes. Our models may be applicable to the case when the male trait is a Y-linked genetic or environmentally determined trait.     

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.     

Temporally consistent species differences in parasite infection but no evidence for rapid parasite‐mediated speciation in Lake Victoria cichlid fish

Parasites may have strong eco‐evolutionary interactions with their hosts. Consequently, they may contribute to host diversification. The radiation of cichlid fish in Lake Victoria provides a good model to study the role of parasites in the early stages of speciation. We investigated patterns of macroparasite infection in a community of 17 sympatric cichlids from a recent radiation and 2 older species from 2 nonradiating lineages, to explore the opportunity for parasite‐mediated speciation. Host species had different parasite infection profiles, which were only partially explained by ecological factors (diet, water depth). This may indicate that differences in infection are not simply the result of differences in exposure, but that hosts evolved species‐specific resistance, consistent with parasite‐mediated divergent selection. Infection was similar between sampling years, indicating that the direction of parasite‐mediated selection is stable through time. We morphologically identified 6 Cichlidogyrus species, a gill parasite that is considered a good candidate for driving parasite‐mediated speciation, because it is host species‐specific and has radiated elsewhere in Africa. Species composition of Cichlidogyrus infection was similar among the most closely related host species (members of the Lake Victoria radiation), but two more distantly related species (belonging to nonradiating sister lineages) showed distinct infection profiles. This is inconsistent with a role for Cichlidogyrus in the early stages of divergence. To conclude, we find significant interspecific variation in parasite infection profiles, which is temporally consistent. We found no evidence that Cichlidogyrus‐mediated selection contributes to the early stages of speciation. Instead, our findings indicate that species differences in infection accumulate after speciation.     

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.     

A test of fitness consequences of hybridization in sibling species of Lake Victoria cichlid fish

Several hundred species of haplochromine cichlid fish have evolved rapidly in Lake Victoria. Divergent sexual and ecological selection probably played an important role in this radiation, generating divergent mating preferences and preference-trait covariance. However, the segregation of hybrid inviability or infertility genes could also potentially generate preference-trait covariance, and the mechanisms that cause the evolution of divergent mating preferences have not been investigated in detail in any cichlid species pair. We investigated intrinsic fitness of hybrids between two sister species in the genus Pundamilia, one of the most species-rich genera of Lake Victoria cichlids. Fitness-related traits were measured in nonhybrid offspring of both species, and in the first and second hybrid generations. There were no differences in fecundity, fertility, sex ratio or growth rates either between the sister species or between these and their hybrids. By contrast, there was a difference in offspring survival between the two sister species. Offspring survival was dependent only on the species of the mother, regardless of whether the cross was conspecific or heterospecific. Further, eggs tended to be larger in the hybrids than in one of the parental species. Hence, hybrids suffered no intrinsic fitness reduction relative to nonhybrids. Our data suggest that intrinsic hybrid incompatibilities are unlikely to have caused speciation in Pundamilia, nor to maintain species boundaries in this system.     

Parasite-mediated sexual selection and species divergence in Lake Victoria cichlid fish

We investigate the role of parasite-mediated sexual selection in the divergence of two species of Lake Victoria cichlids. Pundamilia pundamilia and Pundamilia nyererei represent a common pattern of male nuptial colour divergence between haplochromine sister species: metallic grey–blue in P. pundamilia and bright yellow and red in P. nyererei . Female mating preferences for different male colours maintain the genetic and phenotypic differentiation of the two species in clear water. Previous work indicated that the red coloration of P. nyererei males, which is subject to directional sexual selection, may be a carotenoid-dependent signal of parasite infestation rate. In the present study, we find a parallel result for P. pundamilia : bright blue males are infected with fewer species of parasites. We also find that parasite infestation rates differ quantitatively between the two species in a way that is consistent with species differences in diet and microhabitat. We conclude that parasite-mediated sexual selection may have contributed to the divergence of female mating preferences between P. pundamilia and P. nyererei , and may currently strengthen reproductive isolation between these species.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 94 , 53–60.     

Population-structure and genetic diversity in a haplochromine cichlid fish [corrected] of a satellite lake of Lake Victoria

The approximately 500 species of the cichlid fish species flock of Lake Victoria, East Africa, have evolved in a record-setting 100,000 years and represent one of the largest adaptive radiations. We examined the population structure of the endangered cichlid species Xystichromis phytophagus from Lake Kanyaboli, a satellite lake to Lake Victoria in the Kenyan Yala wetlands. Two sets of molecular markers were analysed--sequences of the mitochondrial control region as well as six microsatellite loci--and revealed surprisingly high levels of genetic variability in this species. Mitochondrial DNA sequences failed to detect population structuring among the three sample populations. A model-based population assignment test based on microsatellite data revealed that the three populations most probably aggregate into a larger panmictic population. However, values of population pairwise FST indicated moderate levels of genetic differentiation for one population. Eleven distinct mitochondrial haplotypes were found among 205 specimens of X. phytophagus, a relatively high number compared to the total number of 54 haplotypes that were recovered from hundreds of specimens of the entire cichlid species flock of Lake Victoria. Most of the X. phytophagus mitochondrial DNA haplotypes were absent from the main Lake Victoria, corroborating the putative importance of satellite lakes as refugia for haplochromine cichlids that went extinct from the main lake in the last decades and possibly during the Late Pleistocene desiccation of Lake Victoria.     

A sex-specific trade-off between mating preferences for genetic compatibility and body size in a cichlid fish with mutual mate choice

Mating preferences for genetic compatibility strictly depend on the interplay of the genotypes of potential partners and are therein fundamentally different from directional preferences for ornamental secondary sexual traits. Thus, the most compatible partner is on average not the one with most pronounced ornaments and vice versa. Hence, mating preferences may often conflict. Here, we present a solution to this problem while investigating the interplay of mating preferences for relatedness (a compatibility criterion) and large body size (an ornamental or quality trait). In previous experiments, both sexes of Pelvicachromis taeniatus, a cichlid fish with mutual mate choice, showed preferences for kin and large partners when these criteria were tested separately. In the present study, test fish were given a conflicting choice between two potential mating partners differing in relatedness as well as in body size in such a way that preferences for both criteria could not simultaneously be satisfied. We show that a sex-specific trade-off occurs between mating preferences for body size and relatedness. For females, relatedness gained greater importance than body size, whereas the opposite was true for males. We discuss the potential role of the interplay between mating preferences for relatedness and body size for the evolution of inbreeding preference.     

Rapid assessment of female preference for male size predicts subsequent choice of spawning partner in a socially monogamous cichlid fish

Although size-assortative mating in convict cichlids, Amatitliana nigrofasciata, is supposed to result from mutual mating preference for larger individuals, female choice in relation to male size remains ambiguous. We revisited the evidence for directional preference for larger males in female convict cichlids using a classical two-way choice apparatus in which each female could decide to spend time in front of a small male or a large one. We found evidence for female preference for large males, as assessed from association preference during a 4-hour period following encounter. Furthermore, females decided to spawn in front of the initially preferred male more often than expected by chance. Our results thus confirm the existence of a directional preference for large males in female convict cichlids, and indicate that association preference measured over a short period of time can provide a quick and reliable proxy for reproductive preference in this species.     

Selfish genetic elements and sexual selection: their impact on male fertility

Females of many species mate with more than one male (polyandry), yet the adaptive significance of polyandry is poorly understood. One hypothesis to explain the widespread occurrence of multiple mating is that it may allow females to utilize post-copulatory mechanisms to reduce the risk of fertilizing their eggs with sperm from incompatible males. Selfish genetic elements (SGEs) are ubiquitous in eukaryotes, frequent sources of reproductive incompatibilities, and associated with fitness costs. However, their impact on sexual selection is largely unexplored. In this review we examine the link between SGEs, male fertility and sperm competitive ability. We show there is widespread evidence that SGEs are associated with reduced fertility in both animals and plants, and present some recent data showing that males carrying SGEs have reduced paternity in sperm competition. We also discuss possible reasons why male gametes are particularly vulnerable to the selfish actions of SGEs. The widespread reduction in male fertility caused by SGEs implies polyandry may be a successful female strategy to bias paternity against SGE-carrying males.     

Selfish genetic elements and sexual selection: their impact on male fertility

Females of many species mate with more than one male (polyandry), yet the adaptive significance of polyandry is poorly understood. One hypothesis to explain the widespread occurrence of multiple mating is that it may allow females to utilize post-copulatory mechanisms to reduce the risk of fertilizing their eggs with sperm from incompatible males. Selfish genetic elements (SGEs) are ubiquitous in eukaryotes, frequent sources of reproductive incompatibilities, and associated with fitness costs. However, their impact on sexual selection is largely unexplored. In this review we examine the link between SGEs, male fertility and sperm competitive ability. We show there is widespread evidence that SGEs are associated with reduced fertility in both animals and plants, and present some recent data showing that males carrying SGEs have reduced paternity in sperm competition. We also discuss possible reasons why male gametes are particularly vulnerable to the selfish actions of SGEs. The widespread reduction in male fertility caused by SGEs implies polyandry may be a successful female strategy to bias paternity against SGE-carrying males.     

An introduction to genetic quality in the context of sexual selection

This special issue of Genetica brings together empirical researchers and theoreticians to present the latest on the evolutionary ecology of genetic quality in the context of sexual selection. The work comes from different fields of study including behavioral ecology, quantitative genetics and molecular genetics on a diversity of organisms using different approaches from comparative studies, mathematical modeling, field studies and laboratory experiments. The papers presented in this special issue primarily focus on genetic quality in relation to (1) sources of genetic variation, (2) polyandry, (3) new theoretical developments and (4) comprehensive reviews.     

Male morphological characteristics and mating success in a protogynous coral reef fish, Halichoeres melanurus

Morphological sexual differences and their effects on male mating success were investigated in the tailspot wrasse, Halichoeres melanurus, on a subtropical coral reef of Okinawa, southern Japan. Male mating territories were established along the reef edge from late April to early October, during which time pair-spawning occurred just before sunset in the male territories. Territorial males were larger and brighter than females in this protogynous fish. The males had longer, colorful ventral fins and colorful caudal fins, both of which were used during courtship. Multiple regression analysis of the effects of male characteristics on male mating success revealed that the yellow spot at the pectoral fin base was the most effective. It is suggested that large body size is favored in male–male competition for establishing mating territories and that conspicuous body color is favored in female mate choice. Received: June 16, 1999 / Accepted: September 22, 1999     

PERMANENT GENETIC RESOURCES: Isolation and characterization of microsatellite loci in the cichlid fish in Lake Victoria, Haplochromis chilotes

Twelve short tandem repeat markers were successfully isolated from a cichlid, Haplochromis chilotes, in Lake Victoria, and characterized in Haplochromis pyrrhocephalus. The microsatellite regions of these markers were found to have between two and 48 alleles with heterozygosity ranging from 0.07 to 0.97. No loci showed significant departures from the Hardy–Weinberg or linkage equilibrium after the Bonferroni correction (P > 0.05). Cross‐species amplification in other cichlids of Lake Victoria, Haplochromis laparogramma, Lithochromis rubripinnis, L. rufus and Haplochromis sp. ‘rockkribensis’, was successful.     

Color polymorphism and sex ratio distortion in a cichlid fish as an incipient stage in sympatric speciation by sexual selection

We investigated a Lake Victoria cichlid with a complex colour polymorphism that apparently represents one original species and two incipient species, all of which are sympatric. In laboratory breeding experiments we observed sex ratio distortion in certain matings between original and incipient species. Mate choice experiments show that males of the incipient species exhibit mating preferences against the original species, and males and females of the original species exhibit strong mating preferences against the incipient species. Mating preferences might evolve by sex ratio selection to avoid matings with distorted progeny sex ratios. Phenotype frequencies in nature suggest that mating preferences translate into mating frequencies, thus restricting gene flow and exerting disruptive sexual selection between the original and incipient species. The incipient species do not differ in morphology or ecology from the original species, implying that colour polymorphism, associated with sex ratio distortion, can be an incipient stage in sympatric speciation, and that disruption of gene flow can precede ecological differentiation.