Phylogenetic Correlation Between Male Nuptial Color and Behavioral Responses to Color Across a Diverse and Colorful Genus of Freshwater Fish (Etheostoma spp., Teleostei: Percidae)

Sexual selection theory predicts that preferences in both sexes select for the elaboration of male nuptial coloration, with empirical evidence supporting these predictions. Empirical studies are often limited in their taxonomic inclusiveness, however, and typically do not examine how male and female preferences contribute to macroevolutionary patterns of male color variation across multiple lineages in a clade. This study examined color preferences in a group of dichromatic freshwater fishes known as darters (genus Etheostoma) that vary in the presence of male coloration. The strengths of attraction to black, blue, gray, and red models were tested in females of 18 species, in addition to males of five species. We found a positive association between the presence of red or orange on the body and the amount of time associating with red models, suggesting color variation is at least in part due to variation in female preferences between species. Males also spent more time associating with colors that most closely resembled conspecifics, suggesting that preferential responses to color in males also can contribute to the diversity of nuptial coloration in darters.     

Male coloration signals direct benefits in the European bitterling (Rhodeus amarus)

Female mating preferences are frequently associated with exaggerated male sexual traits. In the European bitterling, Rhodeus amarus, a fish with a resource-based mating system, male coloration is not associated with indirect genetic benefits of female mate choice, and does not reliably signal spawning site quality. We tested a link between the extent of male carotenoid-based coloration and testis size and number of spermatozoa stripped from the testes. Male body size predicted spermatozoa number, but less reliably than the extent of male coloration. Male color was a highly significant predictor of spermatozoa number, with approximately 26 % of variance in the number of spermatozoa stripped from males predicted from male color after controlling for male body size. Body size, but not coloration, predicted teste size. Female bitterling often risk sperm limitation, especially during pair spawnings, and male nuptial coloration may be under direct selection through female mate choice as a signal of male fertilization efficiency.     

Sexual selection in an anadromous population of threespine sticklebacks — no role for parasites

Summary We examined the hypothesis that trematode parasites played a role in the evolution of the red colour of male threespine sticklebacks (Gasterosteus aculeatus L.) and whether the parasites affected female fitness. Parasites (blackspot disease) played no role either in determining the outcome of male—male competition for breeding territories or in female mate choice. Among males with territories, mating success was highly variable. Some males obtained over 3000 eggs (approximately 10 matings) whereas others received none. In 1 year of the 2 year study, males with the greatest amount of red nuptial coloration had the greatest mating success. Although male colour may sometimes affect female choice in this system, this preference has probably not evolved because of the Hamilton—Zuk mechanism of sexual selection. The parasites had small, but statistically significant effects on female fitness. Females with high parasite loads were in poorer condition and produced fewer eggs than less parasitized fish.     

Conspicuous Female Ornamentation and Tests of Male Mate Preference in Threespine Sticklebacks (Gasterosteus aculeatus)

Sexual selection drives the evolution of exaggerated male ornaments in many animal species. Female ornamentation is now acknowledged also to be common but is generally less well understood. One example is the recently documented red female throat coloration in some threespine stickleback (Gasterosteus aculeatus) populations. Although female sticklebacks often exhibit a preference for red male throat coloration, the possibility of sexual selection on female coloration has been little studied. Using sequential and simultaneous mate choice trials, we examined male mate preferences for female throat color, as well as pelvic spine color and standard length, using wild-captured threespine sticklebacks from the Little Campbell River, British Columbia. In a multivariate analysis, we found no evidence for a population-level mate preference in males, suggesting the absence of directional sexual selection on these traits arising from male mate choice. Significant variation was detected among males in their preference functions, but this appeared to arise from differences in their mean responsiveness across mating trials and not from variation in the strength (i.e., slope) of their preference, suggesting the absence of individual-level preferences as well. When presented with conspecific intruder males, male response decreased as intruder red throat coloration increased, suggesting that males can discriminate color and other aspects of phenotype in our experiment and that males may use these traits in intrasexual interactions. The results presented here are the first to explicitly address male preference for female throat color in threespine sticklebacks.     

Color-Based Association Among Heterospecifics in Lake Malaŵi Rock-Dwelling Cichlids

Female mate choice can be an imperfect barrier against hybridization. Among the cichlid fishes of the East African great lakes, sexual selection on male nuptial coloration has been noted as being particularly important for reproductive isolation among closely related lineages. Diversification of the rock‐dwelling cichlids of Lake Mala?i has led to a repeating pattern of color morphs wherein more distantly related species may look more similar than a more closely related pair. Using members of the Metriaclima zebra group and a heterogener, I tested the hypothesis that females would spend greater time associating with males more similarly colored to her species than females would with divergently colored, although more closely related males. Experimental results were consistent with this hypothesis, thus supporting the speculation and some field observation that mate choice can fail as a barrier to hybridization if a female encounters a distantly related male that shares the nuptial coloration of males of her own species and color morph. This notion is discussed in the broader context of both the adaptive and non‐adaptive mechanisms that have been suggested to be important to the radiation of this group.     

Male–male competition facilitates female choice in sticklebacks

In many species, secondary sexual characteristics are used in both male–male competition and in attracting females. This suggests that social control of deception could contribute to the maintenance of honest sexual signalling. In the three-spined stickleback Gasterosteus aculeatus, male red breeding coloration plays a dual role in sexual selection by functioning as both a threat signal in male–male competition and as a cue for female choice. To investigate whether male competition determines the level of signalling, the expression of red coloration and courtship activity were recorded both before and after male interactions. The results show that male competition influences signal expression by increasing the difference between males in signalling level. This in turn facilitates female choice and induces a preference for dominant males. Since a preference for dominant males may benefit females both directly and indirectly in this species with exclusively paternal care, male–male competition seems to increase the honesty of signalling and, thus, facilitates female choice in relation to male quality. This may increase the intensity of sexual selection and promote the evolution of breeding aggregations.     

Video mate preferences of female three-spined sticklebacks from populations with divergent male coloration

This study evaluated whether diversity in male ornamental traits between populations is associated with a corresponding diversity in female preferences, or whether males can evolve divergent ornamentation even when female preferences remain relatively consistent. Video editing techniques were used to manipulate the coloration of recorded images of male three-spined sticklebacks, Gasterosteus aculeatus, and these images were presented to female sticklebacks from populations with black or red male nuptial coloration. Overall, females responded preferentially to images of males with black or red coloration over images with the dull coloration of females and some males; although preferences differed between populations, these differences were not statistically significant. Thus divergence in male ornaments was probably not caused by a corresponding divergence in female preferences. The results do not, however, allow clear discrimination between the various hypotheses for the evolution of female mating preferences.     

CONVERGENT EVOLUTION OF RED CAROTENOID COLORATION IN WIDOWBIRDS AND BISHOPS (EUPLECTES SPP.)

Avian carotenoid‐based signals are classic examples of sexually selected, condition‐dependent threat displays or mate choice cues. In many species, male dominance or mating success is associated with redder (i.e., longer wavelength) color hues, suggesting that red colors are either more efficient or more reliable signals than yellow colors. Few studies, however, have investigated selection for redness in a macroevolutionary context. Here, we phylogenetically reconstruct the evolution of carotenoid coloration in the African widowbirds and bishops (Euplectes spp.), for which agonistic selection for redder hues, as well as pigmentary mechanisms, is well documented. Using reflectance spectrometry for objective color quantification, and accounting for phylogenetic uncertainty, we find that yellow plumage color is a retained ancestral state in Euplectes, and that red color hues have convergently evolved two or three times. Results are discussed in relation to a known diversity in pigment mechanisms, supporting independent origins of red color, and suggesting that agonistic selection and physiological constraints have interacted to generate color diversity in Euplectes.     

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.     

Does part reproductive history predict competitive interactions and male mating success in pupfish?

Two experiments were performed to determine the effect of past territoriality and mating success on subsequent dominance and ability to attract females. First, in 14 staged, pair-wise encounters, the development of nuptial coloration and agonistic behaviour was examined in two types of males: previously territorial (PT) and previously non-territorial (PNT) males. Previously territorial males developed a more intense nuptial coloration and won all contests. Second, to test the males' ability to attract females, other factors were controlled that could have affected female mate choice, such as male size, quality of breeding substrate and male-male interactions. In 40 trials, PT males were more active, developed a more intense nuptial coloration, courted females more vigorously, spawned sooner and had a higher mating success than PNT males. Thus, in pupfish, Cyprinodon pecosensis, previous reproductive history is a good indicator of both dominance and mating success. Only males in good physical condition achieve high mating success, and both intra- and inter-sexual selection are important in maintaining the close correlation between expression of nuptial coloration, a second sexual trait, and other male attributes, such as physical condition and vigour, that allow a male to secure and defend a territory against rivals and to attract and spawn with females.     

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.     

Black Male Bellies and Red Female Throats: Color Changes with Breeding Status in a Threespine Stickleback

This paper provides the first report of black nuptial coloration on the ventral side for a population of threespine sticklebacks, Gasterosteus aculeatus, in Northern California. Black nuptial coloration was least intense during precourtship. Although the black coloration intensified during courtship, it was not a significant predictor of female choice and, unlike the red throat and blue eyes, was not inversely correlated with the number of female introductions necessary before spawning occurred. Black coloration was the most intense for males who successfully hatched embryos, supporting a parental-defense role late in the cycle. Unsuccessful fathers had more intensely colored red throats, blue eyes, and black bellies during most of the reproductive cycle than successful fathers. Some females in this study developed red coloration on their throat, although none to the intensity or distribution typical of a breeding male.     

The ecological drivers of nuptial color evolution in darters (Percidae: Etheostomatinae)

Closely related animal lineages often vary in male coloration, and ecological selection is hypothesized to shape this variation. The role of ecological selection in inhibiting male color has been documented extensively at the population level, but relatively few studies have investigated the evolution of male coloration across a clade of closely related species. Darters are a diverse group of fishes that vary in the presence of elaborate male nuptial coloration, with some species exhibiting vivid color patterns and others mostly or entirely achromatic. We used phylogenetic logistic regression to test for correlations between the presence/absence of color traits across darter species and the ecological conditions in which these species occur. Environmental variables were correlated with the presence of nuptial color in darters with colorful species tending to inhabit environments that would support fewer predators and potentially transmit a broader spectrum of natural light compared to species lacking male coloration. We also tested the color preferences of a common darter predator, largemouth bass, and found that it exhibits a strong preference for red, providing further evidence of predation as a source of selection on color evolution in darters. Ecological selection therefore appears to be an important factor in dictating the presence or absence of male coloration in this group of fishes.     

Population-Specific Covariation between Immune Function and Color of Nesting Male Threespine Stickleback

Multiple biological processes can generate sexual selection on male visual signals such as color. For example, females may prefer colorful males because those males are more readily detected (perceptual bias), or because male color conveys information about male quality and associated direct or indirect benefits to females. For example, male threespine stickleback often exhibit red throat coloration, which females prefer both because red is more visible in certain environments, and red color is correlated with male immune function and parasite load. However, not all light environments favor red nuptial coloration: more tannin-stained water tends to favor the evolution of a melanic male phenotype. Do such population differences in stickleback male color, driven by divergent light environments, lead to changes in the relationship between color and immunity? Here, we show that, within stickleback populations, multiple components of male color (brightness and hue of four body parts) are correlated with multiple immune variables (ROS production, phagocytosis rates, and lymphocyte:leukocyte ratios). Some of these color-immune associations persist across stickleback populations with very different male color patterns, whereas other color-immune associations are population-specific. Overall, lakes with red males exhibit stronger color-immune covariance while melanic male populations exhibit weak if any color-immune associations. Our finding that color-immunity relationships are labile implies that any evolution of male color traits (e.g., due to female perceptual bias in a given light environment), can alter the utility of color as an indicator of male quality.     

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.     

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.     

Processes driving male breeding colour and ecomorphological diversification in rainbow skinks: a phylogenetic comparative test

We used a phylogenetic comparative approach to investigate the importance of ecological shifts in the diversification of both signalling traits and ecomorphological traits in a diverse group of Australian skinks (Carlia). First, we tested whether divergence in male breeding coloration is associated with shifts in habitat openness. Second, we examined whether the type or location of male breeding coloration changes predictably with habitat openness. Third, we tested the ecomorphological predictions that body size should vary in relation to habitat openness and that limb length, toe length and head depth should vary with substrate use. Divergence in male breeding coloration was positively associated with shifts in habitat openness. Our results also indicate that species occupying more open habitats tend to use male sexual signals located on lateral body regions and not necessarily on body regions that are potentially more concealed from aerial predators (e.g. chest and throat). With regard to ecomorphological traits, habitat openness appears to have no predictable influence on body size at the inter-specific level, contrary to expectations based on intra-specific studies. However, consistent with functional predictions, we found that preference for rocky habitats is associated with relatively longer hind limb length, presumably due to selection for greater speed and jumping ability on these substrates. Overall, results of this study support the hypothesis that ecological shifts play a central role in promoting morphological diversification.     

Quantifying Reproductive Barriers in a Sympatric Pair of Darter Species

Quantifying and comparing the strengths of different reproductive barriers between diverging lineages is especially useful for determining the evolutionary mechanisms driving speciation. Etheostoma barrenense and Etheostoma zonale are closely related sympatric species of darters that are sexually dimorphic and exhibit clear differences in male nuptial coloration. Prior studies demonstrated that these species exhibit complete behavioral isolation, and that both intraspecific and interspecific variation in male coloration play a role in female choice, all consistent with speciation by sexual selection on male nuptial color. Remaining unclear, however, is whether behavioral isolation is the strongest reproductive barrier between these species or, alternatively, whether additional reproductive barriers are equally strong, which could implicate mechanisms other than sexual selection in speciation. Here, we compare the relative strengths of multiple reproductive barriers between the two focal species, measuring: (1) ecological isolation, (2) gametic incompatibility, (3) hybrid inviability, (4) conspecific sperm precedence, and comparing these measures to a previously estimated strength of behavioral isolation. We find that behavioral isolation is the strongest reproductive barrier measured to date and suggest it may be the only barrier that has evolved to completion. This result provides additional empirical evidence for speciation driven by sexual selection and provides insight into the maintenance of sympatric species in nature.     

Possible relationships between morphology,territory quality,and skin color of American Kestrels1

ABSTRACT Carotenoid‐based coloration of skin and plumage has been found to be correlated with individual quality in many species of birds during the breeding season. However, less is known about the possible role of these signals during the nonbreeding season, particularly among nonpasserines that defend winter territories. American Kestrels (Falco sparverius) are sexually dimorphic raptors that defend winter territories and possess carotenoid‐based morphological features known to be correlated with individual quality. Much is known about winter territory use and habitat segregation by male and female kestrels, but possible relationships among morphological features, individual quality, and habitat quality have not been examined. Our objective was to examine possible relationships between morphology, territory quality, and skin color of American Kestrels. Male kestrels had brighter skin than females, and the skin color of male kestrels was positively correlated with size (wing chord and tail length) and territorial quality (hunting territories with less canopy and more grass cover). No such relationships were found for female kestrels. Skin color appears to be an honest indicator of quality for male American Kestrels and may serve both intersexual (territory acquisition) and intersexual (mate choice) functions during the breeding and nonbreeding seasons.     

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.