The function of anal fin egg-spots in the cichlid fish Astatotilapia burtoni

Color and pigmentation patterns of animals are often targets of sexual selection because of their role in communication. Although conspicuous male traits are typically implicated with intersexual selection, there are examples where sex-specific displays play a role in an intrasexual context, e.g. when they serve as signals for aggression level and/or status. Here, we focus on the function of a conspicuous male ornament in the most species-rich tribe of cichlid fishes, the haplochromines. A characteristic feature of these ca. 1500 species are so-called egg-spots in form of ovoid markings on the anal fins of males, which are made up of carotenoid based pigment cells. It has long been assumed that these yellow, orange or reddish egg-spots play an important role in the courtship and spawning behavior of these maternal mouth-brooding fishes by mimicking the eggs of a conspecific female. The exact function of egg-spots remains unknown, however, and there are several hypotheses about their mode of action. To uncover the function of this cichlid-specific male ornament, we used female mate choice experiments and a male aggression test in the haplochromine species Astatotilapia burtoni. We manipulated the number and arrangement of egg-spots on the anal fins of males, or removed them entirely, and tested (1) female preference with visual contact only using egg-traps, (2) female preference with free contact using paternity testing with microsatellites and (3) male aggression. We found that females did not prefer males with many egg-spots over males with fewer egg-spots and that females tended to prefer males without egg-spots over males with egg-spots. Importantly, males without egg-spots sired clutches with the same fertilization rate as males with egg-spots. In male aggression trials, however, males with fewer egg-spots received significantly more attacks, suggesting that egg-spots are an important signal in intrasexual communication.     

Heritability and adaptive significance of the number of egg-dummies in the cichlid fish Astatotilapia burtoni

Cichlid fishes are a textbook example of rapid speciation and exuberant diversity--this applies especially to haplochromines, a lineage with approximately 1800 species. Haplochromine males uniquely possess oval, bright spots on their anal fin, called 'egg-spots' or 'egg-dummies'. These are presumed to be an evolutionary key innovation that contributed to the tribe's evolutionary success. Egg-spots have been proposed to mimic the ova of the mouthbrooding females of the corresponding species, contribute to fertilization success and even facilitate species recognition. Interestingly, egg-spot number varies extensively not only between species, but also within some populations. This high degree of intraspecific variation may appear to be counterintuitive since selection might be expected to act to stabilize traits that are correlated with fitness measures. We addressed this 'paradox' experimentally, and found that in the haplochromine cichlid Astatotilapia burtoni, the number of egg-spots was related to male age, body condition and dominance status. Intriguingly, the egg-spot number also had a high heritable component (narrow sense heritability of 0.5). These results suggest that the function of egg-spots might have less to do with fertilization success or species recognition, but rather relate to mate choice and/or male-male competition, helping to explain the high variability in this important trait.     

Hybrid origin of a swordtail species (Teleostei: Xiphophorus clemenciae) driven by sexual selection

The swordlike exaggerated caudal fin extensions of male swordtails are conspicuous traits that are selected for through female choice. Swords are one of only few examples where the hypothesis of a pre-existing bias is believed to apply for the evolution of a male trait. Previous laboratory experiments demonstrated that females prefer males with longer swords and even females from some swordless species show an affiliation for males of sworded species. Earlier phylogenetic studies based on maternally inherited mitochondrial DNA placed the sworded southern swordtail Xiphophorus clemenciae with swordless platies, contradicting its morphology-based evolutionary affinities. The analyses of new nuclear DNA markers now recover its traditional phylogenetic placement with other southern swordtails, suggesting that this species was formed by an ancient hybridization event. We propose that sexual selection through female choice was the likely process of hybrid speciation, by mating of platy females with males of an ancestral swordtail lineage. In artificial crosses of descendent species from the two potential ancestral lineages of X. clemenciae the hybrid and backcross males have swords of intermediate lengths. Additionally, mate choice experiments demonstrate that hybrid females prefer sworded males. These experimental lines of evidence make hybridization through xeno-specific sexual selection by female choice the likely mechanism of speciation.     

Did sexually dimorphic dorsal coloration evolve by a pre-existing bias in males in the lizard Sceloporus minor?

Theory and empirical evidence indicate that male secondary sex traits can evolve by co-option of pre-existing biases in females. However, relatively few studies have explored whether male pre-existing biases could drive the evolution of traits important in male contests. Male spiny lizards (Sceloporus) are characterized by the expression of sexually dimorphic blue throat and abdominal patches. These features are revealed to conspecifics during social interactions, and variation in ventral color can predict the outcome of male contests in some species of spiny lizards. In Sceloporus minor, males in some populations also express bright blue color on the dorsal surfaces. Given the significance of blue color in intrasexual signaling in other species of Sceloporus, blue dorsal color may have evolved in S. minor by co-option of a male sensory bias for the color blue. We tested this hypothesis in a population that exhibits an ancestral phenotype for male dorsal color (brown/orange), and lacks males with bright blue dorsal coloration. Resident territorial males were presented with one of three types of intruder males manipulated in dorsal color by painting. Orange males mimicked the ancestral dorsal phenotype found at the study site; blue males resembled those from a population with the derived (blue) form of this trait; and green males represented a novel stimulus control. If blue dorsal color evolved in S. minor in part due to co-option of a male sensory bias, we predicted that resident males would exhibit either increased or decreased levels of aggression to blue intruders relative to controls. We found no difference in resident aggressive behavior across all treatments, thus failing to support the predictions of a pre-existing bias. We discuss these findings in the context of social behavior in Sceloporus, and propose directions for further study in this species.     

Female Preference for Male Lateral Projection Area in the Shortfin Molly, Poecilia mexicana: Evidence for a Pre-existing Bias in Sexual Selection

Sailfin molly (Poecilia latipinna) males possess a large dorsal fin (sailfin) and perform an elaborate courtship display. Females prefer to associate and mate with males of greater body and sailfin size. Evidence supports a single origin for the sailfin species complex from a shortfin ancestor. Unlike sailfin species, males of the shortfin species complex are sexually monomorphic in fin size and exhibit little or no courtship behavior. In this study, we tested the pre‐existing bias and lateral projection area (LPA) hypotheses for sexual selection by examining female mating preferences in the shortfin molly, P. mexicana. Specifically, we presented females with pairs of dummy males differing in: (1) dorsal fin and body size together (holding fin:body size ratio constant); (2) body size (holding dorsal fin size constant); (3) dorsal fin size (holding body size constant); and dorsal fin:body size ratio (holding total LPA constant). Females spent more time near dummies of greater body and dorsal fin size. The preference functions based on the first three sets of stimuli showed a similar pattern: the greater the LPA difference between paired dummies, the stronger the preference for the larger of the two. However, in the fourth experiment, neither fin size, body size, nor any particular dorsal fin + body size combination was preferred. These findings support the LPA hypothesis suggesting that increased LPA is more stimulating to sexually receptive females and that females consequently prefer larger males. Moreover, these data are consistent with results obtained in an identical series of experiments conducted on P. latipinna. The preference for increased male dorsal fin size/LPA by both female P. latipinna and P. mexicana supports the pre‐existing bias hypothesis. Thus, a bias for increased male LPA and consequent selection for enlarged dorsal fins may have preceded the appearance of the sailfin trait within the Molliensia lineage.     

Heritability and heterochrony of polychromatism in a Lake Victoria Cichlid fish: Stepping stones for speciation?

In many haplochromine cichlid fish, male nuptial coloration is subject to female mate choice and plays a central role in the evolution of reproductive isolation between incipient species. Intraspecific variation in male coloration may serve as a target for diversifying sexual selection and provide a starting point for species divergence. Here, we investigated a polychromatism in Neochromis omnicaeruleus, a haplochromine from Lake Victoria, East-Africa. In this species, male coloration ranges from skyblue to yellow-red and females are grey-blue to yellow. We found that both genetic and environmental factors influence the expression of these colours during individual development. In a natural population, we found that male colour was associated with size and sexual maturity: yellow males were smaller than blue males and tended to be sexually immature. In females, size and maturity did not differ between colour types. Laboratory crosses revealed that there is a heritable component to the observed colour variation: yellow parents produced more yellow offspring than blue parents. Together with repeated aquarium observations of yellow individuals that gradually become blue, these data suggest that yellow males change to blue as they approach sexual maturity, and that the occurrence and timing of this transition is influenced by both environmental and genetic effects. The significance of this mechanism of colour expression as a possible target for divergent selection remains to be evaluated.     

Female bias for enlarged male body and dorsal fins in Xiphophorus variatus

Female preference for male fin elaborations in Poeciliid fishes may be driven by a sensory bias for increased lateral projection area (LPA) that has existed since the lineages diverged from a common ancestor. Previous research supports this hypothesis demonstrating female Poecilia latipinna, Poecilia mexicana, and Poecilia reticulata prefer males of larger body and dorsal fin size, but exhibit no such preferences when controlling for total LPA. In the current study, we further tested this hypothesis by presenting female platys, Xiphophorus variatus, with pairs of dummy males differing in: (1) body size (holding dorsal fin size constant); (2) dorsal fin size (holding body size constant); and (3) dorsal fin: body size ratio (holding total LPA constant). Females spent more time near dummies of greater body and dorsal fin size; however, in the third experiment, neither fin size, body size, nor any particular dorsal fin + body size combination was preferred. These results provide additional support for the LPA and sensory bias hypotheses, demonstrating that female X. variatus not only prefer males with “swords”, but sailfin-like dorsal fins as well when body size is held constant. Shared preference for increased LPA is consistent with common ancestry of the sensory/neural systems in females of all four species.     

The ontogenetic development of egg-spots in the haplochromine cichlid fish Astatotilapia burtoni

A series of Astatotilapia burtoni photographs were used to investigate the ontogenetic development of male egg-spots, a putative evolutionary key innovation of haplochromine cichlids. Four stages of egg-spot development were defined and all males had developed true egg-spots (stage 4) before reaching a standard length of 25 mm. Raising condition only slightly influenced the timing of the first appearance of true egg-spots.     

Do Female Western Mosquitofish,Gambusia affinis,Prefer Ornaments That Males Lack?

Some species in the family Poeciliidae are known for extravagant male ornaments and courtship behavior (e.g., guppies), but the majority of poeciliids are characterized by coercive male copulation attempts that seem to circumvent female choice. In some lineages with male ornaments, female sensory bias may have preceded the evolution of corresponding male signals. We examined female preferences for colorful ornaments in Western mosquitofish, Gambusia affinis, in which males lack ornamentation and reproduce primarily through coercive mating attempts. We found that females exhibited a positional affinity for males that were artificially ornamented with blue coloration over males that had been treated with a transparent ornament. Females exhibited the opposite effect for males treated with red ornaments. In contrast, focal females did not exhibit behavioral discrimination between two live stimulus females or two models (silver fishing lures) with blue vs. transparent ornaments. This suggests a sexual context for female discrimination between males based on ornament color and whether an ornament was present. Because tribe Gambusiini is the basal branch of family Poeciliidae, the results of this study are consistent with the hypothesis that female responsiveness to male coloration is the ancestral poeciliid character state.     

A test of sensory exploitation in the swordtail characin (Corynopoma riisei) based on colour matching between female prey and a male ornament

The sensory exploitation hypothesis states that pre-existing biases in female sensory systems may generate strong selection on male signals to match such biases. As environmental conditions differ between populations, sexual preferences resulting from natural selection are expected to vary as well. The swordtail characin (Corynopoma riisei) is a species in which males carry a flag-like ornament growing from the operculum that has been proposed to function as a prey mimic to attract females. Here, we investigated if female plasticity in feeding preferences is associated with plasticity in preference for an artificial male ornament in this species. Females were trained for 10 days by offering them differently coloured food items and were then tested for changes in preferences for differently coloured artificial male ornaments according to foraging experience. We found a rapid and pronounced change in female preference for the colouration of the artificial ornament according to food training. Thus our results support the possibility that sensory exploitation may act as a driving force for female preferences for male ornaments in this species.     

The evolution of preference strength under sensory bias: a role for indirect selection?

Evidence suggests that female preferences may sometimes arise through sensory bias, and that males may subsequently evolve traits that increase their conspicuousness to females. Here, we ask whether indirect selection, arising through genetic associations (linkage disequilibrium) during the sexual selection that sensory bias imposes, can itself influence the evolution of preference strength. Specifically, we use population genetic models to consider whether or not modifiers of preference strength can spread under different ecological conditions when female mate choice is driven by sensory bias. We focus on male traits that make a male more conspicuous in certain habitats-and thus both more visible to predators and more attractive to females-and examine modifiers of the strength of preference for conspicuous males. We first solve for the rate of spread of a modifier that strengthens preference within an environmentally uniform population; we illustrate that this spread will be extremely slow. Second, we used a series of simulations to consider the role of habitat structure and movement on the evolution of a modifier of preference strength, using male color polymorphisms as a case study. We find that in most cases, indirect selection does not allow the evolution of stronger or weaker preferences for sensory bias. Only in a "two-island" model, where there is restricted migration between different patches that favor different male phenotypes, did we find that preference strength could evolve. The role of indirect selection in the evolution of sensory bias is of particular interest because of ongoing speculation regarding the role of sensory bias in the evolution of reproductive isolation.     

Assortative aggression among males in a sympatric pair of Labeotropheus from Lake Malaŵi,Africa

Female mate choice has strong experimental support as a diversifying force in the speciation of the haplochromine cichlid fishes of Lake Malaŵi, Africa. Somewhat less understood is the role that male–male aggression might have played in the evolution of new species of these fishes. In the rock-dwelling haplochromines of Lake Malaŵi, primarily territory-holding males successfully court females; by determining which males gain territories, male–male aggression could support speciation by excluding less-fit males from the breeding population. To test the hypothesis that males should direct more aggression towards conspecific rivals, the aggression directed towards conspecific and heterospecific opponents was compared in a sympatric pair of cichlids of the genus Labeotropheus Ahl 1927 (Labeotropheus fuelleborni Ahl 1927 and Labeotropheus trewavasae Fryer 1956). It was found that when presented with a pair of rivals, males of both species did direct more aggression towards the conspecific opponent, and the amount of aggression increased when the conspecific opponent was larger than the heterospecific opponent. In addition, this study found a difference in the behavioural repertoire of the species: L. fuelleborni tends to rely on displays to intimidate opponents, whereas L. trewavasae employs more physical attacks to drive away opponents. Males of both species can thus recognize conspecifics and assess an opponent's relative threat to their ability to successfully reproduce, and use species-specific strategies to intimidate opponents.     

Sensory bias as an explanation for the evolution of mate preferences

The sensory bias model of sexual selection posits that female mating preferences are by-products of natural selection on sensory systems. Although sensory bias was proposed 20 years ago, its critical assumptions remain untested. This paradox arises because sensory bias has been used to explain two different phenomena. First, it has been used as a hypothesis about signal design, that is, that males evolve traits that stimulate female sensory systems. Second, sensory bias has been used as a hypothesis for the evolution of female preference itself, that is, to explain why females exhibit particular preferences. We focus on this second facet. First, we clarify the unique features of sensory bias relative to the alternative models by considering each in the same quantitative genetic framework. The key assumptions of sensory bias are that natural selection is the predominant evolutionary mechanism that affects preference and that sexual selection on preferences is quantitatively negligible. We describe four studies that would test these assumptions and review what we can and cannot infer about sensory bias from existing studies. We suggest that the importance of sensory bias as an explanation for the evolution of female preferences remains to be determined.     

Female choice linked to male dorsal fin height in a shortfin molly

Sexual selection is a possible mechanism of speciation. This could be true even in systems where female mate choice has not been clearly observed, because pre-existing biases may be expressed if female decision-making results in male trait evolution. In some mollies, males have enlarged dorsal fins and courtship display is the prevailing mating process. In others, male dominance is thought to play a greater role. We tested females of a species in the latter group, Poecilia mexicana, for consistent preference related to dorsal fin morphology. We found that females were biased toward larger dorsal fins. This latent preference could be an important driver in trait evolution.     

Developmental plasticity and variability in the formation of egg-spots,a pigmentation ornament in the cichlid Astatotilapia calliptera

Vertebrate pigmentation patterns are highly diverse, yet we have a limited understanding of how evolutionary changes to genetic, cellular, and developmental mechanisms generate variation. To address this, we examine the formation of a sexually-selected male ornament exhibiting inter- and intraspecific variation, the egg-spot pattern, consisting of circular yellow-orange markings on the male anal fins of haplochromine cichlid fishes. We focus on Astatotilapia calliptera, the ancestor-type species of the Malawi cichlid adaptive radiation of over 850 species. We identify a key role for iridophores in initializing egg-spot aggregations composed of iridophore-xanthophore associations. Despite adult sexual dimorphism, aggregations initially form in both males and females, with development only diverging between the sexes at later stages. Unexpectedly, we found that the timing of egg-spot initialization is plastic. The earlier individuals are socially isolated, the earlier the aggregations form, with iridophores being the cell type that responds to changes to the social environment. Furthermore, we observe apparent competitive interactions between adjacent egg-spot aggregations, which strongly suggests that egg-spot patterning results mostly from cell-autonomous cellular interactions. Together, these results demonstrate that A. calliptera egg-spot development is an exciting model for investigating pigment pattern formation at the cellular level in a system with developmental plasticity, sexual dimorphism, and intraspecific variation. As A. calliptera represents the ancestral bauplan for egg-spots, these findings provide a baseline for informed comparisons across the incredibly diverse Malawi cichlid radiation.     

A Test for Female Attraction to Male Orange Coloration in Poecilia picta

Examining the distribution of female preference and attractive male secondary sexual characters in closely related species can help evaluate the various models for the evolution of female preference. We examined whether orange coloration in males was attractive to females of Poecilia picta, a species in the same subgenus as the guppy, P. reticulata. Females did not respond differently to males with or without a conspicuous orange stripe on the dorsum of the tail, a characteristic ornamentation of the male of this species. This lack of preference in a taxon that possesses a conspicuous, secondary sexual character directly contradicts the predictions of the sensory exploitation hypothesis for the evolution of female preference, but may support a model of antagonistic sexual selection proposed by Rice (1996).     

Sexual selection,reproductive behavior,and speciation in the mbuna species flock of Lake Malawi (Pisces: Cichlidae)

Synopsis The cichlid species flocks of the African Great Lakes represent the most extreme case of adaptive radiation among vertebrates. Recently, attention has focused on the potential for sexual selection to drive or accelerate speciation in these fishes. Cichlids as a whole are social in nature and display complex behavior, particularly during courtship and spawning; however, the extent to which changes in species recognition cues may account for species diversity among haplochromine lineages has remained speculative. Our investigations have indicated that oral incubating haplochromines show a reduction in diversity and extent of courtship relative to substrate brooding cichlids, and apparently retain aspects of a primitive specific mate recognition system. Laboratory observations of courtship in the Malawian endemicPseudotropheus zebra suggest that organization of the spawning bout is loose, and lacking in any well defined stimulus-response chain. Interspecific comparisons of in situ courtship behavior among male mbuna, lithophilous haplochromines of Lake Malawi, revealed only one potential example of species-specific behavior, and indicated that mate choice occurred prior to the onset of intense courtship. Courtship display by male mbuna does not appear critical to species recognition and may represent an evolutionary relict. Alternatively, male courtship display may have an indirect effect on successful reproduction or may be maintained through pleiotropic effects. The mbuna display no evidence of behavioral innovation and show limited interspecific differentiation in behavioral expression. More generally, there is no evidence at present to suggest that epigamic sexual selection, acting on courtship behavior, has been a major mechanism in the diversification of the haplochromine species flocks.     

Monogamy in the maternally mouthbrooding Lake Tanganyika cichlid fish Tropheus moorii

Supported by evidence for assortative mating and polygynandry, sexual selection through mate choice was suggested as the main force driving the evolution of colour diversity of haplochromine cichlids in Lakes Malawi and Victoria. The phylogenetically closely related tribe Tropheini of Lake Tanganyika includes the genus Tropheus, which comprises over 100 colour variants currently classified into six morphologically similar, polyphyletic species. To assess the potential for sexual selection in this sexually monochromatic maternal mouthbrooder, we used microsatellite-based paternity inference to investigate the mating system of Tropheus moorii. In contrast to haplochromines in Lake Malawi, multiple paternity is rare or even absent in broods of T. moorii. Eighteen of the 19 analysed families were consistent with genetic monogamy, while either a mutation or more than one sire explained the genotype of one offspring in another brood. We discuss the differences in breeding behaviour between T. moorii and the Lake Malawi haplochromines, and evaluate additional factors or alternatives to sexual selection as promoters of colour diversification. A preliminary survey of other Tropheini species suggested that multiple paternity is infrequent in the entire tribe.     

Female preferences in a fish genus without female mate choice.

The evolution and the adaptive logic (if any) of female mate choice are subjects of lively debate. Whereas most researchers believe that females have evolved to recognize signs of male 'quality' (the ability to provide females or their offspring with direct or indirect genetic or material benefits), there is intriguing evidence that males can evolve to appeal to pre-existing female preferences. Evidence for these pre-existing biases is often ambiguous because phylogenetic reconstructions have usually failed to establish conclusively whether the female preference or the favored male traits evolved first. This potential difficulty is minimal in the mosquitofish genus Gambusia, none of whose 45 species appears to have a female-choice mating system in the wild, and none of which shows the male behavioral and morphological traits that are characteristic of female choice. Nevertheless, in an experimental situation in the laboratory, female Gambusia holbrooki readily chose between models of males and demonstrated significant and reliable preferences for a variety of exaggerated male traits that are not seen in their species or their genus. Other morphological alterations were not preferred. The latent willingness of females to choose traits in a genus without such traits and without evident female choice in the wild is remarkable and may indicate a pre-existing bias in females that is ready to drive male evolution, should the social system or the ecological variables that control it change.     

Sexual selection and senescence: male size-dimorphic ungulates evolved relatively smaller molars than females

As a general rule, males of sexually dimorphic ungulate species have evolved larger body size than females but shorter reproductive life spans as elements of their strategy for intrasexual competition for mating opportunities. Evolutionary theories of senescence predict that the durability of somatic structures should relate to the length of reproductive life span. This prediction has recently been tested for red deer (Cervus elaphus): molariform teeth of males are smaller and less durable than those of females, which corresponds with sex differences in reproductive life span. However, general evidence that male teeth are smaller than expected by allometric rules as a consequence of sexual selection for increasing male body mass requires an interspecific comparison between dimorphic and nondimorphic ungulates. Here we investigate the relationship between cheek-teeth size (occlusal surface area; OSA) and body mass in 123 species of extant ungulates. We found lower slopes for dimorphic species compared with nondimorphic ones and smaller OSA, relative to body mass, in males of dimorphic species compared with females of dimorphic species. Rates of evolution of OSA relative to rates of evolution of body mass were greater in females than in males and also greater in nondimorphic than in dimorphic species. Our results are consistent with the hypothesis that sexual selection in polygynous male ungulates favors body size more than tooth size, with possible consequences in male senescence via early depletion of male teeth compared to females.