Female Ornamentation Research Articles

Female ornamentation and the fecundity trade-off in a sex-role reversed pipefish.

Sexual ornaments found only in females are a rare occurrence in nature. One explanation for this is that female ornaments are costly to produce and maintain and, therefore, females must trade‐off resources related to reproduction to promote ornament expression. Here, we investigate whether a trade‐off exists between female ornamentation and fecundity in the sex‐role reversed, wide‐bodied pipefish, Stigmatopora nigra. We measured two components of the disk‐shaped, ventral‐striped female ornament, body width, and stripe thickness. After controlling for the influence of body size, we found no evidence of a cost of belly width or stripe thickness on female fecundity. Rather, females that have larger ornaments have higher fecundity and thus accurately advertise their reproductive value to males without incurring a cost to fecundity. We also investigated the relationship between female body size and egg size and found that larger females suffer a slight decrease in egg size and fecundity, although this decrease was independent of female ornamentation. More broadly, considered in light of similar findings in other taxa, lack of an apparent fecundity cost of ornamentation in female pipefish underscores the need to revisit theoretical assumptions concerning the evolution of female ornamentation.

Dynamic signalling using cosmetics may explain the reversed sexual dichromatism in the monogamous greater flamingo

Colourful plumage is typical of males in species with conventional sex roles, in which females care for offspring and males compete for females, as well as in many monogamous species in which both sexes care for offspring. Reversed sexual dichromatism—more colourful females than males—is predominant in species with sex role reversal. In the latter species, males care for offspring and females compete for mates, the mating system is mainly polyandrous and there is reversed size dimorphism—females are larger than males. Here, we document a case of reversed dichromatism, in the greater flamingo Phoenicopterus roseus, in which there is no sex role reversal and no reversed size dimorphism. Although theoretical models postulate that cases of reversed dichromatism should be rare among monogamous ornamented birds, our findings show that the use of cosmetics might be a mechanism for the occurrence of more ornamented females than males. Indeed, the concentrations of carotenoids in the uropygial secretions used as make-up were higher in females than in males. Apparently, there was a trade-off between coloration and antioxidant defence, as the concentrations of carotenoids in the uropygial secretions were lower during chick provisioning than in other periods, contrary to those in plasma. In this system, the application of make-up would act as a dynamic signal, which would allow a rapid reallocation of resources used for signalling among functions depending on needs. Cases like this may have evolved to signal the ability to provide parental care when females are more physiologically stressed than males. For species in which there is no sex role reversal, but females are ornamented and the resources allocated to ornaments are important for offspring viability, it has even been suggested that females should be less ornamented than males. This may be because for females, it would be better to invest directly in fecundity rather than in costly ornaments. We show a case of reversed sexual dichromatism in a monogamous bird with no sex role reversal, the greater flamingo, where females apply make-up over feathers. In the case of this species, there could be directional male mate preferences for female plumage coloration because the costs of signalling would not affect breeding investment in females, since cosmetic coloration is not used after it is no longer required, thus allowing the resources used in make-up (carotenoids) to be used in other functions.

Performance, behavior and offspring morphology may offset reproductive costs of male‐typical ornamentation for female lizards

Females of sexually dimorphic species that bear male-typical secondary sexual traits, such as male ornaments, may incur costs. However, in some species, ornamented females can be found in high numbers, suggesting that they may experience benefits that offset these costs. Some female fence lizards (Sceloporus undulatus) possess blue badges that are similar to, but less dramatic than, those displayed by males during courtship and dominance contests. Females bearing these badges have reduced reproductive investment and are less desirable as mates, costs that are difficult to reconcile with the high prevalence of this trait (up to 95% of females) in some populations. To test the hypothesis that there are potential benefits associated with male-typical ornamentation in females, we compared fitness-relevant performance, behavior and morphology of ornamented and unornamented female fence lizards and their offspring. Ornamented females achieved faster sprinting speeds and had offspring that were more likely to flee from predatory attacks and had longer bodies; these traits are associated with higher survival in this species. These results suggest the presence of two female morphotypes that may be differentially favored under contrasting environmental conditions. Unornamented females appear to have a reproductive advantage that should be favored under low predation environments. By contrast, ornamented females have traits that would confer a fitness advantage in high-predation environments. This work suggests a potential mechanism maintaining male-typical female ornamentation in nature.

Female ornamentation is associated with elevated aggression and testosterone in a tropical songbird

Relationships between testosterone, ornamentation, and aggression are relatively well resolved in males, but what about females? The White-shouldered Fairywren provides a useful context to address this question because female plumage varies across populations, whereas males are uniform. Females with elaborate plumage are more aggressive than dull females and also have elevated concentrations of testosterone. These relationships differ from those of males, consistent with selection on female ornamentation, likely for purposes of social competition.

Artificial selection reveals sex differences in the genetic basis of sexual attractiveness

Mutual mate choice occurs when males and females base mating decisions on shared traits. Despite increased awareness, the extent to which mutual choice drives phenotypic change remains poorly understood. When preferences in both sexes target the same traits, it is unclear how evolution will proceed and whether responses to sexual selection from male choice will match or oppose responses to female choice. Answering this question is challenging, as it requires understanding, genetic relationships between the traits targeted by choice, mating success, and, ultimately, fitness for both sexes. Addressing this, we applied artificial selection to the cuticular hydrocarbons of the fly Drosophila serrata that are targeted by mutual choice and tracked evolutionary changes in males and females alongside changes in mating success. After 10 generations, significant trait evolution occurred in both sexes, but intriguingly there were major sex differences in the associated fitness consequences. Sexually selected trait evolution in males led to a genetically based increase in male mating success. By contrast, although trait evolution also occurred in females, there was no change in mating success. Our results suggest that phenotypic sexual selection on females from male choice is environmentally, rather than genetically, generated. Thus, compared with female choice, male choice is at best a weak driver of signal trait evolution in this species. Instead, the evolution of apparent female ornamentation seems more likely due to a correlated response to sexual selection on males and possibly other forms of natural selection.

Male mate choice, female competition, and female ornaments as components of sexual selection.

Male mate choice, female competition, and female ornaments as components of sexual selection.

The Mating Behavior of Rhamphomyia pectinata (Empididae: Diptera) with Notes on Other Members of the Genus Found at the Same Locale in Northern Virginia

The previously unstudied empidid fly Rhamphomyia pectinata is, like many other members of the genus, a sex-role-reversed species with highly ornamented females that gather in swarms to await the arrival of prey-bearing males. Receptive males transfer their nuptial gifts to females before mating with them in the air. Rhamphomyia pectinata is diurnal, with swarming and copulations occurring in the afternoon. Other members of the genus occur at the study site but are crepuscular.

The evolution of male mate choice and female ornamentation: a review of mathematical models.

The evolution of male preferences and of female ornaments in species with traditional sex roles (i.e., polygyny) have been highlighted as areas in need of more active research by an accumulation of recent findings. The theoretical literature on these topics is relatively small and has centered on the evolution of male choice. Mathematical models have emphasized that, under polygyny, the evolution of male preferences faces much greater competition costs than does the evolution of female preferences. We discuss ways in which costly male choice can nonetheless evolve, via (1) direct selection that favors preferences, primarily through mating with highly fecund females, (2) mechanisms that rely on indirect selection, which weakly counters competitive costs of male preferences, and (3) genetic constraints, primarily in the form of pleiotropy of male and female preferences and traits. We also review a variety of mathematical models that have elucidated how costs to male preferences can be avoided. Finally, we turn our attention to the relatively scant theoretical literature on the effects of male mate choice on the evolution of female traits. We emphasize the finding that the presence of male preferences cannot be assumed to lead to the evolution of female ornaments during polygyny, and point out situations where models have elucidated ways in which female ornaments can nevertheless evolve.

Male mate choice in livebearing fishes: an overview.

Although the majority of studies on mate choice focus on female mate choice, there is growing recognition of the role of male mate choice too. Male mate choice is tightly linked to 2 other phenomena: female competition for males and ornamentation in females. In the current article, I review the existing literature on this in a group of fishes, Poeciliidae. In this group, male mate choice appears to be based on differences in female quality, especially female size, which is a proxy for fecundity. Some males also have to choose between heterospecific and conspecific females in the unusual mating system of the Amazon molly. In this case, they typically show a preference for conspecific females. Whereas male mate choice is relatively well documented for this family, female ornamentation and female competition are not.

Release from ecological constraint erases sex difference in social ornamentation

Sex differences in animal ornamentation are thought largely genetically fixed due to stronger sexual selection on males of species with conventional sex roles. But, other types of sex differences are not genetically fixed. For example, several differences in human social behavior result instead from sociocultural or economic constraints on women. Since gregarious animals use ornamentation for various social functions, perhaps some of their sex differences are, similarly to human behavior, due to social coercion or ecological constraint (their closest equivalents to human social and economic constraints, respectively). We found sex differences in ornamentation that disappear plastically in a social species with conventional sex roles. The red bill of common waxbills (Estrilda astrild) is on average more saturated in males, but in our experiment female bill color correlated with night temperature, an important energetic stressor, suggesting that sexual dichromatism disappears when ecological conditions are favorable to females. Female ornamentation may be more adversely affected by ecology because of their life history that requires balancing investment in ornamentation with maintaining reproductive condition. Manipulation of stress-related physiology (ACTH challenge) suggests that this effect was not mediated by stress mechanisms. Social coercion appears to not explain sexual dichromatism: males were not more aggressive than females, aggressiveness was not related to bill color, and manipulation of reproductive axis’ physiology (GnRH challenge, which in many species mediates aggressiveness) did not increase bill color. Our results show parallels to the plastic sex differences of humans in social animals and suggest that studying their ecological vs. social causes provides a biological backdrop for understanding the human case as well. Many sex differences in human social behavior result from economic or sociocultural constraints on women, while sex differences in the ornamentation of animals with conventional sex roles are thought largely genetically fixed. We show that a sex difference in ornamentation—the redder bills of male than female common waxbills—disappears plastically in an animal with conventional sex roles due to, in part, changes in female ornamentation. Social coercion did not explain reduced female ornamentation: aggressiveness did not predict bill color, and males were not dominant over females. Instead, female bill color was reduced during colder weather, perhaps because females under energetic stress need to balance investment in social ornamentation vs. maintaining reproductive condition. Similarly to humans, some sex differences of gregarious animals may be due to females requiring appropriate conditions to express their full social potential.

Male mate choice as differential investment in contest competition is affected by female ornament expression.

High male mating effort and high variation in female quality select for male mate choice, which may be expressed as differential investment of reproductive effort based on female value. Male reproductive effort includes investment in direct contest competition with rival males for access to females, yet variation in male–male contest behavior is rarely examined in the context of male mate choice. We examine such male response to variation in female body size, reproductive state, and female-specific ornamentation in the striped plateau lizard, Sceloporus virgatus. We housed lizards in trios of 2 size-matched males and one female for 5 days, such that all 3 lizards were physically isolated and the males could see the female but not each other. We then placed males simultaneously into the female’s cage and scored the interaction. Male–male aggression was not significantly affected by female body size, reproductive state, nor ornament color, but was influenced by ornament size which reliably signals the phenotypic quality of the female and her offspring. In the presence of larger-ornamented females, males engaged in more male–male aggressive display behavior more quickly, and performed fewer high-intensity contact behaviors but were equally likely to escalate to this riskier level of fighting. Our data suggest that males adjust their energetic investment during intrasexual competitive interactions in response to variation in the contested female which, assuming males gain direct or indirect benefits from their strategic allocation of reproductive effort, fits the modern understanding of male mate choice.

Variation in female aggression in 2 three-spined stickleback populations with female throat and spine coloration.

Despite growing interest in female ornament evolution, we still have a rudimentary understanding of female display traits relative to similar traits in males. Under one popular adaptive scenario, female ornaments are hypothesized to function in female–female competition and serve as badges of status, such that their expression is linked with elevated aggression in some cases. In this study, we investigated the relationship between 2 female ornaments—male-like red throat color and red spine coloration—and female aggression in 2 independently derived stream-resident populations of three-spined stickleback Gasterosteus aculeatus. Using simulated intrusions, we tested whether females with redder ornaments were generally more aggressive, and for variation in aggressive and social behaviors between the 2 populations. We found that the red intensity of the throat and spine did not predict aggression levels in either population, suggesting a limited role for both female ornaments during female–female interaction. The 2 populations exhibited different levels of aggressive behaviors, unrelated to the color patches. Our results suggest that variation in selective pressures between populations may promote interpopulation variance in aggressive behavior but not the correlation between female ornamentation and aggression, and raise the possibility that red coloration may have evolved through different mechanisms or processes in the 2 populations.

Plumage color manipulation has no effect on social dominance or fitness in zebra finches

Colorful plumage ornaments may evolve because they play a role in mate choice or in intrasexual competition, acting as signals of species identity or of individual quality. The zebra finch (Taeniopygia guttata) is a model organism for the study of mate choice and its colorful plumage ornaments are thought to be used in both of these contexts. Numerous genetic color variants have been described for this species, but they are rare in the wild. This raises the question whether discrimination against deviant phenotypes maintains the species’ uniform plumage color (rare-mate disadvantage). Furthermore, comparison to closely related species suggests that the lack of colorful ornaments in female zebra finches is a derived condition. Male preferences for less-ornamented females may have led to sexual dichromatism in the zebra finch. Here, we test the role of plumage ornaments experimentally by altering male and female coloration to mimic 2 types of naturally occurring genetic color variants. We estimated effects on social dominance and reproductive success in large breeding aviaries in one domesticated and 2 recently wild-derived populations. Hypotheses, methods, and analyses were preregistered to ensure maximal objectivity of the results presented. Despite a fairly drastic manipulation and a powerful experimental design, we found no effect of the treatment on social dominance or on reproductive success. Our results suggest that mate choice is not the mechanism that maintains homogeneity of zebra finch plumage coloration, or that can explain the loss of ornaments in females.

Experimental manipulation of female tail length did not cause differential allocation by males in the barn swallow

AbstractThe evolution and maintenance of female ornamentation has attracted increasing attention, because the previous explanation, that is a non‐functional copy of functional male ornamentation, seems insufficient to explain female ornamentation. A post‐mating sexual selection, differential allocation, may be more common than pre‐mating sexual selection, but few studies have investigated differential allocation by males. Here, we studied differential allocation of incubation investment by male barn swallows Hirundo rustica, a model species for the study of sexual selection, because our previous correlative study demonstrated a positive relationship between female tail length and male incubation investment. We manipulated the length of the outermost tail feathers in females after clutch completion and examined whether males adjust incubation investment according to female ornamentation. Because extra‐pair paternity is virtually absent in the study population, we were able to study differential allocation based on the tradeoff between current and future reproductive investments, rather than the tradeoff between current paternal investment and additional mating effort. The experimental treatment had no significant effect on male nest attentiveness, whereas female tail length before manipulation predicted male nest attentiveness. The observed pattern is consistent with differential access; that is, well‐ornamented individuals have greater access to mates with high reproductive (parental) ability, rather than differential allocation during incubation. Alternatively, males can directly assess eggs in their nests, and thus, as seen in other species, males might adjust their incubation investment based on the egg characteristics of long‐tailed females.

Female ornaments signal own and offspring quality in a sex‐role‐reversed fish with extreme male parental care

AbstractAlthough female ornaments have been described in many taxa, the full spectrum of information conveyed by such traits together with the potential male fitness benefits are far from fully understood. Here, we used a sex‐role‐reversed species, the black‐striped pipefish, Syngnathus abaster, where females are the ornamented sex and intensively compete for mates who present an extreme form of paternal care (male pregnancy). We investigated what information is conveyed by female traits and if males are using it during mate choice. We further assessed which traits would reflect offspring quality at birth. We found that although body length generally portrays information on female reproductive potential (gonadosomatic index and oocyte diameter), it does so indirectly. Different aspects of the female traits, such as stripe width and trunk broadness, were found to be better direct indicators. When size is kept constant, males prefer females with wider stripes. Moreover, stripe coloration was found to reflect offspring quality as darker‐striped females produced larger newborns. Our observations suggest that in a species with exclusive paternal care, independently from the male's direct investment in reproduction, female contribution decisively impacts male fitness. Thus, at least in sex‐role‐reversed species such as the black striped pipefish, female ornaments can be selected in an analogous way to those of males in species with conventional sex roles (i.e. by mate choice).

Evolution of a mating preference for a dual-utility trait used in intrasexual competition in genetically monogamous populations.

The selection pressures by which mating preferences for ornamental traits can evolve in genetically monogamous mating systems remain understudied. Empirical evidence from several taxa supports the prevalence of dual‐utility traits, defined as traits used both as armaments in intersexual selection and ornaments in intrasexual selection, as well as the importance of intrasexual resource competition for the evolution of female ornamentation. Here, we study whether mating preferences for traits used in intrasexual resource competition can evolve under genetic monogamy. We find that a mating preference for a competitive trait can evolve and affect the evolution of the trait. The preference is more likely to persist when the fecundity benefit for mates of successful competitors is large and the aversion to unornamented potential mates is strong. The preference can persist for long periods or potentially permanently even when it incurs slight costs. Our results suggest that, when females use ornaments as signals in intrasexual resource competition, males can evolve mating preferences for those ornaments, illuminating both the evolution of female ornamentation and the evolution of male preferences for female ornaments in monogamous species.

Males Become Choosier in Response to Manipulations of Female Wing Ornaments in Dry Season Bicyclus anynana Butterflies.

Male investment towards reproduction is substantial in some species, and this leads to the evolution of choosy males. Male choice is often directed towards female phenotypes that are good indicators of fecundity such as body size, age, or virgin status, and often acts in the same direction as fecundity selection. In insects, only a few examples exist where male choice is directed towards female ornaments as proxies Butler of female quality. Here, we use dry season males of the sex-role reversed butterfly species Bicyclus anynana to test for differences in male choosiness and investment towards females of varying attractiveness using ornament-manipulations. Male reproductive investment in this species is in the form of a nuptial gift, a spermatophore, given to females upon mating. Males were placed in cages with either wild-type ornamented females or with nonornamented females (center of the dorsal forewing eyespots painted over), and time to mating, duration of mating, and longevity of males and females after a single mating were measured. Ornament manipulations consisted of blocking the UV-reflective scales in the center of the dorsal forewing eyespots of females, a known sexual ornament. Males displayed lower latency to mate and longer mating durations with ornamented females. The longer mating duration did not, however, translate in the transfer of a nuptial gift that increased female longevity or reduced male longevity. Instead, we propose that longer mating durations with ornamented females may represent increased mate guarding behavior or increased sperm transfer.

Are sex ratio distorting endosymbionts responsible for mating system variation among dance flies (Diptera: Empidinae)?

Maternally inherited bacterial endosymbionts are common in many arthropod species. Some endosymbionts cause female-biased sex ratio distortion in their hosts that can result in profound changes to a host’s mating behaviour and reproductive biology. Dance flies (Diptera: Empidinae) are well known for their unusual reproductive biology, including species with female-specific ornamentation and female-biased lek-like swarming behaviour. The cause of the repeated evolution of female ornaments in these flies remains unknown, but is probably associated with female-biased sex ratios in individual species. In this study we assessed whether dance flies harbour sex ratio distorting endosymbionts that might have driven these mating system evolutionary changes. We measured the incidence and prevalence of infection by three endosymbionts that are known to cause female-biased sex ratios in other insect hosts (Wolbachia, Rickettsia and Spiroplasma) across 20 species of dance flies. We found evidence of widespread infection by all three symbionts and variation in sex-specific prevalence across the taxa sampled. However, there was no relationship between infection prevalence and adult sex ratio measures and no evidence that female ornaments are associated with high prevalences of sex-biased symbiont infections. We conclude that the current distribution of endosymbiont infections is unlikely to explain the diversity in mating systems among dance fly species.

Multivariate genetic architecture of the Anolis dewlap reveals both shared and sex-specific features of a sexually dimorphic ornament.

Darwin viewed the ornamentation of females as an indirect consequence of sexual selection on males and the transmission of male phenotypes to females via the 'laws of inheritance'. Although a number of studies have supported this view by demonstrating substantial between-sex genetic covariance for ornament expression, the majority of this work has focused on avian plumage. Moreover, few studies have considered the genetic basis of ornaments from a multivariate perspective, which may be crucial for understanding the evolution of sex differences in general, and of complex ornaments in particular. Here, we provide a multivariate, quantitative-genetic analysis of a sexually dimorphic ornament that has figured prominently in studies of sexual selection: the brightly coloured dewlap of Anolis lizards. Using data from a paternal half-sibling breeding experiment in brown anoles (Anolis sagrei), we show that multiple aspects of dewlap size and colour exhibit significant heritability and a genetic variance-covariance structure (G) that is broadly similar in males (Gm ) and females (Gf ). Whereas sexually monomorphic aspects of the dewlap, such as hue, exhibit significant between-sex genetic correlations (rmf ), sexually dimorphic features, such as area and brightness, exhibit reduced rmf values that do not differ from zero. Using a modified random skewers analysis, we show that the between-sex genetic variance-covariance matrix (B) should not strongly constrain the independent responses of males and females to sexually antagonistic selection. Our microevolutionary analysis is in broad agreement with macroevolutionary perspectives indicating considerable scope for the independent evolution of coloration and ornamentation in males and females.

Production of plumage ornaments among males and females of two closely related tropical passerine bird species

The evolution of elaborate secondary sexual traits (i.e., ornaments) is well‐studied in males but less so in females. Similarity in the appearance of ornaments between males and females supports the view that female ornaments arise as a neutral byproduct of selection on male traits due to genetic correlation between sexes, but recent research suggests an adaptive function of female ornaments in at least some contexts. Information on the degree to which production of ornaments differs between the sexes can shed light on these alternative perspectives. We therefore characterized the structural underpinnings of melanin‐based plumage production in males and females of two closely related passerine bird species (genus Malurus). Importantly, both ornamented and unornamented phenotypes in each sex are present between these two species, providing an opportunity to test the null expectation of equivalent modes of production in male and female ornamented phenotypes. In Malurus alboscapulatus, ornamented females are qualitatively similar to males, but we describe a distinctive ornamented female phenotype that differs from that of males in lacking a blue sheen and in lower feather barbule density. In M. melanocephalus, unornamented males and females are also similar in appearance, and we describe a similarity between unornamented phenotypes of males and females in both color and underlying feather barbule structure and pigment composition. Unornamented male M. melanocephalus can flexibly transition to the ornamented phenotype in weeks, and we found extreme differences in color and feather structure between these two alternative male phenotypes. These results contradict the idea that female ornaments have evolved in this system following a simple switch to male‐like plumage by demonstrating greater complexity in the production of the ornamented phenotype in males than in females.