Ornaments are equally informative in males and females: a bivariate meta-analysis in birds

Female ornaments are often reduced, male-like traits. Although these were long perceived as nonadaptive, it is now broadly accepted that female ornaments can be functional. However, it is unclear whether this is as common in females as it is in males, and whether ornaments fulfil similar signalling roles. To test this, we conduct a systematic review and apply a phylogenetically controlled bivariate meta-analysis to a large dataset of ornaments in mutually ornamented birds. As expected, female ornament expression tends to be reduced compared to males. However, ornaments are equally strongly associated with indicators of body condition and aspects of reproductive success in both sexes, regardless of the degree of sexual dimorphism. Thus, ornaments in birds provide similar information in both sexes: more ornamented individuals are in better condition and achieve higher reproductive success. Although limited by their correlational nature, these outcomes imply that female ornaments could widely function in a similar manner as male ornaments.

Sex-specific ornament evolution is a consistent feature of climatic adaptation across space and time in dragonflies

Adaptation to different climates fuels the origins and maintenance of biodiversity. Detailing how organisms optimize fitness for their local climates is therefore an essential goal in biology. Although we increasingly understand how survival-related traits evolve as organisms adapt to climatic conditions, it is unclear whether organisms also optimize traits that coordinate mating between the sexes. Here, we show that dragonflies consistently adapt to warmer climates across space and time by evolving less male melanin ornamentation—a mating-related trait that also absorbs solar radiation and heats individuals above ambient temperatures. Continent-wide macroevolutionary analyses reveal that species inhabiting warmer climates evolve less male ornamentation. Community-science observations across 10 species indicate that populations adapt to warmer parts of species’ ranges through microevolution of smaller male ornaments. Observations from 2005 to 2019 detail that contemporary selective pressures oppose male ornaments in warmer years; and our climate-warming projections predict further decreases by 2070. Conversely, our analyses show that female ornamentation responds idiosyncratically to temperature across space and time, indicating the sexes evolve in different ways to meet the demands of the local climate. Overall, these macro- and microevolutionary findings demonstrate that organisms predictably optimize their mating-related traits for the climate just as they do their survival-related traits.

High-resolution characterization of male ornamentation and re-evaluation of sex linkage in guppies

Coloration plays a key role in the ecology of many species, influencing how an organism interacts with its environment, other species and conspecifics. Guppies are sexually dimorphic, with males displaying sexually selected coloration resulting from female preference. Previous work has suggested that much of guppy colour pattern variation is Y-linked. However, it remains unclear how many individual colour patterns are Y-linked in natural populations as much of the previous work has focused on phenotypes either not found in the wild, or aggregate measures such as total colour area. Moreover, ornaments have traditionally been identified and delineated by hand, and computational methods now make it possible to extract pixels and identify ornaments with automated methods, reducing the potential for human bias. Here we developed a pipeline for semi-automated ornament identification and high-resolution image analysis of male guppy colour patterns and applied it to a multigenerational pedigree. Our results show that loci controlling the presence or the absence of individual male ornaments in our population are not predominantly Y-linked. However, we find that ornaments of similar colour are not independent of each other, and modifier loci that affect whole animal coloration appear to be at least partially Y-linked. Considering these results, Y-linkage of individual ornaments may not be important in driving colour changes in natural populations of guppies, or in expansions of the non-recombining Y region, while Y-linked modifier loci that affect aggregate traits may well play an important role.

Flies improve the salience of iridescent sexual signals by orienting toward the sun

Sunlight is the ultimate source of most visual signals. Theory predicts strong selection for its effective use during communication, with functional links between signal designs and display behaviors a likely result. This is particularly true for iridescent structural colors, whose moment-to-moment appearance bears a heightened sensitivity to the position of signalers, receivers, and the sun. Here, we experimentally tested this prediction using Lispe cana, a muscid fly in which males present their structurally colored faces and wings to females during ground-based sexual displays. In field-based assays, we found that males actively bias the orientation of their displays toward the solar azimuth under conditions of full sunlight and do so across the entire day. This bias breaks down, however, when the sun is naturally concealed by heavy cloud or experimentally obscured. Our modeling of the appearance of male signals revealed clear benefits for the salience of male ornaments, with a roughly 4-fold increase in subjective luminance achievable through accurate display orientation. These findings offer fine-scale, causal evidence for the active control of sexual displays to enhance the appearance of iridescent signals. More broadly, they speak to predicted coevolution between dynamic signal designs and presentation behaviors, and support arguments for a richer appreciation of the fluidity of visual communication.

HIGH-RESOLUTION CHARACTERIZATION OF MALE ORNAMENTATION AND REEVALUATION OF SEX LINKAGE IN GUPPIES

Colouration plays a key role in the ecology of many species, influencing how an organism interacts with its environment, other species and conspecifics. Guppies are sexually dimorphic, with males displaying sexually selected colouration resulting from female preference. Previous work has suggested that much of guppy colour pattern variation is Y-linked. However, it remains unclear how many individual colour patterns are Y-linked in natural populations as much of the previous work has focused on phenotypes either not found in the wild, or aggregate measures such as total colour area. Moreover, ornaments have traditionally been identified and delineated by hand, and computational methods now make it possible to extract pixels and identify ornaments more automatedly, reducing the potential for human bias. Here we developed a pipeline for automated ornament identification and high-resolution image analysis of male guppy colour patterns and applied it to a multigenerational pedigree. Our results show that loci controlling the presence or absence of individual male ornaments in our population are not predominantly Y-linked. However, we find that ornaments of similar colour are not independent of each other, and modifier loci that affect whole animal colouration appear to be at least partially Y-linked. Considering these results, Y-linkage of individual ornaments may not be important in driving colour changes in natural populations of guppies, or in expansions of the non-recombining Y region, while Y-linked modifier loci that affect aggregate traits may well play an important role.

Flies improve the salience of iridescent sexual signals by orienting toward the sun

Sunlight is the ultimate source of most visual signals. Theory predicts strong selection for its effective use during communication, with functional links between signal designs and display behaviours a likely result. This is particularly true for iridescent structural colours, whose moment-to-moment appearance bears a heightened sensitivity to the position of signallers, receivers, and the sun. Here we experimentally tested this prediction using Lispe cana, a muscid fly in which males present their structurally coloured faces and wings to females during ground-based sexual displays. In field-based assays we found that males actively bias the orientation of their displays toward the solar azimuth under conditions of full sunlight and do so across the entire day. This bias breaks down, however, when the sun is naturally concealed by heavy cloud or experimentally obscured. Our modelling of the appearance of male signals revealed clear benefits for the salience of male ornaments, with a roughly four-fold increase in subjective luminance achievable through accurate display orientation. These findings offer fine-scale, causal evidence for the active control of sexual displays to enhance the appearance of iridescent signals. More broadly, they speak to predicted coevolution between dynamic signal designs and presentation behaviours, and support arguments for a richer appreciation of the fluidity of visual communication.

Female preferences when female condition and male ornament expression vary

Variation in the condition of females can affect their mate preferences. This may explain variation in the expression of male ornaments. We tested these ideas in the mealworm beetle (Tenebrio molitor), a species in which females choose males based on their pheromones. We modified female condition using diets that differed in proteins and carbohydrates. We then allowed females to choose among males in which we had previously modified pheromone expression (either by varying diets as in females, or by fungal infection). Females were offered a choice between two males, both of which had been fed the same diet as the female, but which differed in whether they were infected or not. We repeated the same diet and infection treatments to determine whether poor (lower carbohydrate) diets decrease survival in both sexes. There was no effect of female diet on mate choice, but the infection state of the male did have an effect, with infected males being preferred. It is possible that infected males invest their resources in producing pheromones rather than attacking the pathogen. Both sexes, independent of infection, had higher survival when fed carbohydrate-rich diets. The results showed no effect of female condition on their preferences, at least not prior to copulation.

Sexual ornaments but not weapons trade off against testes size in primates

Males must partition their limited reproductive investments between traits that promote access to females (sexual ornaments and weapons) and traits that enhance fertilization success, such as testes and ejaculates. Recent studies show that if the most weaponized males can monopolize access to females through contest competition, thereby reducing the risk of sperm competition, they tend to invest less in sperm production. However, how males invest in sexual ornaments relative to sperm production remains less clear. If male ornaments serve as badges of status, with high-ranking males attaining near-exclusive access to females, similar to monopolizing females through combat, their expression should also covary negatively with investment in post-mating traits. In a comparative study across primates, which exhibit considerable diversification in sexual ornamentation, male weaponry and testes size, we found relative testes size to decrease with sexual ornaments but increase with canine size. These contrasting evolutionary trajectories might be driven by differential selection, functional constraints or temporal patterns of metabolic investment between the different types of sexual traits. Importantly, however, our results indicate that the theory of relative investments between weapons and testes in the context of monopolizing females can extend to male ornaments.

Facial masculinity does not appear to be a condition-dependent male ornament and does not reflect MHC heterozygosity in humans

Recent studies have called into question the idea that facial masculinity is a condition-dependent male ornament that indicates immunocompetence in humans. We add to this growing body of research by calculating an objective measure of facial masculinity/femininity using 3D images in a large sample (n = 1,233) of people of European ancestry. We show that facial masculinity is positively correlated with adult height in both males and females. However, facial masculinity scales with growth similarly in males and females, suggesting that facial masculinity is not exclusively a male ornament, as male ornaments are typically more sensitive to growth in males compared with females. Additionally, we measured immunocompetence via heterozygosity at the major histocompatibility complex (MHC), a widely-used genetic marker of immunity. We show that, while height is positively correlated with MHC heterozygosity, facial masculinity is not. Thus, facial masculinity does not reflect immunocompetence measured by MHC heterozygosity in humans. Overall, we find no support for the idea that facial masculinity is a condition-dependent male ornament that has evolved to indicate immunocompetence.