Evolution Of Secondary Sexual Traits Research Articles

Male mating behaviour affects growth of secondary sexual traits: a mechanism for rapid phenotypic change

Intra- and intersexual selection drives the evolution of secondary sexual traits, leading to increased body size, trait size and generally increased reproductive success in bearers with the largest, most attractive traits. Evolutionary change through natural selection is often thought of primarily in terms of genetic changes through mutations and adaptive selection. However, this view ignores the role of the plasticity in phenotypes and behaviour and its impact on accelerating or decelerating the expression of sexually selected traits. Here, we argue that sudden changes in selection pressures (e.g. predation pressure) may cause a cascade of behavioural responses, leading to a rapid change in the size of such traits. We propose that selective removal of individuals with the most prominent traits (such as large antlers or horns in male ungulates) induces behavioural changes in the surviving males, leading to a reduction in the growth of these traits (phenotypic expression). To test this idea, we used an individual-based simulation, parametrized with empirical data of male bighorn sheep, Ovis candensis. Our model shows that the expression (phenotype, not genotype) of the trait under selection (here horn size) can be negatively impacted, if the biggest, most dominant males in the population are removed. While the selective removal of prime males opens breeding opportunities for younger, smaller males, we predicted that it would come at the expense of growth and maintenance. As predicted, we observed a rapid decline in average male horn length in our model. We argue that this decline happens because smaller males, instead of allocating energy into growth, divert this energy towards participation in mating activities that are typically exclusively available to prime males. While our model deals with ecological life-history trade-offs, it cannot predict evolutionary outcomes. However, this nongenetic mechanism is important for the understanding of evolutionary processes because it describes how heritable traits can rapidly change because of behavioural plasticity, long before any genetic changes might be detectable.

Eco‐evolutionary dynamics of sexual selection and sexual conflict

Abstract The research framework of eco‐evolutionary dynamics is increasing in popularity, as revealed by a steady stream of review articles and a recent and influential book, but primary empirical research is lagging behind. Moreover, the few empirical case studies demonstrating eco‐evolutionary dynamics might not be entirely representative. Much current research on eco‐evolutionary dynamics is focused on how ecological interactions lead to natural selection on phenotypic traits (“eco‐evo”), and in turn how the evolutionary change in such traits feed back on ecological dynamics (“evo‐eco”). A key feature of eco‐evolutionary dynamics is thus a feedback loop between ecology (e.g., population dynamics) and evolution (i.e., genetic change). In contrast to previous research on eco‐evolutionary dynamics driven by natural selection, the role of eco‐evolutionary feedbacks in sexual selection and sexual conflict is largely unknown. Here, I review theory and the limited empirical evidence in this area and identify some promising future lines of research. I update a past review on contemporary evolution of secondary sexual traits in natural populations and formulate six explicit and rigorous criteria for contemporary evolution of secondary sexual traits by natural or sexual selection or sexual conflict. I then discuss the other key prediction of eco‐evolutionary dynamics (i.e., evolution by sexual selection or sexual conflict shapes ecological dynamics). My overview reveals that our current knowledge in this area is limited and mainly come from theoretical models and laboratory experiments. A major challenge in eco‐evolutionary dynamics is therefore to link ecological and population dynamics with sexual selection and sexual conflict. This is not an easy task but might be possible with carefully chosen study systems and methods. A plain language summary is available for this article.

Boldness is related to the development of the cephalic crest in the male of the river blenny Salaria fluviatilis (Asso, 1801)

Abstract Boldness is defined as the tendency of an individual to take risks when exposed to novel objects or situations. The main aim of this work was to dilucidate if boldness was related to the development of the secondary sexual traits (SSTs) in the male of the river blenny Salaria fluviatilis, a freshwater fish which takes care of eggs. As a second objective SSTs effect on parental status adoption was also be explored. Wild young fish were caught in the Segre River (Ebro basin) in November 2010. Fish were kept in five aquaria in groups of eight males and eight females with artificial nests. Boldness (boldness score and hesitancy) of males (initially with little SSTs development) was tested as the time required to exit a refuge when exposed to a new environment. Fish were mantained in the same aquaria for several months, and males’ SSTs development and reproductive behaviour were monitored. Boldness score was negatively associated to cephalic crest development. Hesitancy was negatively related to male length and was also influenced by the interaction between male length and cephalic crest. Parental status acquisition was positively related to the male’s length, marginally related to anal gland development, and non-related to cephalic crest. These results suggest an intrasexual role of the crest as an informative trait of boldness (honest signal) which might not necessarily be chosen by the females. It is also discussed that correlational selection could be responsible for linking boldness and growth rate in this species. Sexual selection, in addition to having directed the evolution of secondary sexual traits, might have favored certain personality traits (e.g. boldness) associated with the achievement of a larger body length.

Using visual modelling to study the evolution of lizard coloration: sexual selection drives the evolution of sexual dichromatism in lacertids

Sexual selection has been invoked as a major force in the evolution of secondary sexual traits, including sexually dimorphic colourations. For example, previous studies have shown that display complexity and elaborate ornamentation in lizards are associated with variables that reflect the intensity of intrasexual selection. However, these studies have relied on techniques of colour analysis based on human--rather than lizard--visual perception. Here, we use reflectance spectrophotometry and visual modelling to quantify sexual dichromatism considering the overall colour patterns of lacertids, a lizard clade in which visual signalling has traditionally been underrated. These objective methods of colour analysis reveal a large, previously unreported, degree of sexual dichromatism in lacertids. Using a comparative phylogenetic approach, we further demonstrate that sexual dichromatism is positively associated with body size dimorphism (an index of intrasexual selection), suggesting that conspicuous coloration in male lacertids has evolved to improve opponent assessment under conditions of intense male-male competition. Our findings provide the first evidence for the covariation of sexual dichromatism and sexual size dimorphism in lacertids and suggest that the prevalent role of intrasexual selection in the evolution of ornamental coloration is not restricted to the iguanian lineage, but rather may be a general trend common to many diurnal lizards.

The Role of Courtship Behavior and Size in Mate Preference in the Sex‐Role‐Reversed Gulf Pipefish, Syngnathus scovelli

AbstractIn sex‐role‐reversed species, sexual selection acts more strongly on females than on males, a situation that can result in the evolution of secondary sexual traits in females and strong mating preferences in males. While some research exploring mating preferences in sex‐role‐reversed species has been conducted, overall, this topic remains relatively unexplored. The Gulf pipefish, Syngnathus scovelli, is a highly polyandrous pipefish species. Sexual selection is significantly stronger in females than in males, which has led to the evolution of both morphological and behavioral female secondary sexual traits. However, because males gestate the offspring in specialized pouches and make a substantial investment in embryos during development, females may also benefit from being choosy. The goal of this study was to examine both male and female mating preferences in this species. We found that male mating preference was significantly associated with female courtship behavior. Larger females were also able to maintain these behaviors for longer intervals than smaller females. No evidence of female mating preference in regard to male size was observed but the data suggest that male behaviors may be providing positive reinforcement to courting females. This research provides further insight into how mate preferences vary among sex‐role‐reversed species.

Sexual selection and the evolution of secondary sexual traits: sex comb evolution in Drosophila

Sexual selection can drive rapid evolutionary change in reproductive behaviour, morphology and physiology. This often leads to the evolution of sexual dimorphism, and continued exaggerated expression of dimorphic sexual characteristics, although a variety of other alternative selection scenarios exist. Here, we examined the evolutionary significance of a rapidly evolving, sexually dimorphic trait, sex comb tooth number, in two Drosophila species. The presence of the sex comb in both D.melanogaster and D.pseudoobscura is known to be positively related to mating success, although little is yet known about the sexually selected benefits of sex comb structure. In this study, we used experimental evolution to test the idea that enhancing or eliminating sexual selection would lead to variation in sex comb tooth number. However, the results showed no effect of either enforced monogamy or elevated promiscuity on this trait. We discuss several hypotheses to explain the lack of divergence, focussing on sexually antagonistic coevolution, stabilizing selection via species recognition and nonlinear selection. We discuss how these are important, but relatively ignored, alternatives in understanding the evolution of rapidly evolving sexually dimorphic traits.

Population differentiation in the swordtail characin (Corynopoma riisei ): a role for sensory drive?

Sensory drive, where the efficacy of a sexual signal depends on the environment in which it is employed, is a potential mechanism behind divergent evolution of secondary sexual traits. Male swordtail characins are equipped with a narrow and transparent extension of the gill cover with a flag-like structure at its tip. This opercular flag mimics a prey item and is employed by males as a 'lure' to attract the attention of females during mating attempts. We conducted a study of genetic and morphological differentiation across swordtail characin populations throughout their native range in Trinidad. The morphology of the opercular flag varied across populations and several aspects of this variation match the predicted hallmarks of sensory drive. First, morphological differentiation of the flag across populations was unrelated to genetic similarity at neutral genetic markers. Second, the shape of the flag covaried with those aspects of body shape that should reflect adaptation to different feeding regimes. Third, and most importantly, the shape of the flag covaried across populations with those environmental characteristics that should most closely reflect differences in local prey abundance. Overall, our results are consistent with a scenario where the evolution of this male sexual signal tracks food-related shifts in female sensory biases across populations, thus providing at least provisional support for a role for sensory drive in population differentiation.

A novel, sexually selected trait in poeciliid fishes: female preference for mustache-like, rostral filaments in male Poecilia sphenops

Female choice can often drive the elaboration of male traits, leading to the evolution of secondary sexual traits. In the Mexican molly, Poecilia sphenops (Poeciliidae), some males exhibit a mustache-like structure on the upper maxilla, the function of which has not been previously recognized. The mustache consists of epidermal outgrowths at the edge of the scales that appear to have no sensory function. Trait expression varies within as well as among populations of P. sphenops, but is not linked to male body size polymorphism. In mate choice experiments, female P. sphenops exhibited a visual mating preference for males with mustaches, suggesting that the trait may be sexually selected. Since the mating behavior of P. sphenops involves contact of the male’s snout and the female genital region prior to copulation, we hypothesize that the mustache may also convey tactile signals to the female.

Mate choice in the dung beetle Onthophagus sagittarius: are female horns ornaments?

Sexual selection typically operates via male contest competition and female choice, favoring the evolution of secondary sexual traits in males. However, there are numerous taxa in which females possess secondary sexual traits and the selective pressures operating on female ornamentation are not well understood. We examined sexual selection operating via mate choice in the dung beetle Onthophagus sagittarius, a species exhibiting sex-specific ornamentation. Precopulatory mate preferences and their subsequent effects on breeding success were examined. Female preferences favored large males and when paired with small males, males with high courtship rates. Large females were choosier than small females. No overt male preferences for female size or ornamentation were found; thus, we conclude that female horns in this species are unlikely to have evolved as ornaments via precopulatory male mate choice. Relative horn length in females determined brood ball productivity, whereas female body size and an interaction between male courtship rate and male body size determined brood ball weight. Our results provide evidence for female but not male mate choice. They suggest that attractive males increase reproductive performance, but it is unclear whether the effect of male phenotype is mediated via differences in paternal investment or female differential allocation toward attractive males. Key words: female horns, mutual mate choice, parental provisioning. [Behav Ecol]

Secondary sexual trait size reveals competitive fertilization success in Drosophila bipectinata Duda

The evolution of male secondary sexual traits traditionally has been ascribed to precopulatory sexual selection. In contrast, the importance of postcopulatory sexual selection for the evolution of secondary sexual traits is uncertain, and what little evidence exists for this process to contribute to the evolution of such traits is mixed. Here we test the hypothesis in Drosophila bipectinata Duda that the male sex comb, a rapidly evolving secondary sexual trait, is under positive postcopulatory sexual selection. We extracted replicate genetic lines exhibiting relatively large and small sex comb size from a natural population. Males from these lines were subjected to an assay of competitive fertilization ability, measured as P2, the proportion of a female’s clutch of eggs fertilized by the second male to mate. Males with the largest sex combs sired more offspring than less ornamented individuals, demonstrating for the first time in any Drosophila species that postcopulatory sexual selection favors increasing sex comb size. This study identifies a postcopulatory selective mechanism that may be contributing to the evolutionary diversification of a secondary sexual trait. Key words: competitive fertilization success, Drosophila bipectinata, ejaculate quality, P2, postcopulatory sexual selection, sex comb size. [Behav Ecol]

EVOLUTIONARY REDUCTION IN TESTES SIZE AND COMPETITIVE FERTILIZATION SUCCESS IN RESPONSE TO THE EXPERIMENTAL REMOVAL OF SEXUAL SELECTION IN DUNG BEETLES

Sexual selection is thought to favor the evolution of secondary sexual traits in males that contribute to mating success. In species where females mate with more than one male, sexual selection also continues after copulation in the form of sperm competition and cryptic female choice. Theory suggests that sperm competition should favor traits such as testes size and sperm production that increase a male's competitive fertilization success. Studies of experimental evolution offer a powerful approach for assessing evolutionary responses to variation in sexual selection pressures. Here we removed sexual selection by enforcing monogamy on replicate lines of a naturally polygamous horned beetle, Onthophagus taurus, and monitoring male investment in their testes for 21 generations. Testes size decreased in monogamous lines relative to lines in which sexual selection was allowed to continue. Differences in testes size were dependent on selection history and not breeding regime. Males from polygamous lines also had a competitive fertilization advantage when in sperm competition with males from monogamous lines. Females from polygamous lines produced sons in better condition, and those from monogamous lines increased their sons condition by mating polygamously. Rather than being costly for females, multiple mating appears to provide females with direct and/or indirect benefits. Neither body size nor horn size diverged between our monogamous and polygamous lines. Our data show that sperm competition does drive the evolution of testes size in onthophagine beetles, and provide general support for sperm competition theory.

Experience leads to preference: experienced females prefer brush-legged males in a population of syntopic wolf spiders

Sexual selection has long been recognized as a potential contributor to the divergence in reproductive characters that ultimately leads to speciation. Schizocosa ocreata and Schizocosa rovneri wolf spiders embody a classic example of species divergence resulting from such sexual selection, as they are reproductively isolated by courtship behavior alone. Here, we characterize a newly discovered population of wolf spiders in which brush-legged males (sensu S. ocreata) and non-ornamented males (sensu S. rovneri) are found syntopically. Mitochondrial sequence data (cytochrome oxidase subunit 1) indicate that the 2 male forms are not reciprocally monophyletic. We exposed subadult females from this mixed population to courtship advances from either brush-legged or non-ornamented males. Experienced females mated significantly more with brush-legged males, whereas inexperienced females showed no mating distinction. In essence, we demonstrate that females from this population will differentially choose between males of 2 distinct forms based on prior experience. Specifically, experience leads to a preference for brush-legged males. We also show that brush-legged males are more sexually aggressive than non-ornamented males. This study highlights the importance of prior experience on subsequent mate choice and has potential implications regarding the extent to which experience can influence polymorphism maintenance and/or species divergence and the evolution of secondary sexual traits.

Contemporary evolution of secondary sexual traits in the wild

SummarySexual selection has been studied intensively, and is often strong in natural populations. Theoretical models, comparative studies and laboratory selection experiments all suggest that evolution driven by sexual selection should be rapid and common.However, there are relatively few documented cases of the contemporary evolution of secondary sexual traits in natural populations. Moreover, the causes are not always due to sexual selection, but often due to altered natural selection regimes, or an altered balance between natural and sexual selection.Here we discuss recent empirical studies that have demonstrated the contemporary evolution of secondary sexual traits in natural populations. Our examples include both continuous traits and discrete polymorphisms. Taxa in which the contemporary (rapid) evolution of secondary sexual traits have been demonstrated include fish, insects, mammals, reptiles and birds. The evolutionary rates of these changes range from 0·005 to 0·570 haldanes (arithmetic mean = 0·14; geometric mean = 0·095; median = 0·12).The relative rarity of examples could be explained by different genetic architectures of sexually selected traits compared with naturally selected traits, or by sexual selection regimes not being sustained in the long term. These factors could potentially slow down evolutionary rates of secondary sexual traits and make the detection of the contemporary evolution empirically more difficult.Promising and underutilized approaches to sexual selection research include reciprocal transplant experiments and estimation of sexual isolation between conspecific populations.

Does dewlap size predict male bite performance in Jamaican Anolis lizards?

Summary The theory of the evolution of secondary sexual traits through male–male competition is based on the assumption that these traits are reliable cues for an animal's fighting capacity. In this paper, we test whether a secondary sexual trait, dewlap size, is an honest predictor of bite strength in Anolis lizards. Since male anoles will bite one another during territorial fights, bite performance may play an important role in determining the outcome of male–male fights. We measured dewlap size and bite force in a size series of adult males of three Jamaican anoles, i.e. Anolis grahami Gray 1845, A. lineatopus Gray 1840 and A. valencienni Duméril & Bibron 1837. In both A. grahami and A. lineatopus, males with relatively large dewlaps tend to bite relatively harder, while the relationship between relative dewlap size and bite force was clearly non‐significant within the twig anole A. valencienni. Our results thus suggest that dewlap size is an indicator of relative bite force in the former two species, but not in the latter. We argue that interspecific variation in territorial behaviour might explain this difference.

Ectoparasites of house sparrows ( Passer domesticus ): an experimental test of the immunocompetence handicap hypothesis and a new model

Conspicuous secondary sexual traits may have evolved as handicap-revealing signals or as badges of status. We present results of an experiment using males of the sexually dimorphic house sparrow (Passer domesticus), that support the idea that the male-specific bib can be both a handicap-revealing signal and a reliable badge indicating the physical condition of the bird. In a test of the immunocompetence handicap hypothesis, wild-caught adult male house sparrows were studied in captivity. Birds implanted with elevated doses of testosterone were more dominant, had higher circulating levels of both testosterone and corticosterone and they also harboured relatively larger ectoparasite loads. Higher parasite loads were also associated with individuals showing lower immunocompetence and larger changes in bib size. A new model for immunocompetence effects in sexual selection is introduced, integrating actions that the hypothalamopituitary axis exerts on gonads, adrenals and the thyroid gland. The ”integrated immunocompetence model” synthesizes both the ”handicap” (i.e. survival-decreasing) and ”badge of status” (i.e. survival- enhancing) models for evolution of secondary sexual traits.

Operational sex ratio influences female preference and male–male competition in guppies

Manipulation of the operational sex ratio (OSR) in guppies, Poecilia reticulata, causes changes in male–male competition and female mate choice. In this study OSR is defined as the number of sexually active males divided by the total number of sexually active adults of both sexes. The rate of male courtship displays decreased, and interference behaviours between males increased, at male-biased OSRs. The OSR influenced both copulatory tactics and postcopulatory guarding. All copulations followed sigmoid displays, except at an OSR of five males to one female where 60% of copulations occurred during sneak attempts. Compared with copulations that followed sigmoid displays, successful sneak copulations were followed by a shorter period of postcopulatory mate guarding and a shorter refractory period before males resumed courtship activities. Females preferred males with more orange colour whenever they had a choice, and the preference for orange colour was stronger with more male-biased OSRs. The OSR thus influences the presence, absence or relative importance of both female mate choice and male–male competition which, in turn, should affect the evolution of secondary sexual traits.