Development Of Secondary Sexual Traits Research Articles

Associations between testosterone and immune activity in alligators depend on bacteria species and temperature

Abstract The immunocompetence handicap hypothesis (ICHH) postulates that testosterone supports the development of secondary sexual traits while simultaneously suppressing immune function, creating a trade‐off between trait quality and pathogen vulnerability. The nature of interactions between testosterone and immunity is complex. Conflicting patterns from the literature suggest that testosterone–immunity relationships are variable across immune measures and may be modified by factors both intrinsic and extrinsic to the organism. In this study, we tested the ICHH in free‐ranging American alligators Alligator mississippiensis and examined how both intrinsic (steroid hormone levels) and extrinsic (temperature) factors modulate the relationship between testosterone and immunity. Specifically, we quantified the simultaneous effects of testosterone and dehydroepiandrosterone (DHEA) on microbial killing capacity of three bacteria species (Escherichia coli, Salmonella typhimurium and Klebsiella pneumoniae) at two challenge temperatures (15°C and 30°C). We found that accounting for circulating levels of DHEA was important for predicting testosterone‐mediated effects on microbial killing capacity. We also found that testosterone‐mediated immunosuppression was dependent on temperature and bacteria species, with negative effects of testosterone present only for S. typhimurium at 15°C. Our results highlight the context dependency of interactions between testosterone and immunity, and illustrate the importance of evaluating the ICHH in natural systems to identify key intrinsic and extrinsic factors modulating testosterone‐immunity trade‐offs. A free Plain Language Summary can be found within the Supporting Information of this article.

The Isolation and Identification of Bacteria on Feathers of Migratory Bird Species.

Worldwide, bacteria are the most ubiquitous microorganisms, and it has been extensively demonstrated that migratory wild birds can increase bacterial global scale dispersion through long-distance migration and dispersal. The microbial community hosted by wild birds can be highly diverse, including pathogenic strains that can contribute to infections and disease spread. This study focused on feather and plumage bacteria within bird microbial communities. Samples were collected during ornithological activities in a bird ringing station. Bacterial identification was carried out via DNA barcoding of the partial 16S rRNA gene. Thirty-seven isolates of bacteria were identified on the chest feathers of 60 migratory birds belonging to three trans-Saharan species: Muscicapa striata, Hippolais icterina, and Sylvia borin. Our results demonstrate the possibility of bacterial transfer, including pathogens, through bird migration between very distant countries. The data from the analysis of plumage bacteria can aid in the explanation of phenomena such as migratory birds’ fitness or the development of secondary sexual traits. Moreover, these results have deep hygienic–sanitary implications, since many bird species have synanthropic behaviors during their migration that increase the probability of disease spread.

Sex Differences in 20-Hydroxyecdysone Hormone Levels Control Sexual Dimorphism in Bicyclus anynana Wing Patterns.

In contrast to the important role of hormones in the development of sexual traits in vertebrates (Cox RM, Stenquist DS, Calsbeek R. 2009. Testosterone, growth and the evolution of sexual size dimorphism. J Evol Biol. 22(8):1586–1598.), the differentiation of these traits in insects is attributed almost exclusively to cell-autonomous mechanisms controlled by members of the sex determination pathway (Verhulst EC, van de Zande L. 2015. Double nexus – doublesex is the connecting element in sex determination. Brief Funct Genomics 14(6):396–406.), such as doublesex. Although hormones can shape the development of sexual traits in insects, variation in hormone levels are not conclusively known to cause dimorphism in these traits (Prakash A, Monteiro A. 2016. Molecular mechanisms of secondary sexual trait development in insects. Curr Opin Insect Sci. 17:40–48.). Here, we show that butterflies use sex-specific differences in 20-hydroxyecdysone hormone titers to create sexually dimorphic wing ornaments. Females of the dry season (DS) form of Bicyclus anynana display a larger sexual ornament on their wings than males, whereas in the wet season form both sexes have similarly sized ornaments (Prudic KL, Jeon C, Cao H, Monteiro A. 2011. Developmental plasticity in sexual roles of butterfly species drives mutual sexual ornamentation. Science 331(6013):73–75.). High levels of circulating 20-hydroxyecdysone during larval development in DS females and wet season forms cause proliferation of the cells fated to give rise to this wing ornament, and results in sexual dimorphism in the DS forms. This study advances our understanding of how the environment regulates sex-specific patterns of plasticity of sexual ornaments and conclusively shows that hormones can play a role in the development of secondary sexual traits in insects, just like they do in vertebrates.

Heterospecific exposure affects the development of secondary sexual traits in male zebra finches (Taeniopygia guttata)

In many animal species, social signals can affect the reproductive physiology and behaviour of conspecifics. In a few species that exhibit vocal learning, exposure to conspecific and sometimes heterospecific sounds can also influence their vocal development. Here we show that heterospecific exposure can affect the development of secondary sexual traits of male zebra finches (Taeniopygia guttata). In a first experiment, we trained young males with a passive playback of domesticated canary (Serinus canaria) song. Song playback enhanced the sexual development of the birds: they started to sing during the presentation of a video clip of a female earlier during development and exhibited secondary sexual plumage ornaments faster than males of the control group kept in silence. Two out of five birds exhibited clear evidence of imitation of canary song. In a second experiment, we raised young male finches with young male canaries in pairs until adulthood. Again, the live contact with a heterospecific companion affected the development of plumage ornaments in finches. We also observed some evidences of vocal convergence, both for calls and song. Moreover, young males of both species could recognize the call of their heterospecific companion when adults. These results suggest that heterospecific exposure can affect both the sexual and the vocal development of the zebra finch and can have long lasting effects.This article is part of a Special Issue entitled: insert SI title.

Male secondary sexual traits are hydrodynamic devices for enhancing swimming performance in a monogamous filefish Paramonacanthus japonicus

The Japanese filefish Paramonacanthus japonicus has extreme sexual dimorphism in its overall shape, even though its mating system is monogamy with biparental care. This sexual dimorphism is mainly due to the development of secondary sexual traits in males. Males become more slender in body with elevated soft dorsal and anal fins as they mature. We examined the function of such male secondary sexual traits by field research and fluid-dynamic analysis. Underwater observations showed that movement rate and steady swimming speed of males were higher than those of females. Male and female P. japonicus showed similar feeding habits and egg-tending behavior, although males attacked potential egg predators more frequently. A wind-tunnel experiment using the air bearing and spring system showed that the drag coefficient of males was significantly lower than that of females, indicating a lower male hydrodynamic drag performance. Also, male elevated soft dorsal and anal fins are considered to give rise to higher thrust performance in monacanthids. Thus, these results suggest that male secondary sexual traits are hydrodynamic devices for enhancing swimming performance that seem to be actually functional under natural conditions. We discuss the evolution of such conspicuous male sexual traits in P. japonicus.

Seasonal variation in the relationship between cellular immune response and badge size in male house sparrows ( Passer domesticus )

The immunocompetence handicap hypothesis postulates that secondary sexual traits are honest signals of male quality because steroid hormones (such as corticosteroids and sex steroids), which are supposed to favor the development of secondary sexual traits, may also have immunosuppressive effects. Certain secondary sexual traits are not only used as mate choice signals but also play a role as badges of status. In the house sparrow (Passer domesticus), males have a bib of black feathers which is used both as a signal of social status in male-male interactions and by females when choosing a mate. We investigated the relationships between bib size and cellular immune response in male house sparrows during and outside the reproductive season. Males with large badges were found to have lower levels of immunocompetence, as assessed using a T-cell-mediated immunity assay, during the reproductive season, as predicted by the immunocompetence handicap hypothesis. Conversely, in November, the correlation between badge size and cellular immune response was positive, possibly reflecting the better access to trophic resources of large-badged dominant males in winter flocks.

Reproductive hormone profiles in captive male orangutans: implications for understanding developmental arrest.

For many years researchers have described some male orangutans as "subadult." These males are of adolescent to adult age and are reproductive, but have little to no secondary sexual trait development. Until now the only endocrine study of this arrest of secondary sexual trait development was performed by Kingsley (1982, 1988). She found that "subadult" or arrested males have lower testosterone levels than similar age developing adolescents or adult males. In this study, urine samples were collected over a two-year period from 23 captive male orangutans in order to more fully define male endocrine profiles. Three study males were juveniles, seven were arrested adolescents, six were developing adolescents, and seven were mature adults. Morning samples were analyzed by radioimmunoassay for levels of testicular steroids and gonadotropins and group hormone profiles were compared by analysis of variance. Results illustrate that arrested adolescent orangutans have significantly lower testosterone and dihydrotestosterone (DHT) levels than developing adolescents, but significantly higher levels than juveniles. Luteinizing hormone (LH) levels also differed between arrested and developing adolescents, with arrested males having lower levels. However, follicle stimulating hormone (FSH) levels were similar in both morphs of adolescent male. The overall hormone profiles for arrested and developing adolescent male orangutans suggest that arrested males lack levels of LH, testosterone, and DHT necessary for development of secondary sexual traits. However, they have sufficient testicular steroids, LH, and FSH to fully develop primary sexual function and fertility. These endocrine data help define alternative developmental pathways in male orangutans. The authors discuss the relationship between these developmental pathways and male orangutan reproductive strategies, and hypothesize about their prepubertal socioendocrine determination.

Potential Reproductive Rates and the Operation of Sexual Selection

In most animals, members of one sex compete more intensely for mates than members of the other sex, and show a greater development of secondary sexual traits. The relative intensity of mating competition in the two sexes depends on the operational sex ratio (OSR) (the ratio of males that are ready to mate to females that are ready to mate) at the site and times when mating occurs. The extent and direction of biases in the OSR is closely related to the potential rates of reproduction that individual males and females can achieve, although the distribution of the two sexes in space and time, sex differences in development time or life expectancy, and biases in the sex ratio at birth or hatching can also be important. The potential rates of reproduction in the two sexes are, in turn, affected by the proportion of time and energy expended by male and female parents on their progeny, though other factors may constrain reproductive rate in one or both sexes. We outline a simple model of the factors affecting the OSR, where relative parental expenditure by the two sexes and the adult sex ratio are fixed, and a more complex model where the adult sex ratio varies in relation to the reproductive activity of the two sexes. This framework for relating sex differences in mating competition to the OSR, potential reproductive rates, and parental expenditure differs from Triver's concept of the relation between parental investment and mating competition in three ways: first, it identifies the OSR as the immediate factor determining which sex completes most intensely for mates; second, it recognizes that factors other than the future fitness costs of rearing offspring can affect the potential reproductive rate of the two sexes; third, it suggests an empirical measure (potential reproductive rate) that can be estimated in natural populations and used to predict the distribution of mating competition.