Clip Whats the difference between male and female hormones?

Thủ Thuật về Whats the difference between male and female hormones? Mới Nhất

Bùi Trường Sơn đang tìm kiếm từ khóa Whats the difference between male and female hormones? được Cập Nhật vào lúc : 2022-11-30 10:10:21 . Với phương châm chia sẻ Thủ Thuật Hướng dẫn trong nội dung bài viết một cách Chi Tiết 2022. Nếu sau khi đọc Post vẫn ko hiểu thì hoàn toàn có thể lại Comments ở cuối bài để Mình lý giải và hướng dẫn lại nha.

Testosterone is a key hormone for the development of secondary sexual characters and dimorphisms in behavior and morphology of male vertebrates. Because females often express detectable levels of testosterone, testosterone has been suggested to also play a role in the modulation of secondary sexual traits in females. Previous comparative analyses in birds and fish demonstrated a relationship between male-to-female testosterone ratios and the degree of sexual dimorphism. Furthermore, female maximum testosterone was related to mating system and coloniality. Here, we reevaluate these previous ideas using phylogenetic analyses and effect size measures for the relationship between birds’ male-to-female maximum testosterone levels. Further, we investigate the seasonal androgen response of female birds (the difference from baseline to maximum testosterone), which in males is strongly related to mating system. We could not confirm a relationship between male-to-female testosterone, maximum female testosterone, or the seasonal androgen response of females with any life-history parameter. We conclude that the expectation that testosterone regulates traits in females in a similar manner as in males should be reconsidered. This expectation may be partially due to hormone manipulation studies using pharmacological doses of testosterone that had similar effects in females than in males but may be of limited importance for the physiological range of testosterone concentrations occurring within ecological and evolutionary contexts. Thus, the assumption that circulating testosterone should covary with ecologically relevant secondary sexual traits in females may be misleading: selection pressures on females differ from those on males and females may regulate behavior differently.

Nội dung chính Show

INTRODUCTIONFemale testosterone—a correlated response to selection on testosterone in males?Mating system and testosteronePlumage and body toàn thân size dimorphism and testosteroneColoniality, latitude, and testosteroneA role of testosterone in the expression of female secondary sexual traits?Future challenges for comparative studies in hormone physiologyCONCLUSIONSSUPPLEMENTARY MATERIALWhat are the different hormones produced by male and female?Who has stronger hormones male or female?What is the difference between male and female testosterone?Can a man have female hormones?

INTRODUCTION

The sex steroid testosterone is a key hormone player with regard to the development of some secondary sexual characters or ornaments in males (including morphological, physiological, and behavioral traits; e.g., Lincoln et al. 1972;,Harding 1981;,Balthazart 1983; Wingfield et al. 1990, 2006; Wingfield and Silverin 2002;,Oliveira 2004;,Hirschenhauser and Oliveira 2006;,Hau 2007;,Fusani 2008b). Although secondary sexual characters are typically more developed in males, females of many species also develop secondary sexual characteristics including weaponry, ornamentation, and aggressive behavior (West-Eberhard 1983;,Andersson 1994; Kraaijeveld et al. 2007). Because female vertebrates often express detectable levels of testosterone and exhibit seasonal cycles of testosterone, several authors have suggested that it may also play a role in the modulation of secondary sexual traits including aggressive behavior in female vertebrates (reviewed, e.g., by Staub and de Beer 1997;,Ketterson et al. 2005;,Rosval 2013).

The evolution of a trait can be influenced by correlations between the effects of genes on male and female characters, and selection acting on one sex may produce a correlated response in the other sex (Lande 1980;,Lande and Arnold 1983). This idea goes back to Darwin (1871) and in this context, it has been suggested that testosterone concentrations in females could be a genetically correlated response to selection on testosterone in males (Ketterson et al. 2005;,Møller et al. 2005;,Mank 2007) and/or vice versa (Ketterson et al. 2005).

Several comparative studies in birds have already attempted to relate levels of testosterone in females to their life history, ecology, and to those of conspecific males. With the exception of one study in actinopterygiian fish (Mank 2007), we are not aware of similar studies in other vertebrate groups (but see Staub and de Beer 1997 for a review on the role of testosterone in female vertebrates and a recent review on “atypical” mammals by French et al. 2013). Three avian studies correlated the ratio of mean maximum levels of testosterone of male and female birds either with a dimorphism index (combining differences in body toàn thân size, plumage, and territorial aggression between males and females; Wingfield 1994;,Wingfield et al. 2000) or with dimorphisms in plumage, territorial aggression, and breeding density separately (Ketterson et al. 2005). These studies assumed that sexual dimorphism could be an indicator of the degree of within-sex competition, that is, the larger sex, the sex with the more brightly colored plumage, or the sex that shows a higher degree of territorial aggression is experiencing a higher degree of within-sex competition than the smaller, the less brightly colored or the less aggressive sex, and that the degree of this competition would be reflected in testosterone concentrations. Indeed, the ratio of mean maximum testosterone concentrations of male and female birds was significantly related to the combined dimorphism index (Wingfield 1994;,Wingfield et al. 2000) or to plumage dimorphism (Ketterson et al. 2005): when dimorphism was low, the ratio of male-to-female testosterone concentrations was lower than when the dimorphism was high. Also, the greater the dimorphism, the more variable was the ratio of male-to-female testosterone.

In addition, Ketterson et al. (2005) found that female maximum testosterone concentrations were related to mating system, with females of socially monogamous mating systems expressing higher levels of testosterone than females of polygynous or polyandrous mating systems.

A fourth avian study investigated the slope of male and female mean maxima of testosterone in a selected subset of birds and found that females of colonial species had relatively higher levels of testosterone compared with females of noncolonial species (Møller et al. 2005). Both Møller et al. (2005) and Ketterson et al. (2005) concluded that current comparative evidence is consistent with both correlated evolution of testosterone concentrations in males and females and with selection acting on each sex separately.

These previous comparative studies (and testosterone manipulation studies) have been crucial in shaping current thinking about the role of testosterone in female birds. But for several reasons, it is timely to reevaluate these previous ideas and discuss them in the light of new analyses.

First, there are several methodological reasons to reanalyze the data. Different species cannot be considered independent data points and hence, any comparison of species needs to take phylogeny into account (Felsenstein 1985). Only the study by Møller et al. (2005) controlled for phylogeny, but this study was limited in scope as it focused on the covariation of male and female testosterone and its relationship to coloniality. Also, state-of-the art meta-analyses (e.g., Arnqvist and Wooster 1995) typically use effect sizes such as Cohen’s d (Cumming and Finch 2001;,Nakagawa and Cuthill 2007), which take the sampling variance of the trait in question into account. As mentioned, the studies by Wingfield (1994), Wingfield et al. (2000), and Ketterson et al. (2005) used the ratios of male-to-female maximum testosterone concentrations, which have the disadvantage that they do not take sampling variance into account and thus may give a biased estimate of differences between males and females. Further, because captivity may have a large effect on plasma testosterone levels (e.g., Calisi and Bentley 2009), a comparison that includes only data from không lấy phí-living wild birds may be more consistent than including data from captive birds (all previous studies). Finally, the dimorphism indices of previous studies unfortunately did not distinguish whether a trait was more prominently expressed in females or males. However, for the evaluation of a dimorphic trait, it is conceptually important to distinguish whether either the male or the female expresses a more brightly colored plumage or a larger body toàn thân size (i.e., it is important to have more brightly colored or larger females on the one end of the scale and more brightly colored or larger males on the other end of the scale; see Methods for details).

Second, there are important conceptual reasons concerning the mechanisms of hormonal action that should make us reconsider the relationship between male and female testosterone within an ecological and evolutionary framework. From a proximate perspective, testosterone manipulation studies in females have nourished the assumption that testosterone has similar effects and functions in females as in males. But is this really the case? Classical studies in endocrinology are concerned with basic mechanisms of hormone action. To study effects of testosterone in males, one would, for example, remove the testes and investigate the changes in behavior, physiology, and morphology (e.g., Berthold 1849). Then, one would attempt to restore the trait in question by administering testosterone (see reviews in Balthazart and Adkins-Regan 2002; Adkins-Regan 2005; Ball and Balthazart 2008). In such studies, females are often used as a “blank slate” to study the organizational and activational effects that testosterone has in males (see, e.g., the classic study on organizational and activational effects of sex steroids on male and female copulation behavior in guinea pigs by Phoenix et al. 1959, or studies on organizational and activational effects of steroids on song or courtship behavior in passerine songbirds, e.g., Leonard 1939;,Gurney and Konishi 1980;,Nottebohm 1980;,Hausberger et al. 1995;,Fusani et al. 2001.,2003.,Day et al. 2007). If females develop male-like traits after administration of testosterone, one would conclude that the trait is testosterone dependent. However, the hormone dosages used in these studies are typically in a pharmacological range: a “normal” female would never experience such concentrations of testosterone under natural and ecologically relevant circumstances. We believe that this rather drastic hormone manipulation approach is well justified within a purely mechanistic perspective (demonstrating that sometimes even fully sexually differentiated females have the capacity to develop male-like traits). But when adopted in a one-to-one manner in physiological or behavioral ecology to study hormone dependency of traits under more natural conditions, this approach may become problematic (see also Rosval 2013). In fact, females may use different mechanisms to generate male-like traits. For example, studies of sex-role-reversed bird species in which females are more competitive than males have failed to demonstrate an important role of high circulating levels of testosterone in the regulation of male-like traits in females (Rissman and Wingfield 1984;,Fivizzani and Oring 1986;,Fivizzani et al. 1986.,1990.,Oring et al. 1988;,Gratto-Trevor et al. 1990;,Goymann and Wingfield 2004;,Goymann et al. 2008). Furthermore, a recent study on the song of the forest weaver (Ploceus bicolor) has convincingly demonstrated that males and females use very different mechanisms to express the same kind of behavior, that is, brain areas that are involved in the control of song are much larger in males, but females show a higher expression of genes relevant for the control of song than males (Gahr et al. 2008). Thus, the rather common assumption that testosterone may have similar functions in female birds as in males is based on relatively weak evidence.

Third, there are important conceptual reasons to reconsider also the ultimate relationship between male and female testosterone within an ecological and evolutionary framework. Previous comparisons of male and female testosterone concentrations and their association with ecologically relevant traits were based on the implicit assumption that the evolution of ornamental traits in females is related directly to sexual selection (representing the predominant explanation for ornamental traits in males; Darwin 1871;,Andersson 1994) or is indirect and evolved as a correlated response to selection acting on males (Darwin 1871). But females may compete for resources and develop secondary sexual characters also outside a mating context and thus these traits may be shaped by evolutionary forces outside the traditional concept of sexual selection (West-Eberhard 1983;,Tobias et al. 2012). Thus, the implicit assumption that secondary sexual characters of females exclusively evolved in a sexual selection context and may thus be related to testosterone could be misleading as well.

Finally, to our knowledge, no study so far has tried to relate the magnitude of the change in testosterone from the seasonal breeding baseline to the breeding maximum concentrations in females to mating system. In male birds, this so-called seasonal androgen response (sensu Goymann et al. 2007) shows a very robust relationship with mating system. This relationship was initially described by Wingfield et al. (1990) and later confirmed for birds (but not other vertebrate groups) by a comparative study (Hirschenhauser and Oliveira 2006).

Because birds are the taxonomic group for which most information regarding plasma testosterone concentrations of không lấy phí-living males and females are available, we decided to base our analysis on this taxon, just as most of the previous studies did. We are convinced, however, that the results will be of general relevance also for other vertebrate groups. Using a coherent, phylogenetically controlled set of plasma testosterone data from 51 không lấy phí-living wild bird species, we here ask whether the standardized difference in mean maximum testosterone concentrations between female and male birds (the standardized effect size) is related to dimorphisms in body toàn thân size and plumage coloration, to the mating system, to the latitudinal distribution of birds (because latitude has an effect in males, see Garamszegi et al. 2005), and to coloniality. Furthermore, we investigated whether maximum levels of testosterone in females relate to any of these parameters and whether the seasonal androgen response of females is related to mating system. In summary, we demonstrate that maximum male-to-female testosterone is not related to measures of dimorphism or any of the other parameters and argue that the expectation that physiological levels of testosterone may have similar effects and functions in female birds as in males may have been misleading and should probably be reconsidered.

METHODS

We reviewed the existing literature (until December 2012) on plasma testosterone levels reported for males and females of the same species taking into account the information provided by previous comparative studies (Wingfield 1994;,Wingfield et al. 2000;,Ketterson et al. 2005;,Møller et al. 2005) and a search in ISI Web of Knowledge using the search terms “testoster*” and “femal*” within the taxonomic group of “aves.” Unlike these previous studies, we only considered data from 51 species of không lấy phí-living, wild birds, because captivity may affect plasma testosterone levels (Calisi and Bentley 2009). To calculate mean peak levels of testosterone of males and females, we included only studies providing several measures (i.e., a seasonal profile) of plasma testosterone for both sexes and a sample size of least 3 individuals for the time of peak testosterone concentrations. The mean peak level of testosterone was defined as the highest average concentration of testosterone (and the respective standard errors) reported in any of the early breeding substages (territory establishment, prebreeding, nest-building, and egg-laying) in actively breeding birds of the respective species. A similar approach was used for baseline testosterone data from females measured during the parental phase, that is, assuming that testosterone levels were basal when females were feeding nestlings (following Wingfield et al. 1990). For cooperative breeders, only data from breeding pairs and not helpers were considered.

A general problem of comparative studies of absolute hormone levels is that hormone concentrations were determined in different laboratories. This is only a minor issue for the following reasons. First, for the male-to-female comparison, we used standardized effect sizes (Cohen’s d) of the difference in male and female maximum levels of testosterone. A similar approach was used for the seasonal androgen response of females. Hence, in these 2 comparisons, absolute differences in hormone levels are no longer relevant ( least when males and females have been measured in the same lab, which is the case in most studies). Second, a previous study did not find any pattern in testosterone that would be explained by lab (Goymann et al. 2004). Nevertheless, for the current study, we decided to include only data gathered by radioimmunoassay (RIA) for the following reason. Several studies have measured plasma testosterone levels of female birds using an Assay Designs (Ann Arbor, MI, #901-065) enzyme immunoassay (EIA) for testosterone. Testosterone levels of female birds measured with this EIA seem consistently higher than those determined by RIA. For example, the testosterone levels of female white-throated sparrows (Zonotrichia albicollis) measured with this EIA (Swett and Breuner 2008) were consistently higher than those of the same species measured with RIA (Spinney et al. 2006). Males of the tan-striped morph of white-throated sparrows had relatively similar mean maximum levels of testosterone with 3ng/mL (EIA; Swett and Breuner 2008) and 2.5ng/mL (RIA; Spinney et al. 2006). In contrast, females of the tan-striped morph had about 1.7ng/mL testosterone with EIA (Swett and Breuner 2008), but only 0.4ng/mL with RIA (Spinney et al. 2006). Thus, because the EIA appears to overestimate testosterone concentrations specifically in females, the relationship between male-to-female testosterone may become distorted. Hence, we decided to include only testosterone data measured after sample extraction with RIA. Also, we did not include testosterone metabolite data from fecal or dropping assays because such assays may not allow a sound comparison of females and males (see Goymann 2005, 2012, for a discussion of this methodological problem).

Information about mating system, body toàn thân size, plumage dimorphism, absolute latitude, and coloniality was extracted from the original papers and additional information using bird handbooks (Cramp 1977;,del Hoyo et al. 1992;,Poole 2005). Similar to previous studies (Wingfield 1994;,Wingfield et al. 2000;,Ketterson et al. 2005), we related differences in testosterone concentration of females and males to differences in body toàn thân size and plumage dimorphism, as well as to mating system (social monogamy, polygyny, classical polyandry, and cooperative breeding) and distinguished whether the species is a colonial breeder or not. With regard to size, the previous studies used a scale from 1 to 3 with 1 = sexes of similar size (80–100% overlap), 2 = 5–80% overlap between sexes, and 3 = no overlap between the sexes. Obviously the studies did not distinguish whether males are larger or females are larger. Instead of a scale, we used body toàn thân mass data extracted from Lislevand et al. (2007) and calculated the proportion of female body toàn thân mass relative to male body toàn thân mass and used this proportion as a covariate in the analysis. With regard to plumage, we scored plumage from −1 (female more brightly colored than male), 0 (female and male with similar plumage) to +1 (male more brightly colored than female). In addition, we also included absolute latitude because previous studies have found that mean maximum testosterone concentrations of male birds can depend on absolute latitude (Goymann et al. 2004;,Garamszegi et al. 2008). The compiled data set with the respective references can be found in Supplementary Tables S1 and S2.

Table 1

Relationship of the standardized difference between male and female maximum testosterone concentrations (Cohen’s d) with coloniality, mating system, plumage and size dimorphism, and latitude

Factor/variable . Posterior mean . −95% CI . +95% CI . P value (MCMC) . DIC . Model 1: effect size ~ coloniality, random = ~animal, mev = effect size variance Colonial (intercept) 1.677 0.276 3.010 168.8 Noncolonial 1.517 0.334 2.683 0.769 Model 2: effect size ~ mating system, random = ~animal, mev = effect size variance Monogamy (intercept) 1.621 0.451 2.829 171.2 Cooperative 0.602 −1.344 2.481 0.270 Polyandry 1.796 0.119 3.789 0.857 Polygyny 1.863 0.328 3.437 0.693 Model 3: effect size ~ plumage dimorphism, random = ~animal, mev = effect size variance Similar (intercept) 1.457 0.368 2.567 Female brighter 1.662 −0.719 4.153 0.858 171.8 Male brighter 1.923 0.566 3.450 0.401 Model 4: effect size ~ body toàn thân size dimorphism, random = ~animal, mev = effect size variance Intercept 1.240 −1.400 3.757 169.9 Body size dimorphism 0.304 −2.095 2.671 0.799 Model 5: effect size ~ latitude, random = ~animal, mev = sampling variance Intercept 0.911 −0.640 2.374 169.1 Latitude 0.016 −0.011 0.042 0.246 Model 6: effect size ~ mating system + body toàn thân size + plumage dimorphism + latitude, random = ~animal, mev = effect size variance Monogamy (intercept) 1.005 −2.532 4.742 178.5 Cooperative 0.213 −3.592 3.908 0.404 Polyandry 1.422 −1.406 4.472 0.709 Polygyny 1.003 −3.471 5.432 0.981 Body size dimorphism 0.043 −3.383 3.601 0.968 Plumage dimorphism 0.308 −2.005 2.535 0.622 Latitude 0.013 −0.018 0.043 0.413

Table 1

Relationship of the standardized difference between male and female maximum testosterone concentrations (Cohen’s d) with coloniality, mating system, plumage and size dimorphism, and latitude

The phylogeny used was derived from Hackett et al. (2008) using MESQUITE (Maddison and Maddison 2007) with arbitrarily ultrametricized branch lengths (Supplementary Figure S1). Effect sizes and their 95% confidence intervals (CIs) between male and female testosterone concentrations and between seasonal baseline and seasonal maxima of testosterone concentrations in females were calculated with the program ESCIdelta (Cumming and Finch 2001). The sampling variance of the effect size was defined as V = [(+95% CI − 95% CI)/4]2. Data were analyzed using a Markov Chain Monte Carlo algorithm (MCMCglmm R package) (Hadfield 2010) in R 2.15 (R Development Core Team) following the instructions for phylogenetic analyses of continuous and categorical characters (Hadfield and Nakagawa 2010). We ran several “animal models” with the effect size difference between maximum testosterone concentrations in males and maximum testosterone concentrations in females as a dependent variable and either body toàn thân size dimorphism, plumage dimorphism, mating system, absolute latitude, or coloniality as separate independent variables or a combined model with body toàn thân size dimorphism, plumage dimorphism, mating system, and absolute latitude as independent variables. When combining all measures in one model, plumage dimorphism was entered as a continuous variable. Similar “animal models” were used to test for an effect of these parameters on female maximum testosterone concentrations and the effect size difference between maximum and breeding baseline concentrations of testosterone (during the parental phase) in females in relation to mating system. In addition, we tested for a correlation of mean maximum testosterone concentrations of males and females. In all models, we controlled for phylogeny (using the random~animal function implemented in MCMCglmm) and measurement error variance (using the mev function implemented in MCMCglmm to control for sampling variance in the effect sizes or mean maximum testosterone concentrations). All models were run in 1000000 iterations with a burn-in period of 60000 iterations and a thinning interval of 100. Autocorrelation of the posterior distribution was checked using the autocorr function implemented in MCMCglmm and model fit was compared using the deviance information criterion (DIC). Meaningful estimates for categorical predictors were extracted by rerunning all models without intercept and reporting the respective posterior means and their confidence limits (following Schielzeth 2011).

To test for publication bias, that is, the likelihood that studies reporting statistically significant effects are more likely to be published than studies with nonsignificant effects, we applied Egger’s regression (Egger et al. 1997) to the meta-analytic residuals (Nakagawa and Santos 2012) plotted against their original measurement error variance using the model of the male–female comparison with the lowest DIC value (model no. 5, latitude only) and the model in which we tested the effect size difference of baseline and maximum testosterone in females with respect to mating system. If the intercept of the Egger’s regression does not significantly differ from zero, then it can be concluded that there is little evidence for publication bias (Egger et al. 1997).

RESULTS

The mean maximum levels of testosterone in male and female bird species were slightly, but significantly, correlated when controlling for phylogeny and sampling variance (MCMCglmm, P = 0.0378; Figure 1).

Mean maximum levels of testosterone in male and female birds are significantly correlated (P = 0.0378). Data points represent means ± 95% CI. The regression line is y = 0.110x + 0.292.

The magnitude of the difference between maximum testosterone concentrations in male and female birds (effect size Cohen’s d) was not related to coloniality (Figure 2a), mating system (Figure 2b), plumage dimorphism (Figure 2c), body toàn thân size dimorphism (Figure 2d), or latitude (Figure 2e and Table 1) when controlling for phylogeny and sampling variance. Also, an overall model including mating system, plumage dimorphism, body toàn thân size dimorphism, and latitude did not explain a significant proportion of the variance in the data (Table 1). In addition, because the previous studies by Wingfield (1994), Wingfield et al. (2000), and Ketterson et al. (2005) used ratios instead of effect sizes, we investigated whether using ratios in a phylogenetic study would give similar results to those reported by these previous authors. However, a phylogenetic analysis of the male-to-female ratio in maximum testosterone from không lấy phí-living birds also did not confirm these previous results (Supplementary Table S3), with the exception that there was a trend for absolute latitude, which was probably driven by testosterone concentrations of males and had nothing to do with females (see below and Garamszegi et al. 2008). The intercept from the Egger’s regression to test for publication bias was statistically significant (b0 = 3.298, 95% CI = 1.991–4.748, Supplementary Figure S2a). This result can be interpreted in 2 ways: Either there is heterogeneity among the studies of our data set, which is caused by unmeasured variables, or the data set is skewed due to publication bias (Egger et al. 1997). Heterogeneity cannot be tested, but publication bias can be assessed by using the trim and fill test, a method to estimate the number of studies that are missing from a meta-analysis and the effect that these studies might have on the outcome of the meta-analysis (Duval and Tweedie 2000). We used the R package meta (Schwarzer 2010) and applied its implemented trim and fill method to the meta-analytic residuals and the corresponding measurement variance. The trim and fill test added 13 additional data points to the original 50 data points and gave an estimate of −0.459 (94% CI = −0.759 to −0.159; Supplementary Figure S2b). Close inspection of Supplementary Figure S2b indicates that the publication bias is due to the fact that there are very few studies with a negative effect size, that is, there are only very few bird species in which females have significantly higher levels of testosterone than males. This “bias” is obviously driven by the fact that males naturally have higher levels of testosterone than females in most species. A true publication bias would indicate that studies reporting significantly higher levels of testosterone in females than in males would be less likely to be published than studies that report higher levels in males than in females (Supplementary Figure S2).

Effect size differences of male-to-female testosterone were not related to (a) coloniality, (b) mating system, (c) plumage dimorphism, (d) body toàn thân size dimorphism, and (e) latitude (see Table 1 for statistics). Data are presented as posterior means (±95% CI) corrected for phylogeny and jittered individual data points.

The magnitude of the difference between maximum testosterone concentrations in male and female birds could be related to either particularly high or low levels in males or particularly high or low levels in females. For example, the effect size could be small because both females and males have very high levels of testosterone, or a similar effect size could emerge because both sexes have very low levels (see also Ketterson et al. 2005). We thus looked whether mean maximum testosterone concentrations of females per se are related to any of the variables in question. Mean maximum levels of testosterone in female birds did not show any relationship with mating system, plumage dimorphism, body toàn thân size dimorphism, coloniality, or absolute latitude (Figure 3 and Table 2), when controlling for phylogeny and sampling variance in female maximum testosterone concentrations.

Table 2

Relationship of female maximum testosterone concentrations with coloniality, mating system, plumage and size dimorphism, and latitude

Factor/variable . Posterior mean . −95% CI . +95% CI . P value (MCMC) . DIC . Model 1: female testo ~ coloniality, random = ~animal, mev = (SEM female testo)2 Colonial (intercept) 0.639 0.161 1.114 51.9 Noncoloniality 0.368 −0.048 0.782 0.144 Model 2: female testo ~ mating system, random = ~animal, mev = (SEM female testo)2 Monogamy (intercept) 0.514 0.060 0.974 60.6 Cooperative 0.299 −0.378 0.973 0.480 Polyandry 0.305 −0.385 1.001 0.495 Polygyny 0.376 −0.186 0.950 0.516 Model 3: female testo ~ plumage dimorphism, random = ~animal, mev = (SEM female testo)2 Similar (intercept) 0.481 0.052 0.901 57.2 Female brighter 0.243 −0.617 1.041 0.528 Male brighter 0.352 −0.159 0.885 0.463 Model 4: female testo ~ body toàn thân size dimorphism, random = ~animal, mev = (SEM female testo)2 Intercept 0.471 0.057 0.858 56.7 Body size dimorphism 0.385 −0.399 1.219 0.359 Model 5: female testo ~ latitude, random = ~animal, mev = (SEM female testo)2 Intercept 0.162 −0.372 0.681 55.1 Latitude 0.007 −0.002 0.016 0.103

Table 2

Relationship of female maximum testosterone concentrations with coloniality, mating system, plumage and size dimorphism, and latitude

Female maximum testosterone concentrations were not related to coloniality (see Table 2 for statistics). Data are presented as posterior means (±95% CI) corrected for phylogeny and jittered individual data points.

Finally, in contrast to the strong relationship in males (Wingfield et al. 1990;,Hirschenhauser and Oliveira 2006;,Goymann et al. 2007), the effect size difference between breeding season baseline levels of testosterone and seasonal maxima of testosterone in female birds was not related to mating system (Figure 4 and Table 3). The intercept of the Egger’s regression to test for publication bias was also statistically significant (b0 = 3.779, 95% CI = 2.437–5.315, Supplementary Figure S3a). Again, also this result can be interpreted in 2 ways: Either there is heterogeneity among the studies of our data set, which is caused by unmeasured variables, or the data set is skewed due to publication bias (Egger et al. 1997). Again, we assessed publication bias by using the trim and fill test (Duval and Tweedie 2000) using the R package meta (Schwarzer 2010) to the meta-analytic residuals and the corresponding measurement variance. In this case, the trim and fill test added 12 additional data points to the original 44 data points and gave an estimate of −0.411 (94% CI = −0.686 to −0.136; Supplementary Figure S3b). Close inspection of Supplementary Figure S3b indicates that the “publication bias” is due to the fact that baseline testosterone concentrations are by definition always lower (or equal) during the parental phase than during the period of peak concentrations of this hormone (Supplementary Figure S3).

Table 3

Effect size of the seasonal androgen response of females in relation to mating system

Factor/variable . Posterior mean . −95% CI . +95% CI . P value (MCMC) . DIC . Model: eff_fem testo ~ mating system, random = ~animal, mev = Var eff_fem testo Monogamy (intercept) 1.034 0.353 1.662 121.4 Cooperative 1.534 0.106 2.825 0.450 Polyandry 0.872 −0.453 2.236 0.801 Polygyny 1.160 0.110 2.271 0.780

Table 3

Effect size of the seasonal androgen response of females in relation to mating system

The effect size of the seasonal androgen response (the difference between seasonal baseline levels of testosterone and the seasonal peak) of female birds was not related to mating system (see Table 3 for statistics). Data are presented as posterior means (±95% CI) corrected for phylogeny and jittered individual data points.

DISCUSSION

In this study, we used effect sizes and phylogeny to study the relationship between male and female maximum levels of plasma testosterone measured in không lấy phí-living birds. The results confirmed earlier reports that mean maximum testosterone levels of male and female birds are correlated (Ketterson et al. 2005;,Møller et al. 2005), albeit with a very shallow slope in the relationship (Figure 1). However, we could not confirm any of the other relationships described in earlier reports: there was no indication that the standardized difference (i.e., effect size) of male-to-female maximum testosterone concentrations was related to mating system, plumage and body toàn thân size dimorphisms, coloniality, or—previously untested—absolute latitude. Also, mean maximum concentrations of testosterone in females per se did not significantly covary with any of these variables. Finally, unlike in male birds (Wingfield et al. 1990;,Hirschenhauser and Oliveira 2006;,Goymann et al. 2007;,Goymann 2009), mating system was not related to the seasonal increase of testosterone in females. Thus, the relationship of male-to-female testosterone did not seem to be a good predictor of sex differences in intra- and intersexual competition and female testosterone concentrations did not seem to relate to differences in female life history. Because our study only considered testosterone in adult males and females, it did not address organizing effects that testosterone may have during ontogenetic development.

Female testosterone—a correlated response to selection on testosterone in males?

Testosterone concentrations of male and female birds were weakly correlated when controlling for phylogeny. But does this imply that female testosterone is a correlated response to selection (and expression) of testosterone in males, or—taking a female perspective (Zuk 2002;,Gowaty 2003)—that male testosterone concentrations could be constrained by selection on low concentrations of this hormone in females (see also Ketterson et al. 2005)? Considering the shallow slope of the relationship and the large variance between and even within species (Figure 1), both ideas seem unlikely, that is, there seem to be some degrees of freedom to avoid a strong constraint. Given that testes—the main tissue producing testosterone in males—do not exist in females and given further that the production, metabolism, and action of testosterone is influenced not just by 1 gene, but by a magnitude of processes (including the expression of production and metabolizing enzymes, receptors, and cofactors; see e.g., Hau 2007), it would be surprising if testosterone concentrations of females would be constrained by selection on males or vice versa. Furthermore, testosterone and androstenedione are precursor molecules of estradiol, a central hormone of female reproductive physiology (Bentley 1998). Thus, all females produce testosterone and/or androstenedione as a first step and then convert them to estradiol (in fact, also in males, many behavioral effects of testosterone are mediated through local conversion to estrogens). It is hard to conceive that females would be constrained in converting testosterone into one of the major sex steroids involved in female reproduction. One of the clearest arguments against the importance of correlated selection with regard to sex steroids is sexual differentiation, a coordinated process that, among other processes, leads to differences in the ratio of estradiol and testosterone between females and males triggering differences in primary and secondary sexual traits without altering other organs or traits (reviewed by Adkins-Regan 2008). Although selection on secondary sexual characteristics indeed can lead to correlated responses in the other sex (e.g., Harrison 1953;,Wilkinson 1993;,Price and Birch 1996;,Chenoweth and Blows 2003), usually such correlated responses are weak (but see Dale et al. 2007 for a potentially strong one). Clutton-Brock (2009) has pointed out that “comparative studies indicate that sex-linked modification of the expression of ornaments (or other sexual traits) is more common than sex-linked inheritance of ornament genes” (see also Amundsen 2000; Wiens 2001;,Pointer et al. 2013). This is particularly true for hormonal pathways, which may show large differences even among closely related species (Hau 2007;,Adkins-Regan 2008). In this context, it is interesting that in fish, the correlation between female and male testosterone has a steep slope (Mank 2007), suggesting a strong connection between female and male testosterone. Given that the magnitude of testosterone expression is similar in female and male fish (Mank 2007), and given that male fish “invented” 11-keto-testosterone that fulfills many of the functions that testosterone does in other vertebrate groups, it is difficult to interpret these findings on testosterone or relate them to those of other vertebrates.

Mating system and testosterone

Arguably, the sample sizes for mating systems other than social monogamy were small (but not smaller than Ketterson et al. 2005, who came to different conclusions) and may prevent a definite answer, but the data did not even show the slightest trend. Even though the sample for nonmonogamous birds was limited, we wonder whether an absence of a relationship between male-to-female testosterone and mating system really is surprising. Previous studies have shown that peak testosterone concentrations of male birds do not vary with mating system (Wingfield et al. 1990;,Beletsky et al. 1995; Hirschenhauser et al. 2003;,Goymann et al. 2004;,Garamszegi et al. 2005; see also summary in Goymann 2010). Hence, any effect related to mating system would need to be driven by differences in maximum testosterone concentrations of females. But if peak testosterone does not vary as a function of mating system in males—the sex in which the hormone arguably plays a role in competition—why should it do so in females? Indeed, also maximum testosterone in females was not related to mating system, when controlling for phylogeny. A number of studies in classically polyandrous birds has demonstrated that maximum testosterone concentrations in females that fiercely compete among each other and often have a more brightly colored plumage than males are similar or even lower than those of species in which females do not compete for access to mates (Rissman and Wingfield 1984;,Fivizzani et al. 1986;,Fivizzani and Oring 1986;,Oring et al. 1988;,Gratto-Trevor et al. 1990;,Goymann and Wingfield 2004). Thus, in a context in which female ornamentation clearly evolved within the sexual selection paradigm, testosterone concentrations of females are not related to competition. However, why should we expect that maximum testosterone should reflect the degree of competition in females, if maximum testosterone is not related to degree of competition in males (see above)? A closer look the significant result of mating system in Ketterson et al. (2005) suggests that the significantly higher levels of testosterone in socially monogamous females were mainly driven by high maximum levels of testosterone (>1ng/mL) in female penguins, albatrosses, the dark-eyed junco, and the Lapland longspur, thus highlighting the importance of controlling for phylogeny (and asking the question why females of these species express such high levels of testosterone?).

What about the seasonal dynamics of testosterone and mating system? In males, the seasonal increase in testosterone is related to mating system with males from socially monogamous mating systems showing a larger increase than polygynous males (Wingfield et al. 1990;,Hirschenhauser and Oliveira 2006;,Goymann et al. 2007). It has been argued that socially monogamous males show this very dynamic response because high levels of testosterone may interfere with parental care (Wingfield et al. 1990). In female birds, the seasonal difference in testosterone from breeding baseline to peak levels was not related to mating system. Again, low sample sizes for mating systems other than social monogamy may preclude definitive answers, but also here, there was not even a trend in the data (but a large scatter in the socially monogamous group). The absence of a relationship of the seasonal change in testosterone with mating system in female birds may not be surprising, though, because peak testosterone levels in females are usually much lower than in males and it is thus unlikely that such low levels would interfere with parental care. Furthermore, in male birds, the testes represent a reliable source of testosterone until they regress the end of the breeding season. In female birds, gonadal testosterone mainly stems from developing follicles that produce sex steroids including testosterone. After finishing egg-laying, the gonadal release of steroids drops (Johnson 1998;,Johnson and Woods 2007;,Williams 2012). Even though primordial and primary follicles may continue to produce steroids (Johnson and Woods 2007), it is likely that after egg-laying, females do not have the capacity to modulate gonadal testosterone in a similar manner as males (see also Jawor et al. 2007 for evidence in dark-eyed juncos). Also in other vertebrate groups, the female gonad typically releases sex steroids in a less predictable manner than that of males (e.g., Crews 1998;,Ferin 1998;,Khan and Thomas 1998). Thus, it is an open question whether the hypothalamic–pituitary–gonadal axis is involved in the regulation of short-term changes in testosterone in female birds and females of other vertebrates. It is well possible that nongonadal sources such as the adrenal gland or the brain could be involved.

Plumage and body toàn thân size dimorphism and testosterone

The phylogenetic effect size analysis could not confirm earlier data suggesting that male-to-female maximum testosterone was significantly related to a dimorphism index (aggression, body toàn thân size, and plumage; Wingfield 1994;,Wingfield et al. 2000) or dimorphism in plumage only (Ketterson et al. 2005). We are fully aware that plumage and the other sexually dimorphic traits served as a proxy for sex differences in competition, but again we wonder whether the absence of a relationship between male-to-female testosterone and plumage dimorphism as a measure for competition is really surprising (even though sample size—in particular for more brightly colored females than males—was again limited, thus possibly preventing a more definite conclusion). From an ultimate perspective, plumage is a complicated trait and sexual selection may not be the only reason for the development of a brightly colored plumage. In particular, the plumage of monomorphic brightly colored and social species may be under selection for social interactions within the group rather than under sexual selection for courtship within a pair (West-Eberhard 1983). In contrast to birds, dichromatism, elongated fins, breeding tubercles, and mating calls in ray-finned fish seem to be unambiguously the result of sexual selection and indeed are related to high levels of 11-keto-testosterone and testosterone in this other vertebrate taxon (Mank 2007).

On a mechanistic level, the dependence of a brightly colored plumage on sex steroids is also debated and may differ depending on the species and molting pattern (e.g., Witschi 1961;,Lindsay et al. 2009, see also Table 4 highlighting the magnitude of control mechanisms of sexual dimorphisms). Postnuptial molt in males typically occurs when androgen levels are low (e.g., Nolan et al. 1992;,Goymann et al. 2006) and can be suppressed by high levels of these hormones (Hahn et al. 1992;,Nolan et al. 1992;,Kimball and Ligon 1999;,Stoehr and Hill 2001; but see Laucht et al. 2011 and McGlothlin et al. 2008 for evidence that breeding season levels of testosterone may correlate with plumage characteristics). Less is known about the influence of androgens on prenuptial molt in males, but there is some evidence that prenuptial molt may indeed be regulated by plasma androgens (e.g., Witschi 1961;,Kimball and Ligon 1999;,Peters et al. 2000;,Day et al. 2006;,Lindsay et al. 2009). Recent evidence suggests that differences in plasma androgen concentrations during prenuptial molt may be even responsible for individual variance in plumage traits including melanin-based and structural colors (Bókony et al. 2008;,Lindsay et al. 2009). In Struthioniformes, Galliformes, and Anseriformes a brightly male-like colored plumage develops in the absence of estrogens, whereas a female-like dull plumage develops in the presence of estrogens (Kimball and Ligon 1999). Similar mechanisms may operate in some passerines (Perlut 2008). Thus, in males of different species, sexually dimorphic plumage traits are regulated by different mechanisms, probably preventing a simple connection of plumage traits to plasma testosterone and sexual selection in males. In comparison, much less is known how elaborate plumage traits are regulated in females. Certainly, females seem to be able to exploit strategies other than plasma testosterone concentrations: In sex-role-reversed red-necked phalaropes (Phalaropus tricolor), females express a more brightly colored breeding plumage than males, but plasma testosterone concentrations of females are far lower than those of males (Gratto-Trevor et al. 1990). Female phalaropes express higher concentrations of androgen conversion enzymes in the skin than males, suggesting that local conversion of sex steroids in the skin could be involved in the regulation of sexually dimorphic plumage in this species (Fivizzani et al. 1990). Hence, a relationship between sex-role-reversed plumage traits and plasma androgens may not necessarily be expected in phalaropes and other species in which females have a more brightly colored plumage than males (but see Muck and Goymann 2011 for an example where testosterone correlates with elaborate female plumage traits). Thus, the influence of androgens depends on the molting pattern (pre- and/or postnuptial molt) and can be regulated locally, preventing a generalization of the relationship between plumage dimorphism and plasma testosterone.

Table 4

Potential control mechanisms of sexual dimorphism in birds

Trait . Ontogenetic/genetic . Epigenetic . Hormonal . Body size and shape Yes Yes Yes Sex-specific brain structures
Song control system, social brain network, parental and aggression circuits, etc. Yes ? Yes Sex-specific color
Plumage, skin, eye iris, eye ring, feet, tarsi, etc. Yes Yes Yes Sex-specific reproductive organs
Oviduct, deferent duct, cloacal protuberance, etc. Yes ? Yes Territorial behavior
Multipurpose territory, lek position, display territory, nest site, mate guarding, etc. Yes Yes Yes Sexual behavior
Pair bonding, courtship, copulatory behavior, etc. Yes Yes Yes Parental behavior
Nest-building, nest maintenance, incubation, brooding, feeding offspring, escort, parental aggression, etc. Yes Yes Yes Parental structures, physiology
Brood patch, crop sac structure, mouth pouches, water carrying, crop-milk, stomach oil, etc. Yes ? Yes

Table 4

Potential control mechanisms of sexual dimorphism in birds

Similarly, is the absence of a relationship between male-to-female testosterone and body toàn thân size dimorphism surprising? Once more, sexual dimorphism in body toàn thân size is a complicated trait, it may have evolved for many reasons and it may be controlled by different mechanisms (including organizing effects of steroids during development, see also Table 4 for an overview of potential mechanisms). Hence, larger body toàn thân size is not necessarily a trait related to increased competition for mates, which could then be reflected in plasma testosterone profiles, if the magnitude of testosterone would be indicative of competition. For example, sexual selection may favor large or small body toàn thân size in males: strong sexual competition for mating partners may favor large-bodied males, whereas in sexual selection for male display agility, females may select even smaller males (Andersson 1994; Székely et al. 2009; but see Dale et al. 2007). But sexual selection is not the only factor shaping differences in body toàn thân size: sexual size dimorphism may have evolved for other reasons, that is, resource division or sexual fecundity (reviewed by Andersson 1994; Blanckenhorn 2000;,Székely et al. 2009). In particular, in classical polyandrous bird species, it is not clear whether females are larger than males because of stronger intrasexual competition between females or because of the fecundity advantages that a larger female may possess. Thus, body toàn thân size difference between the sexes is not a universal indicator of increased competition in the larger sex and, for this simple reason, may not be indicative for the relationship of plasma testosterone levels.

Coloniality, latitude, and testosterone

Møller et al. (2005) found that females of colonial species had significantly higher levels of testosterone compared with females of noncolonial species. Møller et al. (2005) used a phylogeny but included data from species held in captivity. Also, the current data set comprises a larger number of noncolonial species than the initial analysis of Møller et al. (2005). Similar to the mating system effect in the Ketterson et al. (2005), all species in the group of colonial birds in which females have particularly high levels of testosterone are either penguins or albatrosses, suggesting that something is special about this group of birds, when it comes to testosterone concentrations in females. Thus, the effect that Møller et al. (2005) found may not have been related so much to coloniality as such, but to the fact that female penguins and albatrosses that nest colonially, express relatively high levels of testosterone compared with females of other colonially nesting species.

Previous comparative analyses have demonstrated a latitudinal effect on testosterone with a trend that males of high latitude species express higher maximum testosterone concentrations than lower latitude males (Goymann et al. 2004;,Garamszegi et al. 2008), although there are many factors that modify this pattern, in particular, the length of the breeding season: the shorter the breeding season, the higher the peak in testosterone also in low latitude birds (Goymann et al. 2004;,Hau et al. 2008). The present data suggest that a similar effect does not exist in females.

A role of testosterone in the expression of female secondary sexual traits?

These results open the question whether there is evidence for a role of plasma testosterone in the expression of female birds’ secondary sexual traits? No doubt, females express detectable levels of androgens (such as testosterone), androgen-metabolizing enzymes, and androgen receptors, and androgens definitely play a role in the regulation of traits in females (see Introduction and, e.g., the review in Staub and de Beer 1997). However, the common assumption that plasma levels of testosterone play a similar role in females as in males, that is, that the hormone is involved in the expression of secondary sexual traits involved in sexual or social competition, may have been overrated due to the effects found in testosterone manipulation studies (see Introduction). Unfortunately, we are still not good dosing hormone implants within a physiological range: the concentration levels that hormone implants initially generate typically by far exceed the possible physiological levels that are present in the circulation of birds (particularly during the first days after implantation, which is rarely checked; see e.g., the studies of Edler et al. 2011 and Fusani 2008a). Such supraphysiological levels of testosterone are problematic if interpreted within an ecological and evolutionary framework. Tail elongation in widowbirds may serve as an example to illustrate the problem: In his famous study on the effect of the elongation of tails in long-tailed widowbirds (Euplectes progne), Andersson (1982) added about 50% to the average tail of 50cm and found that males with such elongated tails were more successful in recruiting females onto their territories than control males. In contrast, the doses that are commonly used to manipulate testosterone may lead to a short-term increase in testosterone concentrations (i.e., for a few days) that may be 10–20 times higher than average levels experienced by female birds (Fusani 2008a; Quispe-Valdez R, Goymann W, unpublished data). This represents the equivalent of a long-tailed widowbird tail that would be 5–10 m long. We doubt that such an over-exaggerated long tail would allow drawing any firm conclusion about sexual or natural selection (some may find this a lame comparison because as hormone receptors become saturated any additional elevation in hormone levels may be neutral. However, hormone dynamics can be complicated, e.g., Hews and Moore 1997;,Adkins-Regan 2005, p. 37f; thus, the comparison may not be so lame all).

Indeed, there are some studies that looked the relationship between aggressive behavior and natural testosterone levels in không lấy phí-living females. Testosterone levels of females sampled after experimental encounters with female decoys increased in some instances (Desjardins et al. 2006;,Gill et al. 2007;,Ross and French 2011), but not in others (Elekonich 2000;,Davis and Marler 2003;,Rubenstein and Wikelski 2005;,Jawor et al. 2006;,Navara et al. 2006;,Goymann et al. 2008). Although the adaptive significance of changes in testosterone during behavioral interactions is still unclear, the presence or absence of a change in testosterone concentrations in female birds depends on the species and the behavioral context (see also Gill et al. 2007). Experimental studies have shown that—in female birds—testosterone implants may induce song and increase aggression in a similar manner as in males of some species (reviewed by Staub and de Beer 1997;,Fusani et al. 2003;,Ketterson et al. 2005;,Sandell 2007). Yet, as discussed above, the testosterone levels generated by such implants typically by far exceed the levels present in the circulation of unmanipulated birds and may be of limited meaning in an ecological and evolutionary context. In female European robins (Erithacus rubecula), treatment with an antiandrogen did not affect territorial aggression (Kriner and Schwabl 1991). A recent study in dark-eyed juncos (Junco hyemalis) suggests that the endogenous capacity to produce testosterone weakly correlates with the latency of aggressive behavior toward a same-sex-simulated territorial intrusion in females (Cain and Ketterson 2012). Currently, this study (in combination with unpublished data from blackbirds Turdus merula; Miranda C, Goymann W, Partecke J, unpublished data) probably presents the best evidence for a potential role of plasma testosterone in the control of aggressive behavior in a female bird within an ecologically relevant context. Studies in mammals suggest that aggression may be the default state in females and hence does not need to be activated by hormones. Rather, steroid hormones may be involved in suppressing aggression during the fertile phase of females (e.g., Floody 1983). In female mice, progesterone modulates aggression induced by estradiol and testosterone (Albert et al. 1992). Also in black coucals (Centropus grillii), a sex-role-reversed bird species in which females compete for territories, progesterone modulates aggression (Goymann et al. 2008). However, this may not be completely independent of androgens, as female black coucals express more androgen receptors in parts of the brain that are responsible for social and agonistic behavior than males (Voigt and Goymann 2007). In female mountain spiny lizards (Sceloporus jarrovi), estradiol may play the main role in modulating aggressive behavior (Woodley and Moore 1999a, 1999b). In spotted hyenas (Crocuta crocuta), where females are more aggressive than males, there is mixed evidence about the importance of testosterone in mediating female dominance during ontogeny: Dloniak et al. (2006) found a significant correlation of fecal androgen metabolites of mothers during late gestation with the aggression of cubs 2–6 months of age, but East et al. (2009) convincingly demonstrated that competitive ability of offspring adulthood was best explained by postnatal maternal behavioral support rather than exposure to maternal hormone concentrations during gestation. At present, there is little evidence that female dominance and aggression is activated by testosterone in adult spotted hyenas (see e.g., Goymann et al. 2001). Also in ring-tailed lemurs (Lemur catta), females are dominant over males. Agonistic interactions and levels of sex steroids peak during the breeding season, but a causal association between levels of testosterone and aggression has also not been established (von Engelhardt et al. 2000;,Drea 2007). French et al. (2013) list further examples of “atypical” mammals in which females are either more aggressive than or dominant over males, but a clear role of androgens as mediators of “atypical” behavior remains to be established. Current evidence suggests that, in mammals, androgens are more likely to play an organizational role in this respect rather than an activational role (see examples in French et al. 2013). Thus, overall, there is limited evidence that changes in physiological levels of plasma testosterone have a strong impact on aggression in female vertebrates (see also Staub and de Beer 1997). If androgens play a role in the modulation of female morphology or behavior, their regulation may occur on the target tissue level, that is, the local sensitivity to testosterone may be enhanced rather than plasma levels of testosterone (e.g., Voigt and Goymann 2007).

Future challenges for comparative studies in hormone physiology

Neural and endocrine regulatory mechanisms are highly conserved across vertebrates (Wingfield 2005). Nonetheless, there are diverse ways in which this system can be adjusted to customize responses of the individual, male or female. Hormones serve as the signaling molecules and circulate in the blood. So far, comparative studies in hormone physiology have focused on these circulating hormone concentrations and related these hormone levels to the life history, the environment, or other traits of interest. The above examples for a potential role of testosterone in the regulation of traits in females made clear that in the future, it will be important to implement the concept that there is more than one way that a hormone can control a trait. Basically, there are 3 major components to endocrine control systems (Wingfield 2005;,Hau and Wingfield 2011). First is the regulation of hormone secretion from perception of the environmental stimulus and transduction by the brain, which results in release of neuroendocrine signals from the hypothalamus. This triggers the release of tropic hormones from the anterior pituitary gland and, in turn, peripheral endocrine secretions that regulate morphological, physiological, and behavioral responses (see Figure 5 for an example). Second, the transport of many hormones (e.g., steroids and thyroid hormones) involves binding to carrier proteins (e.g., Breuner and Orchinik 2002). Finally, once the hormone signal arrives a target cell, there are multiple fates of that hormone that can have profound influences on the type of response (e.g., Wingfield 2005). In some cases, the target cell may express enzymes that deactivate the hormone before it can interact with a receptor or change it to another form that may interact with a very different receptor (Figure 5). All of these components of the perception–transduction–response axes and the resultant cascade of hormone actions are sites of regulation of how an individual can respond to signals from the physical and social environments. Furthermore, combinations of regulatory points enable highly diverse ways for individuals to respond to similar environmental cues. These may be the bases of species and sex differences in several species studied. Future techniques will have to be developed to assess all of these components simultaneously and implement them in comparative studies.

Potential control mechanisms for avian plumage and skin color in birds. There are 3 major components to control mechanisms: the regulation of hormone secretion from the hypothalamic–pituitary–gonadal axis (left-hand part of the figure), transport of hormones such as testosterone or estradiol in the blood (lines in red), and the mechanisms associated with action of the hormone in the target cell, in this case, a skin or feather follicle cell (central part of the figure). The net result is the regulation of plumage and skin traits (right-hand part of the figure). This 3-part system of control of hormone secretion, transport, and effects on target organs is an important concept because it provides many points of potential regulatory mechanisms. The secretion component on the left summarizes how sensory information is transduced through neurotransmitter, for example, glutamate (NMDA) and neuroendocrine secretions such as gonadotropin-releasing hormone (GnRH) and gonadotropin-inhibiting hormone (GnIH) into release of gonadotropins luteinizing hormone (LH), follicle-stimulating hormone (FSH—not shown), and melanocyte-stimulating hormone (MSH) from the anterior pituitary into the blood. LH circulates to the gonad where it acts on cells that express steroidogenic enzymes to stimulate secretion of sex steroids such as testosterone (T) or estradiol (E2) that are in turn released into the blood. Sex steroids have negative on neuroendocrine and pituitary secretions (not shown). In birds, circulating T and E2 bind weakly to corticosterone-binding globulin (CBG) before entering a target cell. Once T has entered a target cell, it has 4 potential fates. First, T can bind directly to the androgen receptor (AR), a thành viên of the type 1 genomic receptors that become gene transcription factors once they are bound to T. Second, T can be converted to E2 by the enzyme aromatase (aro). E2 can then bind to either estrogen receptor alpha (Erα) or estrogen receptor beta (Erβ) both of which are genomic receptors that regulate gene transcription, but different genes from those regulated by AR. Third, T can be converted to 5alpha-dihydrotestosterone (5α-DHT) that also binds to AR and cannot be aromatized, thus enhancing the AR gene transcription pathway. Fourth, T can be converted to 5beta-dihydrotestosterone (5β-DHT) that binds to no known receptors and also cannot be aromatized, indicating a deactivation shunt. A complex system of corepressors and coactivators of genomic steroid receptor action are also known. The end result is regulatory action in the skin or feather follicle cell. Even in species in which the gonads do not affect plumage dimorphism, it is possible that sex steroids may play a role, as they can be produced locally: steroid metabolizing enzymes are present in skin, see for example, Schlinger et al. (1989).

CONCLUSIONS

Our analysis has shown that relating sexually dimorphic traits to testosterone in birds is problematic because such traits can evolve for reasons other than sexual selection and may not necessarily be controlled by sex steroids. Thus, for a proper comparison, it would be necessary to know whether plumage and body toàn thân size dimorphisms are related to sexual selection and whether the molt of a species is under androgenic control. Further, pharmacological manipulations of testosterone that lead to the expression of male-like traits in females have generated the assumption that secondary sexual traits are regulated in a similar manner in females and males. However, to draw firm conclusions about the role of testosterone in the expression of secondary sexual traits in females within an ecophysiological and evolutionary context, it will be essential to manipulate testosterone within the physiological range and during various stages of ontogenetic development.

Overall, the relationship of male-to-female testosterone may not be a good predictor of sex differences in intra- and intersexual competition. Females are likely to use other means to regulate aggression or sexually dimorphic traits such as a colorful plumage. The regulation may occur other stages of the perception–transduction–response system of hormones or females may rely on completely different mechanisms than males (see Gahr et al. 2008 for an illustrative example). The discussion above shows that meta-analyses of hormone levels face the challenge that the action of hormones is regulated different times and different levels (Wingfield 2012) and that sexually dimorphic traits can be modulated by interactions of physiology, genetics, and the environment (Table 4). The degree of regulation each of these different levels may differ between species, between the sexes, and even between individuals (giving rise to different phenotypes). This very much complicates meta-analyses that focus on just one time point or level (i.e., the level of hormone secretion during adulthood in the current case), but we are on the verge of new technologies that will allow us to address the various levels of regulatory mechanisms (e.g., Pavey et al. 2012).

SUPPLEMENTARY MATERIAL

Supplementary material can be found Supplementary Data

FUNDING

J.C.W. is grateful for support from grant number IOS-0750540 from the National Science Foundation and the Endowed Professorship in Physiology from the University of California, Davis. W.G. is grateful for funding from M. Gahr and the Max-Planck Gesellschaft.

This article is dedicated to W. Wickler on occasion of his 82nd birthday. We would like to thank L. Fusani, M. Hau, K. Hirschenhauser, E. Ketterson, and 2 anonymous referees who critically read previous versions of this manuscript and whose comments greatly improved these earlier drafts. Furthermore, we would like to thank S. Nakagawa for suggesting the use of Egger’s regression test and practical help in implementing it to the MCMCglmm models.

REFERENCES

Hormones and animal social behavior

. :

Princeton University Press

Do hormonal control systems produce evolutionary inertia?

. :–.

Interaction of estradiol, testosterone, and progesterone in the modulation of hormone-dependent aggression in the female rat

. . :–.

Why female birds are ornamented?

. :–.

Female choice selects for extreme tail length in a widowbird

. . :–.

. . :

Princeton University Press

Meta-analysis: synthesizing research findings in ecology and evolution

. . :–.

Individual variation and the endocrine regulation of behaviour and physiology in birds: a cellular/molecular perspective

. . :–.

Hormonal correlates of behavior

. In: , editors. . Vol. . : . p. –.

Sexual differentiation of brain and behavior in birds

. In: , editors.

Hormones, brain and behavior

. : . p. –.

Testosterone and polygyny in birds

. . :–.

Comparative vertebrate endocrinology

. 3rd ed. :

Cambridge University Press

Transplantation der Hoden

Arch Anat Physiol Wissensch Med

. :–.

The evolution of body toàn thân size: what keeps organisms small?

. :–.

Testosterone and melanin-based black plumage coloration: a comparative study

. . :–.

Downstream from corticosterone: seasonality of binding globulins, receptors and behavior in the avian stress response

. In: , editors. . : . p. –.

Competitive females are successful females; phenotype, mechanism, and selection in a common songbird

. . :–.

Two sides of the same coin? Consistency in aggression to conspecifics and predators in a female songbird

. . :–.

Lab and field experiments: are they the same animal?

. :–.

Signal trait sexual dimorphism and mutual sexual selection in Drosophila serrata

. . :–.

Sexual selection in females

. . :–.

Handbook of the birds of Europe, the Middle East and North Africa: the birds of the western Palearctic

. : .

Reptilian reproduction, overview

. In: , editors.

Encyclopedia of reproduction

. : . p. –.

A primer on the understanding, use, and calculation of confidence intervals that are based on central and noncentral distributions

. . :–.

Sexual selection explains Rensch’s rule of allometry for sexual size dimorphism

. . :–.

The descent of man, and selection in relation to sex

. :

The progesterone challenge: steroid hormone changes following a simulated territorial intrusion in female Peromyscus californicus

. . :–.

Testosterone and its effects on courtship in golden-collared manakins (Manacus vitellinus): seasonal, sex, and age differences

. . :–.

Testosterone increases display behaviors but does not stimulate growth of adult plumage in male golden-collared manakins (Manacus vitellinus)

. . :–.

Male and female cooperatively breeding fish provide support for the “Challenge Hypothesis”

. . :–.

Rank-related maternal effects of androgens on behaviour in wild spotted hyaenas

. . :–.

Sex and seasonal differences in aggression and steroid secretion in Lemur catta: are socially dominant females hormonally `masculinized’?

. :–.

Trim and fill: a simple funnel-plot–based method of testing and adjusting for publication bias in meta-analysis

. . :–.

Maternal effects on offspring social status in spotted hyenas

. . :–.

Experimentally elevated testosterone levels enhance courtship behaviour and territoriality but depress acquired immune response in red bishops Euplectes orix

. . :–.

Bias in meta-analysis detected by a simple, graphical test

. . :–.

Female song sparrow, Melospiza melodia, response to simulated conspecific and heterospecific intrusion across three seasons

. . :–.

Androgen levels and female social dominance in Lemur catta

. . :–.

Phylogenies and the comparative method

. . :–.

. . In: , editors.

Encyclopedia of reproduction

. : . p. –.

Plasma steroid hormone levels in không lấy phí-living Wilson’s phalaropes, Phalaropus tricolor

. . :–.

Plasma steroid hormones in relation to behavioral sex role reversal in the spotted sandpiper, Actitis macularia

. . :–.

Hormonal basis of male parental care and female intersexual competition in sex-role reversed birds

. In: , editors.

Endocrinology of birds: molecular to behavioral

. : . p. –.

Hormones and aggression in female mammals

. In: , editor.

Hormones and aggressive behavior

. : . p. –.

The influence of androgenic steroid hormones on female aggression in ‘atypical’ mammals

. . :.

Endocrinology in field studies: problems and solutions for the experimental design

. . :–.

Testosterone control of male courtship in birds

. . :–.

Testosterone regulates the activity and expression of aromatase in the canary neostriatum

. . :–.

Aromatase inhibition affects testosterone-induced masculinization of song and the neural song system in female canaries

. . :–.

Bi-directional sexual dimorphisms of the song control nucleus HVC in a songbird with unison song

. . :.

Testosterone, testes size, and mating success in birds: a comparative study

. . :–.

Latitudinal distribution, migration, and testosterone levels in birds

. . :–.

Context matters: female aggression and testosterone in a year-round territorial Neotropical songbird (Thryothorus leucotis)

. . :–.

Sexual natures: how feminism changed evolutionary biology

. . :–.

Non-invasive monitoring of hormones in bird droppings: biological validations, sampling, extraction, sex differences, and the influence of diet on hormone metabolite levels

. . :–.

Social modulation of androgens in male birds

. . :–.

Pair-bonding, mating systems and hormones

. In: , editors.

Encyclopedia of animal behavior

. : . p. –.

On the use of non-invasive hormone research in uncontrolled, natural environments: the problem with sex, diet, metabolic rate and the individual

. . :–.

Androgens and the role of female “hyperaggressiveness” in spotted hyenas (Crocuta crocuta)

. . :–.

Testosterone and corticosterone during the breeding cycle of equatorial and European stonechats (Saxicola torquata axillaris and S. t. rubicola)

. . :–.

Distinguishing seasonal androgen responses from male-male androgen responsiveness—revisiting the Challenge Hypothesis

. . :–.

Testosterone in tropical birds: effects of environmental and social factors

. . :–.

Competing females and caring males. Sex steroids in African black coucals, Centropus grillii

. . :–.

Progesterone modulates aggression in sex-role reversed African black coucals

. . :–.

Seasonal changes in gonadal steroids of a monogamous versus a polyandrous shorebird

. . :–.

Hormone-induced sexual differentiation of brain and behavior in zebra finches

. . :–.

et al.

A phylogenomic study of birds reveals their evolutionary history

. . :–.

MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package

. . :–.

General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters

. . :–.

Adjustments of the prebasic molt schedule in birds

. . :–.

Social modulation of circulating hormone levels in the male

. . :–.

Reversal of a secondary sex character by selection

. . :–.

Regulation of male traits by testosterone: implications for the evolution of vertebrate life histories

. . :–.

Tropical field endocrinology: ecology and evolution of testosterone concentrations in male birds

. . :–.

Hormonally-regulated trade-offs: evolutionary variability and phenotypic plasticity in testosterone signaling pathways

. In: , editors.

Molecular mechanisms of life history evolution

. : . p. –.

Testosterone-induced singing in female European starlings (Sturnus vulgaris)

. . :–.

Hormones and sex-specific traits: critical questions

. In: , editor.

Parasites and pathogens: effects on host hormones and behavior

. : p. –.

Social modulation of androgens in male vertebrates: meta-analyses of the challenge hypothesis

. . :–.

Comparative analysis of male androgen responsiveness to social environment in birds: the effects of mating system and paternal incubation

. . :–.

Handbook of the birds of the world

. : .

Testosterone response to GnRH in a female songbird varies with stage of reproduction: implications for adult behaviour and maternal effects

. . :–.

Females competing to reproduce: dominance matters but testosterone may not

. . :–.

Ovarian cycles and follicle development in birds

. In: , editors.

Encyclopedia of reproduction

. : . p. –.

Ovarian dynamics and follicle development

. In: , editor.

Reproductive biology and phylogeny of birds

. : . p. –.

Testosterone in females: mediator of adaptive traits, constraint on sexual dimorphism, or both?

. :–.

Ovarian cycles, teleost fish

. In: , editors.

Encyclopedia of reproduction

. : . p. –.

Evolution of avian plumage dichromatism from a proximate perspective

. . :–.

The evolution of mutual ornamentation

. . :–.

Control of winter song and territorial aggression of female robins (Erithacus rubecula) by testosterone

. . :–.

Sexual dimorphism, sexual selection, and adaptation in polygenic characters

. . :–.

The measurement of selection on correlated characters

. . :–.

Individual variation in plasma testosterone levels and its relation to badge size in house sparrows Passer domesticus: it’s a night-and-day difference

. . :–.

Induction of singing in female canaries by injections of male hormone

. . :–.

The way in which testosterone controls the social and sexual behavior of the red deer stag (Cervus elaphus)

. . :–.

Plumage colour acquisition and behaviour are associated with androgens in a phenotypically plastic tropical bird

. . :–.

Avian body toàn thân sizes in relation to fecundity, mating system, display behavior, and resource sharing

. . :.

Mesquite: a modular system for evolutionary analysis. Version 2.75 [cited on 2014 February 8]

. Available from: ://mesquiteproject.org.

The evolution of sexually selected traits and antagonistic androgen expression in actinopterygiian fishes

. . :–.

Hormones and honest signals: males with larger ornaments elevate testosterone more when challenged

. . :–.

Correlated evolution of male and female testosterone profiles in birds and its consequences

. . :–.

Throat patch size and darkness covaries with testosterone in females of a sex-role reversed species

. . :–.

Effect size, confidence interval and statistical significance: a practical guide for biologists

. . :–.

Methodological issues and advances in biological meta-analysis

. . :–.

Yolk androgens vary inversely to maternal androgens in eastern bluebirds: an experimental study

. . :–.

Testosterone and avian life histories: effects of experimentally elevated testosterone on prebasic molt and survival in male dark-eyed juncos

. . :–.

Testosterone triggers growth of brain vocal control nuclei in adult female canaries

. . :–.

Social modulation of androgens in vertebrates: mechanisms and function

. . :–.

Hormonal changes associated with natural and manipulated incubation in the sex-role reversed Wilson’s phalarope

. . :–.

What is needed for next-generation ecological and evolutionary genomics?

. :–.

Female bobolink molts into male-like plumage and loses fertility

. . :–.

Testosterone is involved in acquisition and maintenance of sexually selected male plumage in superb fairy wrens, Malurus cyaneus

. . :–.

Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig

. . :–.

Masculinization of gene expression is associated with exaggeration of male sexual dimorphism

. . :.

The birds of North America online

. :

Cornell Laboratory of Ornithology

Repeated evolution of sexual color dimorphism in passerine birds

. . :–.

Hormonal correlates of polyandry in the spotted sandpiper, Actitis macularia

. . :–.

Female marmosets’ behavioral and hormonal responses to unfamiliar intruders

. . :–.

Proximate perspectives on the evolution of female aggression: good for the gander, good for the goose?

. :.

Steroid hormones and aggression in female Galapagos marine iguanas

. . :–.

Exogenous testosterone increases female aggression in the European starling (Sturnus vulgaris)

. . :–.

Simple means to improve the interpretability of regression coefficients

. . :–.

Aromatase, 5a- and 5b-reductase in brain, pituitary and skin of the sex-role reversed Wilson’s phalarope

. . :–.

Endocrine correlates of alternative phenotypes in the white-throated sparrow (Zonotrichia albicollis)

. . :–.

The role of androgens in female vertebrates

. . :–.

The effects of elevated testosterone on plumage hue in male house finches

. . :–.

Interaction of testosterone, corticosterone and corticosterone binding globulin in the white-throated sparrow (Zonotrichia albicollis)

Comp Biochem Physiol A Mol Integr Physiol

. :–.

Sexual size dimorphism in birds

. In: , editors.

Sex, size & gender roles. Evolution of sexual size dimorphism

. : . p. –.

The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition

. . :–.

Sex-role reversal is reflected in the brain of African black coucals (Centropus grillii)

. . :–.

Sexual selection, social competition, and speciation

. . :–.

Widespread loss of sexually selected traits: how the peacock lost its spots

. . :–.

Artificial sexual selection alters allometry in the stalk-eyed fly Cyrtodiopsis dalmanni (Diptera: Diopsidae)

. . :–.

Physiological adaptations for breeding in birds

. :

Princeton University Press

Hormone-behavior interactions and mating systems in male and female birds

. In: editors.

The differences between the sexes

. :

Cambridge University Press

. p. –.

Communicative behaviors, hormone–behavior interactions, and reproduction in vertebrates

. In: , editor.

Physiology of reproduction

. : . p. –.

Regulatory mechanisms that underlie phenology, behavior, and coping with environmental perturbations: an alternative look biodiversity

. . :–.

The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies

. . :–.

Toward an ecological basis of hormone-behavior interactions in reproduction of birds

. In: , editors. . : p. –.

Contexts and ethology of vertebrate aggression: implications for the evolution of hormone-behavior interactions

. : editor. . : . p. –.

Ecophysiological studies of hormone-behavior relations in birds

. In: , editors.

Hormones, brain and behavior

. : . p. –.

Sex and secondary sexual characteristics

. In: , editor.

Biology and comparative physiology of birds

. : . p. –.

Female territorial aggression and steroid hormones in mountain spiny lizards

. . :–.

Ovarian hormones influence territorial aggression in không lấy phí-living female mountain spiny lizards

. . :–.

Sexual selections. What we can and what we can’t learn about sex from animals

. :

University of California Press

What are the different hormones produced by male and female?

The main reproductive hormones estrogen, testosterone, and progesterone are instrumental in sexuality and fertility. They are responsible for pregnancy, puberty, menstruation, menopause, sex drive, sperm production and more. These hormones are produced in the ovaries (in females) and testes (in males).

Who has stronger hormones male or female?

Women, however, also have naturally occurring testosterone, and testosterone sometimes functions via conversion to estradiol (4). Although testosterone exists and functions similarly in women and men, men have markedly higher average testosterone than women.

What is the difference between male and female testosterone?

They remain lower than 2 nmol/L in women of all ages. However, from the onset of male puberty the testes secrete 20 times more testosterone resulting in circulating testosterone levels that are 15 times greater in healthy young men than in age-similar women.

Can a man have female hormones?

Although it's called the female hormone, a man's body toàn thân also makes estrogen. A healthy balance of estrogen and testosterone is important for sexual growth and development. When these hormones become imbalanced, your sexual development and function may be affected. Tải thêm tài liệu liên quan đến nội dung bài viết Whats the difference between male and female hormones?

Video Whats the difference between male and female hormones? ?

Bạn vừa Read nội dung bài viết Với Một số hướng dẫn một cách rõ ràng hơn về Video Whats the difference between male and female hormones? tiên tiến nhất

Chia Sẻ Link Tải Whats the difference between male and female hormones? miễn phí

Người Hùng đang tìm một số trong những ShareLink Download Whats the difference between male and female hormones? miễn phí.

Hỏi đáp thắc mắc về Whats the difference between male and female hormones?

Nếu sau khi đọc nội dung bài viết Whats the difference between male and female hormones? vẫn chưa hiểu thì hoàn toàn có thể lại Comments ở cuối bài để Mình lý giải và hướng dẫn lại nha #Whats #difference #male #female #hormones - 2022-11-30 10:10:21

Clip Whats the difference between male and female hormones? - Lớp.VN

Thủ Thuật về Whats the difference between male and female hormones? Mới Nhất

INTRODUCTION

METHODS

RESULTS

DISCUSSION

Female testosterone—a correlated response to selection on testosterone in males?

Mating system and testosterone

Plumage and body toàn thân size dimorphism and testosterone

Coloniality, latitude, and testosterone

A role of testosterone in the expression of female secondary sexual traits?

Future challenges for comparative studies in hormone physiology

CONCLUSIONS

SUPPLEMENTARY MATERIAL

FUNDING

REFERENCES

What are the different hormones produced by male and female?

Who has stronger hormones male or female?

What is the difference between male and female testosterone?

Can a man have female hormones?

Video Whats the difference between male and female hormones? ?

Chia Sẻ Link Tải Whats the difference between male and female hormones? miễn phí

Hỏi đáp thắc mắc về Whats the difference between male and female hormones?

نموذج الاتصال