Sex-specific Divergence Research Articles

Vivianne Tawfik, M.D., Ph.D., a Recipient of the 2022 James E. Cottrell, M.D., Presidential Scholar Award

Vivianne Tawfik, M.D., Ph.D., a Recipient of the 2022 James E. Cottrell, M.D., Presidential Scholar Award

Sex-Specific Population Differences in Resting Metabolism Are Associated with Intraspecific Variation in Sexual Size Dimorphism of Brown Anoles.

AbstractSexual size dimorphism can vary in direction and magnitude across populations, but the extent to which such intraspecific variation is associated with sex and population differences in underlying metabolic processes is unclear. We compared resting metabolic rates (RMRs) of brown anole lizards (Anolis sagrei) from two island populations in the Bahamas (Eleuthera and Great Exuma) that differ in the magnitude of male-biased sexual size dimorphism. Whereas females from each population exhibit similar growth rates and body sizes, males from Great Exuma grow more quickly and attain larger body sizes than males from Eleuthera. We found that these population differences in growth of males persisted in captivity. Therefore, we predicted that males from each population would differ in RMR, whereas females would not. Consistent with this prediction, we found that RMR of males from Eleuthera was higher than that of males from Great Exuma, particularly at higher temperatures. As predicted, RMR of females did not differ between populations. Despite this apparent sex-specific trade-off between growth rate and RMR at the population level, we found a positive relationship between growth rate and RMR at the individual level. The fact that Great Exuma males maintain lower RMR than Eleuthera males, despite their greater absolute growth rates and the positive relationship between RMR and growth rate across individuals, suggests that Great Exuma males may have lower baseline metabolic demands and/or greater growth efficiency than Eleuthera males. Our results call attention to sex-specific divergence in metabolism as a potential mechanism for intraspecific divergence in sexual size dimorphism.

Cross-sex genetic correlations and the evolution of sex-specific local adaptation: Insights from classical trait clines in Drosophila melanogaster.

Natural selection varies widely among locations of a species' range, favoring population divergence and adaptation to local environmental conditions. Selection also differs between females and males, favoring the evolution of sexual dimorphism. Both forms of within-species evolutionary diversification are widely studied, though largely in isolation, and it remains unclear whether environmental variability typically generates similar or distinct patterns of selection on each sex. Studies of sex-specific local adaptation are also challenging because they must account for genetic correlations between female and male traits, which may lead to correlated patterns of trait divergence between sexes, whether or not local selection patterns are aligned or differ between the sexes. We quantified sex-specific divergence in five clinally variable traits in Drosophila melanogaster that individually vary in their magnitude of cross-sex genetic correlation (i.e., from moderate to strongly positive). In all five traits, we observed parallel male and female clines, regardless of the magnitude of their genetic correlation. These patterns imply that parallel spatial divergence of female and male traits is a reflection of sexually concordant directional selection imposed by local environmental conditions. In such contexts, genetic correlations between the sexes promote, rather than constrain, local adaptation to a spatially variable environment.

Sex-specific divergence of antioxidant pathways in fetal brain, liver, and skeletal muscles

The sex-specific divergence of antioxidant pathways in fetal organs of opposite-sex twin is unknown and remains urgently in need of investigation. Such study faces many challenges, mainly the ethical impossibility of obtaining human fetal organs. Opposite-sex sheep twins represent a unique model for studying a sex dimorphism for antioxidant systems. The activity of total superoxide dismutase (SOD), SOD1, SOD2, glutathione peroxidase (GPX), glutathione reductase (GR) and catalase (CAT), the content of total glutathione, reduced glutathione (GSH), and oxidized glutathione (GSSG) were measured in brain, lung, liver, kidney, and skeletal muscles of female and male fetuses collected from sheep twin pregnancies at day 65 of gestation. Lipid peroxidation was assessed by measuring melondialdehyde (MDA) tissue content. Male brain has greater total SOD and SOD1 activities than female brain. Female liver has greater SOD2 activity than male liver. Male liver has greater GR activity than female liver. Male liver has higher total GSH and GSSG content than female liver. Male skeletal muscles have higher total GSH, GSH, and GSSG content than female skeletal muscles. Female brain and liver have higher MDA content than male brain and liver. This is the first report of a sex dimorphism for fetal organ antioxidative pathways. Brain, liver, and skeletal muscles of male and female fetuses display distinct antioxidant pathways. Such sexually dimorphic responses to early life oxidative stress might be involved in the sex-related difference in fetal development that may have a long-term effect on offspring. Our study urges researchers to take into consideration the importance of sex as a biologic variable in their investigations.

Sex-specific divergence for body size and desiccation-related traits in Drosophila hydei from the western Himalayas

Sex-specific-differences are a widespread source of genetic variation in various Drosophila species. In the present study, we have examined desiccation survival in males and females of Drosophila hydei from colder and drier montane conditions of the western Himalayas (altitudinal populations; 600–2202m). In contrast with most other studies in drosophilids, D. hydei males exhibited comparatively higher desiccation resistance despite smaller body size compared to females. Accordingly, we tested the physiological basis of such adaptations in both sexes of D. hydei. Body size traits (wing length, wet weight and dry weight) were ~1.2 fold higher in females than males. However, desiccation resistance was 10 to 13h higher in males than females. These differences matched enhanced storage of trehalose content (~1.2 fold), higher hemolymph content (~1.2 fold) and enhanced cuticular lipid mass (~1.5 fold) in males than females. Water loss before succumbing to death (dehydration tolerance) was much higher in males (~81%) than females (~64%). A greater loss of hemolymph water until death under desiccation stress was associated with higher desiccation resistance in males. Further, there were lacks of differences in the rate of water loss, rate of trehalose utilization and rate of hemolymph depletion between the sexes in D. hydei. Therefore, sex-specific differences in desiccation resistance of D. hydei were independent of body size as well as the exhaustion of metabolite reserves and rather were caused by the higher dehydration tolerance as well as higher acquisition of hemolymph and trehalose contents.

Ontogenetic mechanisms underlying sexual size dimorphism in Urodele amphibians: An across-species approach

Abstract Why do two sexes of the same species differ in body size holds a long-standing question of evolutionary biology. While many across-species comparisons have focused on ultimate causes behind sexual size dimorphism (SSD), only have a few been directed toward elucidating its ontogenetic basis. Urodeles are an amphibian group in which the direction and degree of SSD vary greatly among species. Using demographic data yielded by skeletochronology for 33 urodele species, the current study reveals a positive across-species correlation between SSD and the sex difference in mean age of adult animals, and the latter increases with the corresponding difference in age at maturity; annual growth rate does not differ between the sexes. We conclude that extended longevities in one sex, which is mediated by delayed maturation, would allow it to grow for longer and get larger, with growth rate making a weak contribution to body size. The sex-specific divergence in ontogenetic trajectory might be explained by potentially high growth costs of reproduction to females in association with stronger fecundity selection, and to males that are expected to experience stronger sexual selection.

Apparent Sex-Specific Divergence of Acylation Stimulating Protein Levels With Respect to Metabolic Parameters of Pathogenetic and Clinical Relevance

Background: Acylation stimulating protein (ASP) is an adipose tissue-derived hormone that regulates triglyceride (TG) synthesis and glucose transport. Associations of ASP and / or its precursor complement C3 have been demonstrated with obesity, insulin resistance, diabetes, and cardiovascular diseases. We determined fasting serum ASP in a Turkish adult population sample and assessed relationships with cardiometabolic risk factors. Methods: Cross-sectional population-based study recruiting 224 men and women from the Turkish Adult Risk Factor (TARF) study. Results: Geometric Mean ASP levels (median) in women (271 nmol / L) tended to be lower than men (305 nmol / L) (P = 0.059), and this was also true in most subgroups with vs . without cardiometabolic disorders. Interestingly, correlations of ASP diverged in direction across genders with TG, glucose, height, age and other risk variables. Conclusion: Gender divergence is an aspect of this Turkish population that has been noted for various lipid parameters (HDL, Lp(a)), association of cardiometabolic risk with smoking and alcohol intake and the response of the pro-inflammatory state to adiposity. This is consistent in the present study, where metabolic states correlate with ASP, but are divergent between genders. doi:10.4021/jem58w

Apparent Sex-Specific Divergence of Acylation Stimulating Protein Levels With Respect to Metabolic Parameters of Pathogenetic and Clinical Relevance

Background: Acylation stimulating protein (ASP) is an adipose tissue-derived hormone that regulates triglyceride (TG) synthesis and glucose transport. Associations of ASP and / or its precursor complement C3 have been demonstrated with obesity, insulin resistance, diabetes, and cardiovascular diseases. We determined fasting serum ASP in a Turkish adult population sample and assessed relationships with cardiometabolic risk factors. Methods: Cross-sectional population-based study recruiting 224 men and women from the Turkish Adult Risk Factor (TARF) study. Results: Geometric Mean ASP levels (median) in women (271 nmol / L) tended to be lower than men (305 nmol / L) (P = 0.059), and this was also true in most subgroups with vs . without cardiometabolic disorders. Interestingly, correlations of ASP diverged in direction across genders with TG, glucose, height, age and other risk variables. Conclusion: Gender divergence is an aspect of this Turkish population that has been noted for various lipid parameters (HDL, Lp(a)), association of cardiometabolic risk with smoking and alcohol intake and the response of the pro-inflammatory state to adiposity. This is consistent in the present study, where metabolic states correlate with ASP, but are divergent between genders. J Endocrinol Metab. 2012;2(1):1-10 doi: https://doi.org/10.4021/jem58w

Whole Mount Enzyme Histochemistry as a Rapid Screen at Necropsy for Expression of β-Galactosidase (LacZ)–Bearing Transgenes: Considerations for Separating Specific LacZ Activity from Nonspecific (Endogenous) Galactosidase Activity

Whole mount enzyme histochemistry to localize lacZ-bearing transgenes (lacZ-WMH) also detects endogenous beta-galactosidases. The experiments reported here evaluated lacZ-WMH as a potential tool for transgene expression analysis during high-throughput rodent necropsies. A lacZ-WMH survey of organs from adult, wild-type, male and female mice (C57BL/6, FVB/N) and female rats (Sprague-Dawley) performed at the optimal pH (> or = 7.0) for bacterial lacZ yielded intense endogenous staining in the gonads, kidney, male accessory sex organs, salivary glands, submucosal glands in the duodenum, and thyroid. Substantial staining occurred in the adrenal cortex, lymph nodes, and linings of the gastrointestinal tract, the urinary bladder and uterus, and (for rat only) in the adenohypophysis, bone marrow, thymus, and trigeminal ganglia. Endogenous galactosidases were distributed similarly in sections of flash-frozen organs used for slide-based lacZ histochemistry (lacZ-SBH) at pH < or = 5.0 (optimal for eukaryotic enzymes). Cerebral neurons were labeled only by lacZ-SBH. At pH 7.4, endogenous but not specific lacZ activity was abolished for lacZ-SBH, while endogenous activity was not halted without reducing specific activity for lacZ-WMH. These data demonstrate that lacZ-WMH is feasible during rodent necropsies for many but not all organs if species-, strain-, and sex-specific divergence in endogenous galactosidase activity is considered and special fixation (3% paraformaldehyde for 3 hours at 4 degrees C) is used.

Sex-specific chick provisioning and kleptoparasitism in the Least Frigatebird, Fregata ariel

We examined sex-specific patterns of provisioning behaviour and kleptoparasitic host-use in the Least Frigatebird Fregata ariel. We aimed to determine, first, whether sex-specific kleptoparasitism, either at sea, or adjacent to the breeding colony, is an important source of food for chick provisioning and, second, whether observed behaviour is consistent with the expectation that sexual size-dimorphism in resource-poor environments consistently results in sex-specific divergence of foraging behaviour. We observed sex-specific differences in the time of day that adult frigatebirds provision chicks but no differences in the overall provisioning rate between sexes. We also observed no sex-specific kleptoparasitism via simultaneous monitoring of provisioning by Least Frigatebirds and Masked Boobies. Sex-specific differences in prey types attacked at the colony were observed, but these conflicted with predictions based on previous studies and were directly correlated with diural patterns of adult frigatebird attendance. Overall, we suggest that sexual differences in foraging behaviour in Least Frigatebirds are minimal and relate to either the use of different risk-sensitive foraging strategies by each sex, or are a consequence of body size differences in independently foraging sexes. While our results must be considered preliminary, we believe they provide justification for further critical examination of mechanisms of sex-specific behavioural divergence in seabird taxa.