Maternal Gestational Cortisol and Testosterone Are Associated with Trade-Offs in Offspring Sex and Number in a Free-Living Rodent (Urocitellus richardsonii)

Abstract

The adaptive manipulation of offspring sex and number has been of considerable interest to ecologists and evolutionary biologists. The physiological mechanisms that translate maternal condition and environmental cues into adaptive responses in offspring sex and number, however, remain obscure. In mammals, research into the mechanisms responsible for adaptive sex allocation has focused on two major endocrine axes: the hypothalamic pituitary adrenal (HPA) axis and glucocorticoids, and the hypothalamic pituitary gonadal (HPG) axis and sex steroids, particularly testosterone. While stress-induced activation of the HPA axis provides an intuitive model for sex ratio and litter size adjustment, plasma glucocorticoids exist in both bound and free fractions, and may be acting indirectly, for example by affecting plasma glucose levels. Furthermore, in female mammals, activation of the HPA axis stimulates the secretion of adrenal testosterone in addition to glucocorticoids (GCs). To begin to untangle these physiological mechanisms influencing offspring sex and number, we simultaneously examined fecal glucocorticoid metabolites, free and bound plasma cortisol, free testosterone, and plasma glucose concentration during both gestation and lactation in a free-living rodent (Urocitellus richardsonii). We also collected data on offspring sex and litter size from focal females and from a larger study population. Consistent with previous work in this population, we found evidence for a trade-off between offspring sex and number, as well as positive and negative correlations between glucocorticoids and sex ratio and litter size, respectively, during gestation (but not lactation). We also observed a negative relationship between testosterone and litter size during gestation (but not lactation), but no effect of glucose on either sex ratio or litter size. Our findings highlight the importance of binding proteins, cross-talk between endocrine systems, and temporal windows in the regulation of trade-offs in offspring sex and number.

Offspring sex ratio in mammals and the Trivers‐Willard hypothesis: In pursuit of unambiguous evidence

“…2). Maternal glucose and testosterone levels, but not corticosterone levels, were positively associated with the proportion of sons in one [45] of two studies [55] where these three factors have been investigated simultaneously. Maternal glucose and testosterone levels, but not corticosterone levels, were positively associated with the proportion of sons in one [45] of two studies [55] where these three factors have been investigated simultaneously.…”

“…Third, maternal production of glucocorticoids in response to stress may also affect offspring sex ratio through sex-biased embryonic mortality [51]. For example, in Richardson's ground squirrels (Urocitellus richardsonii) stressed females with high levels of cortisol during gestation produce more sons possibly due to a complex relationship between cortisol, testosterone, and embryonic mortality [54,55]. Mothers with high glucocorticoid (cortisol and corticosterone) levels, which are expected to be in poor condition, should thus produce more daughters.…”

Developmental sexual dimorphism and the evolution of mechanisms for adjustment of sex ratios in mammals

“…Those that have looked at multiple factors generally find support for multiple interacting mechanisms (e.g., Refs. and ), which is not surprising given the strong interactions between reproductive and stress hormones and chromosomally determined metabolic and developmental asynchronies. Furthermore, studies have found sex‐ratio adjustment that is highly context specific (e.g., Ref.…”

Costs of Franklin’s ground squirrel (Poliocitellusfranklinii) ectoparasitism reveal adaptive sex allocation

“…No significant difference in the litter size of insecticide-treated versus control females was detected, however, despite the significant and consistent difference in litter sex ratios within the two treatment groups at juvenile emergence. It is possible, by chance alone, that with our small sample of dams in both the manipulated and control group, dams in the manipulated group commenced gestation with larger presumptive litter sizes than those in the control group, and reduced their litters to a similar number of offspring in response to the selective resorption of female blastocysts (Cameron and Linklater 2002;Ryan et al 2012Ryan et al , 2014 or selective neglect of individuals of the non-preferred sex during lactation (Moses et al 1995). We did not, however, sacrifice dams after young were weaned to count placental scars, as would be necessary to collect definitive data on gestational manipulation of offspring sex (though blastocysts resorbed prior to implantation would leave no detectable sign along a uterine horn), or excavate nest burrows for evidence of neglected neonates, out of concern for the persistence of our study population.…”

“…Field research providing supplementary food for Virginia opossums (Didelphis virginiana Kerr, 1792) demonstrated that females are capable of manipulating offspring sex ratio in response to experimentally increased body condition (Austad and Sunquist 1986). Both D r a f t 5 laboratory and field studies have confirmed that females bias the allocation of resources to offspring sex according to dam quality (Labov et al 1986;Meikle et al 1993;Moses et al 1995;Ryan et al 2012Ryan et al , 2014. Inconsistencies in the direction of such biases, however, highlight the complexity of potential trade-offs among body condition, litter size and litter sex ratio in polytocous species.…”