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.
Highlights
Since its inception, adaptive sex allocation (ASA) has been of great interest to evolutionary biologists and ecologists, but has largely focused on the environmental conditions favoring the production of offspring of one sex over the other [1,2,3,4]
A separate analysis found that total plasma cortisol and free cortisol were significantly higher for the sampling protocol described here than from baseline samples taken within 3 minutes, bound cortisol, testosterone, and glucose were not [41]
Physiological parameters throughout the breeding season Total plasma cortisol decreased throughout the breeding season, with significantly lower levels during lactation compared to early gestation (Table 1)
Summary
Adaptive sex allocation (ASA) has been of great interest to evolutionary biologists and ecologists, but has largely focused on the environmental conditions favoring the production of offspring of one sex over the other [1,2,3,4]. The first, involving glucocorticoids (GCs, cortisol and/or corticosterone) and the hypothalamic-pituitary adrenal (HPA) axis, was founded on observations that social and environmental stressors were linked to sex ratio in both birds [16,17] and mammals [14,18] Given their role in reproduction, embryonic development, and immune function, GCs are promising candidates for the translation of ecological and physiological cues into ASA [19,20,21]. [26]) about the function of free versus bound glucocorticoids, their biological relevance to downstream physiological metrics [27], and their effects on individual life history strategies [28] This additional layer of complexity could prove necessary for understanding potential mechanisms connecting GCs and sex ratio
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