Abstract
Females of many species adaptively program their offspring to predictable environmental conditions, a process that is often mediated by hormones. Laboratory studies have shown, for instance, that social density affects levels of maternal cortisol and testosterone, leading to fitness-relevant changes in offspring physiology and behaviour. However, the effects of social density remain poorly understood in natural populations due to the difficulty of disentangling confounding influences such as climatic variation and food availability. Colonially breeding marine mammals offer a unique opportunity to study maternal effects in response to variable colony densities under similar ecological conditions. We therefore quantified maternal and offspring hormone levels in 84 Antarctic fur seals (Arctocephalus gazella) from two closely neighbouring colonies of contrasting density. Hair samples were used as they integrate hormone levels over several weeks or months and therefore represent in utero conditions during foetal development. We found significantly higher levels of cortisol and testosterone (both P < 0.001) in mothers from the high density colony, reflecting a more stressful and competitive environment. In addition, offspring testosterone showed a significant positive correlation with maternal cortisol (P < 0.05). Although further work is needed to elucidate the potential consequences for offspring fitness, these findings raise the intriguing possibility that adaptive foetal programming might occur in fur seals in response to the maternal social environment. They also lend support to the idea that hormonally mediated maternal effects may depend more strongly on the maternal regulation of androgen rather than cortisol levels.
Highlights
In mammalian species, most of the development of all major organs occurs during the prenatal phase, making the foetus vulnerable to external influences
A significant positive correlation was observed between maternal cortisol and testosterone that was unaffected by colony density (Fig 3, Model 3, Table 2; t = 8.22, P < 0.001)
Pup testosterone levels were elevated in the high density colony and correlated positively with maternal cortisol (Fig 3; Model 6, Table 2; t = 2.03, P < 0.05) but not with maternal testosterone (Model 7, Table 2; t = 0.38, P = 0.70)
Summary
Most of the development of all major organs occurs during the prenatal phase, making the foetus vulnerable to external influences. It has been proposed that environmental stimuli during critical periods may alter foetal development, with important implications for the offspring later in life Foetal Programming to Social Density fee by the Deutsche Forschungsgemeinschaft and the Open Access Publication Funds of Bielefeld University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript
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