Final Report Summary - SOCODEV (Social development and life history evolution in cooperative mammals: an integrated approach)
How much does an individual’s health and behaviour in later life depends on the conditions it experienced in the womb, or the amount of care and attention received during development? This is a deep biological question of outstanding interest to researchers in both evolutionary and biomedical science. Much of what we know about early life effects on adult behaviour and life history is derived from studies of laboratory rats and mice living in sterile, controlled conditions. But there is growing recognition that studies of wild animals living in their natural environment can offer new insight into this question, by revealing the extent to which early life effects on behaviour and health reflect evolved, adaptive responses, rather than maladaptive or pathological outcomes. Our project aimed to test how variation in maternal nutrition during pregnancy, and the amount and quality of care received in early life, affect offspring development and adult behaviour and physiology in a uniquely suited wild social mammal, the banded mongoose (Mungos mungo) in Uganda.
Banded mongooses live in extended family groups of around twenty individuals in which there are multiple female breeders. Pregnant females synchronise birth to exactly the same day, and the communal litter is raised by the rest of the group. Over the five years of the project we fed half the breeding females in each group with extra nutrient-rich food during pregnancy, leaving the other half of females as controls. We then followed the fate of their offspring, measuring their growth, hormonal stress, telomere length (a marker of aging and health), and later behaviour. Our results revealed something remarkable: while fed mothers produced larger pups, these fed mothers worked extra hard to raise the offspring of control mothers, so much so that by the end of the care period they had levelled out any differences in weight between their own offspring and those of the control mothers. We have shown using mathematical models that this levelling of inequalities is adaptive for mothers if they cannot discriminate which offspring are their own, and hence there is a chance that the smaller offspring might belong to them. In theoretical terms, there is a ‘veil of ignorance’ over maternity in this system (because of extreme birth synchrony), which favours cooperation and the levelling of inequalities between group members. We are currently testing whether control offspring continue to do as well (or better) than experimental offspring later in life.
In addition to these results, we made several fascinating unanticipated discoveries during the course of the project that have broad relevance for our understanding of evolution. For example, we found evidence that mothers reduce their levels of oxidative damage during pregnancy to protect their developing offspring from harm during sensitive developmental windows (what has come to be known as the ‘oxidative shielding’ hypothesis). We also studied cultural inheritance, and showed that developing offspring learn their adult foraging niche via cultural inheritance from unrelated carers known as ‘escorts’, not from their genetic parents. In this study we confirmed a classic (but untested) theoretical prediction that one-to-one cultural inheritance from a single ‘role model’ promotes behavioural diversity in the group. Finally, we investigated the causes and consequences of intergroup conflict, which is particularly severe in this system. We found that as groups get older, the risk of inbreeding grows, so females seek out matings with neighbouring groups, leading to violent battles in which males are often wounded or even killed. But females are less likely to abort their litter if they are attacked by another group while pregnant, perhaps because there is greater incentive to recruit new members to the group when rival groups threaten their territory. These and other findings have received a great deal of media attention, and inspired new research directions (e.g. to further test the oxidative shielding hypothesis).
Overall our study has shown that postnatal care is used to compensate for prenatal disadvantage in a wild mammal society, and that cultural inheritance operates alongside genetic inheritance to shape lifelong behaviour. More widely, our study demonstrates the power of long-term research on known, individually marked wild animals to advance the frontiers of knowledge of social development and genetic and cultural evolution.
Banded mongooses live in extended family groups of around twenty individuals in which there are multiple female breeders. Pregnant females synchronise birth to exactly the same day, and the communal litter is raised by the rest of the group. Over the five years of the project we fed half the breeding females in each group with extra nutrient-rich food during pregnancy, leaving the other half of females as controls. We then followed the fate of their offspring, measuring their growth, hormonal stress, telomere length (a marker of aging and health), and later behaviour. Our results revealed something remarkable: while fed mothers produced larger pups, these fed mothers worked extra hard to raise the offspring of control mothers, so much so that by the end of the care period they had levelled out any differences in weight between their own offspring and those of the control mothers. We have shown using mathematical models that this levelling of inequalities is adaptive for mothers if they cannot discriminate which offspring are their own, and hence there is a chance that the smaller offspring might belong to them. In theoretical terms, there is a ‘veil of ignorance’ over maternity in this system (because of extreme birth synchrony), which favours cooperation and the levelling of inequalities between group members. We are currently testing whether control offspring continue to do as well (or better) than experimental offspring later in life.
In addition to these results, we made several fascinating unanticipated discoveries during the course of the project that have broad relevance for our understanding of evolution. For example, we found evidence that mothers reduce their levels of oxidative damage during pregnancy to protect their developing offspring from harm during sensitive developmental windows (what has come to be known as the ‘oxidative shielding’ hypothesis). We also studied cultural inheritance, and showed that developing offspring learn their adult foraging niche via cultural inheritance from unrelated carers known as ‘escorts’, not from their genetic parents. In this study we confirmed a classic (but untested) theoretical prediction that one-to-one cultural inheritance from a single ‘role model’ promotes behavioural diversity in the group. Finally, we investigated the causes and consequences of intergroup conflict, which is particularly severe in this system. We found that as groups get older, the risk of inbreeding grows, so females seek out matings with neighbouring groups, leading to violent battles in which males are often wounded or even killed. But females are less likely to abort their litter if they are attacked by another group while pregnant, perhaps because there is greater incentive to recruit new members to the group when rival groups threaten their territory. These and other findings have received a great deal of media attention, and inspired new research directions (e.g. to further test the oxidative shielding hypothesis).
Overall our study has shown that postnatal care is used to compensate for prenatal disadvantage in a wild mammal society, and that cultural inheritance operates alongside genetic inheritance to shape lifelong behaviour. More widely, our study demonstrates the power of long-term research on known, individually marked wild animals to advance the frontiers of knowledge of social development and genetic and cultural evolution.