Social Determinants of Immature Phenotype and Survival in Wild Baboons and Other Mammals
Abstract If any animal is to reproduce, it must first survive to adulthood. It must navigate a veritable gauntlet as it develops first from a single-celled embryo to an immature animal living outside of its egg or mother, then through a growth phase of sexual immaturity before finally reaching adulthood. The nature and duration of these life stages varies greatly across species, but the period of an animal’s life prior to attaining sexual maturity is universally one of great vulnerability. The risks faced by immature individuals are numerous, and the determinants of survival are multi-faceted and often difficult to observe and measure. As a result, the task of understanding all the factors contributing to offspring survival in a single species may seem hopelessly challenging, even in a relatively well-studied model organism living under controlled conditions. This challenge is even greater when considering free-living animals that are subject to neither invasive monitoring, experimental manipulation, nor human protection from the environment.
The goal of this dissertation is to bring us closer to that lofty target by providing insight into the role that the social environment plays in immature survival in populations of wild mammals. In it, I place a particular emphasis on social determinants of immature development, behavior, and survival in the wild baboons of the Amboseli basin.The Amboseli baboons have been under continuous, near-daily observation since 1971. For five decades, researchers have collected a wealth of high-quality demographic, environmental, and behavioral data from over 1700 live-born individuals, as well as data from nearly 300 failed pregnancies. This extraordinary dataset has allowed me to explore a wide range of questions focused on offspring survival and phenotype in early life, before and after birth. This historical data has been my primary tool in seeking to understand how social factors affect offspring survival, but I have also used the infrastructure of the long-term study to collect my own short-term, targeted data regarding maternal care and infant social development in early life. My goal is always to link my behavioral and life history results to a broader understanding of social evolution. To this end, I have also used theory and computer modelling, in parallel with empirical approaches, to make predictions about the evolution of various social behaviors.
The results of this dissertation can be distilled into four main conclusions. First, immature baboon survival is threatened by sexually selected feticide and infanticide by males. I document this behavior by relying on demographic data, rather than observing the killing of fetuses and infants directly—an example of the power of long-term demographic data to reveal otherwise hidden social phenomena. Second, sexually selected feticide and the Bruce effect (collectively dubbed “male-mediated prenatal loss”) may be more widespread across mammalian taxa and more influential in the evolution of mammalian social behavior than is sexually selected infanticide. Yet, these phenomena have not been as thoroughly studied as has infanticide because of the difficulty in documenting them.
Third, baboon mothers influence their offspring’s phenotype in numerous ways, including their offspring’s social development, survival, and ability to successfully rear their own future offspring. As a result, maternal death that occurs early in life has previously undocumented acute and chronic effects on offspring survival such that (i) offspring are more likely to die during the juvenile period if their mothers are going to die in the near future, and (ii) the effects of early maternal loss cascade from one generation to the next, resulting in an intergenerational effect of early maternal loss on offspring survival. These effects are not restricted to baboons, but are replicated in several other primate species. These links between maternal survival and offspring fitness outcomes have important implications for the evolution of slow primate life histories: in species where stronger links exist between maternal survival and offspring fitness, there may be increased selection for longevity at the expense of fertility, leading to the evolution of slower life histories in species with extended dependence between offspring and mother that lasts well beyond the age at weaning.
Finally, I show that the intergenerational effects of early-life adversity might be mitigated by social relationships between adult males and offspring born to compromised mothers. Offspring whose mothers experienced higher levels of early adversity spend time in close proximity to relatively many adult males in their earliest months of life, and males in turn allow infants increased independence and social exploration. Collectively, the contents of this dissertation bring us several steps closer to the goal of understanding the many social determinants that influence immature development, behavior, and survival in wild primates.
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