Intergenerational effects of early adversity on survival in wild baboons

Early life adversity can affect an individual’s health, survival, and fertility for many years after the adverse experience. Whether early life adversity also imposes intergenerational effects on the exposed individual’s offspring is not well understood. We fill this gap by leveraging prospective, longitudinal data on a wild, long-lived primate. We find that juveniles whose mothers experienced early life adversity exhibit high mortality before age 4, independent of the juvenile’s own experience of early adversity. These juveniles often preceded their mothers in death by 1 to 2 years, indicating that high adversity females decline in their ability to raise offspring near the end of life. While we cannot exclude direct effects of a parent’s environment on offspring quality (e.g., inherited epigenetic changes), our results are completely consistent with a classic parental effect, in which the environment experienced by a parent affects its future phenotype and therefore its offspring’s phenotype.

data set. We asked whether the early adversity experienced by these females ("maternal early 81 adversity") predicted the survival of their juvenile offspring in the next generation, after 82 controlling for the early adversity directly experienced by the offspring themselves. 83 We considered five types of early adverse conditions (Table 1) (Table S1).

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We built a mixed effects Cox proportional hazards model of offspring survival during the 96 juvenile period that included early adversity measures present in the mother's and the offspring's 97 early life as binary fixed effects. We defined the juvenile period based on survival until age 4, 98 near the age of menarche for females and earliest dispersal for males in this population (52). We 99 included data on maternal early adversity for all five adverse early life conditions, and we 100 included data on offspring early adversity for four of the five conditions. We excluded the birth 101 of a close-in-age younger sibling for the offspring generation because the survival of the focal 102 offspring strongly affects the length of the subsequent birth interval (i.e., offspring that die shortly after birth also have the closest-in-age younger siblings). We included maternal and 48% higher probability of dying throughout the first four years of life than unaffected offspring, 127 and offspring whose mothers had a close-in-age sibling experienced a 39% higher probability of 128 dying than unaffected offspring. This effect is striking especially considering that a median of 129 7.0 and 8.0 years separated the offspring's own birth from the mother's experience of maternal 130 loss or birth of a close-in-age sibling, respectively. Notably, previous work in our population 131 found that these two sources of adversity-maternal loss and the presence of a close-in-age  than maternal loss in the mother's generation. In contrast, the effect of having a low-ranking 143 mother, which was associated with a 43% increase in offspring mortality risk, was comparable in 144 its effect size to the two significant predictors from the maternal generation (maternal loss and 145 close-in-age sibling for the mother, 48% and 39% increase in offspring mortality, respectively).

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Thus, two adverse conditions in a mother's early life had as large or larger of an impact on her 147 offspring's survival than all but one adverse condition experienced by the offspring directly.
survival of offspring to age four years (Table 2) could arise if offspring die after their mothers 150 die: even after weaning (approximately 1.5 years of age), juvenile baboons rely on their mothers 151 for social support and social learning (53). Alternatively, these offspring may die before their 152 mothers die if those mothers are themselves in poor condition. To distinguish these alternatives, 153 we modeled offspring survival to age 2 years (halfway through the juvenile period) as a function 154 of maternal death during years 2-4 after an offspring's birth (i.e., the two years that followed the 155 offspring survival period modeled in the response variable). In this analysis we considered only 156 the subset of offspring in our dataset whose mothers survived the entirety of the first two years of 157 the offspring's life, and for whom we were able to evaluate the four significant predictors of 158 offspring survival identified above and in Table 2 (N=671). Our results showed that offspring 159 were less likely to survive during the first two years of life if they were born to mothers who died 160 2-4 years after their birth. In other words, these offspring were more likely to die even when their 161 mother was still alive (hazard ratio=1.50 [1.01-2.23], p=0.045).

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To test whether this link between offspring survival and maternal viability was driven by 163 maternal early adversity, we next partitioned our analysis of offspring survival to age 2 based on 164 whether the mother experienced either maternal loss or a close-in-age younger sibling (i.e., either 165 or both of the two maternal early life conditions that significantly predicted their offspring's 166 survival; Table 2). We found that, among offspring whose mothers experienced either or both of offspring than other mothers, through differences in either maternal behavior or physiology (e.g. 180 reduced nutrient content in milk). Second, females who experienced early adversity might also 181 exhibit reduced egg and/or amniotic environmental quality (an established mechanism for 182 transmission of maternal effects (37, 54)). We were able to partially test the first hypothesis by 183 drawing on longitudinal behavioral data for this population. Specifically, we built linear mixed 184 effects models to test whether maternal early adversity affected the proportion of time during 10-185 minute focal follows that a mother spent either carrying or suckling her dependent infants. Fixed 186 effects in the model included maternal viability (a binary variable indicating whether the mother 187 survived for four years after offspring birth), the two early adverse circumstances experienced by 188 the mother that affected offspring survival (the mother's maternal loss and close-in-age sibling), 189 offspring age (both as a linear and as a quadratic term), maternal rank, maternal age, the number 190 of adult females in the social group, and season. We also included maternal ID, offspring ID, 191 group ID, and observer ID as random effects. buffered against the effects of maternal loss, those offspring that experienced maternal loss and 238 whose mothers had also experienced maternal loss were more likely, not less likely, to die, as 239 compared to offspring that experienced maternal loss but whose mothers did not. Thus, offspring experience constraints not only as a result of their own early environment, but also as a result of 241 their mother's developmental history, including events that occurred years before the offspring's lives compared to females that did not experience adversity (18). In addition to the five sources of early adversity discussed above, this previous analysis also considered early social 287 connectedness (social integration versus social isolation) as a sixth source of adversity (18).

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Social connectedness data are missing for some mothers who were born relatively early in the 289 long-term study. To maximize our sample size, we therefore did not include measures of social  Table S7.  Table S8 308 for model syntax).    The focal individual was born to a mother with a low social rank (mother's rank fell in the bottom quartile of the group's dominance hierarchy).
0.17 0.23 Close-In-Age Younger Sibling The focal individual had a younger sibling born to its mother within 18 months of the focal's birth. outranks. An animal therefore has a low maternal rank if her mother's rank is <0.25. The reduced 6 frequency with which low maternal rank appears in the maternal generation is a likely a result of 7 offspring of low-ranking mothers surviving less well (84), and therefore not surviving to appear 8 as mothers in our dataset.

0.002
Offspring survive less well if they were born to a low-ranking mother. a An alternative model that considered cumulative maternal adversity was not a better or worse fit 3 than the reduced multivariate maternal adversity model (see Table S7. For both the model 4 presented here and that in Table S7, R 2 =0.07, log likelihood = -1598).