Biology subjects

Alberts, S. C.

Publications and source records attributed to Alberts, S. C..

31 records · Page 2Linked to original sources

bioRxiv2022

Early life adversity and adult social relationships have independent effects on survival in a wild animal model of aging

Does social isolation in adulthood predict survival because socially isolated individuals are already unhealthy due to adversity earlier in life (health selection)? Or do adult social environments directly cause poor health and increased mortality risk ("social causation")? These alternative hypotheses are difficult to disentangle in humans because prospective data on survival and the environment for both early life and adulthood are rarely available. Using data from the baboon population of Amboseli, Kenya, a model for human behavior and aging, we show that early adversity and adult social isolation contribute independently to reduced adult survival, in support of both health selection and social causation. Further, strong social bonds and high social status can buffer some negative effects of early adversity on survival. These results support a growing change in perspective, away from "either-or" hypotheses and towards a multi-causal perspective that points to multiple opportunities to mitigate the effects of social adversity. TeaserEarly life environments and adult social bonds have strong, but largely independent effects on survival in wild baboons.

animal behavior and cognition↗

bioRxiv2022

Ecology and age, but not genetic ancestry, predict fetal loss in a wild baboon hybrid zone

ObjectivesPregnancy failure and fetal loss represent a major fitness cost for any mammal, particularly those with slow life histories such as primates. Here, we quantified the risk of fetal loss in wild hybrid baboons, including genetic, ecological, and demographic sources of variance. We were particularly interested in testing the hypothesis that hybridization imposes a cost by increasing fetal loss rates. Such an effect would help explain how baboons maintain taxonomic integrity despite interspecific gene flow. Materials and MethodsWe analyzed pregnancy outcomes for 1,020 pregnancies observed over 46 years in a natural yellow baboon-anubis baboon hybrid zone. Fetal losses and live births were scored based on near-daily records of female reproductive state and the appearance of live neonates. We modeled the probability of fetal loss as a function of a females genetic ancestry (based on whole-genome resequencing data), age, number of previous fetal losses, dominance rank, group size, climate, and habitat quality using binomial mixed effects models. ResultsFemale genetic ancestry did not predict the likelihood of fetal loss. Instead, the risk of fetal loss is elevated for very young and very old females. Fetal loss is most robustly predicted by ecological factors, including poor habitat quality and extreme heat during pregnancy. DiscussionOur results suggest that gene flow between yellow baboons and anubis baboons is not impeded by an increased risk of fetal loss for hybrid females. Instead, ecological conditions and female age are key determinants of this component of female reproductive success. Research HighlightsO_LIFemale baboons do not experience fetal loss as a cost of hybridization. C_LIO_LIHeat stress, poor habitat quality, and young and old age elevate the risk of fetal loss, emphasizing roles for ecology and life history in determining birth outcomes. C_LI Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=124 SRC="FIGDIR/small/505836v1_ufig1.gif" ALT="Figure 1"> View larger version (23K): org.highwire.dtl.DTLVardef@74dd64org.highwire.dtl.DTLVardef@7301b5org.highwire.dtl.DTLVardef@751e9dorg.highwire.dtl.DTLVardef@12ce924_HPS_FORMAT_FIGEXP M_FIG Neonate drawings by Emily Nonnamaker. C_FIG

evolutionary biology↗

bioRxiv2022

Genetic variance and indirect genetic effects for affiliative social behavior in a wild primate

Affiliative social behaviors are linked to fitness components in multiple species. However, the role of genetic variance in shaping affiliative social behaviors remains largely unknown, limiting our understanding of how these behaviors can respond to natural selection. Here, we employed the animal model to estimate both environmental and genetic sources of variance and covariance in grooming behavior in the well-studied Amboseli baboon population in Kenya. We found that grooming given, grooming received, and total grooming all are similarly heritable (h2=0.22, h2=0.16, and h2=0.26 respectively), and that rank and the presence of kin contribute to environmental variance. We detected small but measurable indirect genetic effects of partner identity on the amount of grooming given within dyadic grooming partnerships. The genetic correlation between grooming given and grooming received was exceptionally strong and positive (R=0.94 {+/-} 0.12), and the indirect and direct genetic effects for grooming given were also strongly positively correlated (R=0.86 {+/-} 0.06). Our results provide insight into the evolvability of affiliative behavior in wild animals, including the possibility for correlations between direct and indirect genetic effects to accelerate the response to selection. As such they provide novel information about the genetic architecture of social behavior in nature, with important implications for the evolution of cooperation and reciprocity.

evolutionary biology↗

bioRxiv2022

Five decades of data yield no support for adaptive biasing of offspring sex ratio in wild baboons (Papio cynocephalus)

Over the past 50 years, a wealth of testable, often conflicting, hypotheses have been generated about the evolution of offspring sex ratio manipulation by mothers. Several of these hypotheses have received support in studies of invertebrates and some vertebrate taxa. However, their success in explaining sex ratios in mammalian taxa, and especially in primates, has been mixed. Here, we assess the predictions of four different hypotheses about the evolution of biased offspring sex ratios in the well-studied baboons of the Amboseli basin in Kenya: the Trivers-Willard, female rank enhancement, local resource competition, and local resource enhancement hypotheses. Using the largest sample size ever analyzed in a primate population (n = 1372 offspring), we test the predictions of each hypothesis. Overall, we find no support for adaptive biasing of sex ratios. Offspring sex is not consistently related to maternal dominance rank or biased towards the dispersing sex, nor it is predicted by group size, population growth rates, or their interaction with maternal rank. Because our sample size confers power to detect even subtle biases in sex ratio, including modulation by environmental heterogeneity, these results suggest that adaptive biasing of offspring sex does not occur in this population.

evolutionary biology↗

bioRxiv2022

Universal gut microbial relationships in the gut microbiome of wild baboons

Ecological relationships between bacteria mediate the services that gut microbiomes provide to their hosts. Knowing the overall direction and strength of these relationships within hosts, and their generalizability across hosts, is essential to learn how microbial ecology scales up to affect microbiome assembly, dynamics, and host health. Here we gain insight into these patterns by inferring thousands of correlations in bacterial abundance between pairs of gut microbiome taxa from extensive time series data (5,534 microbiome profiles from 56 wild baboon hosts over a 13-year period). We model these time series using a statistically robust, multinomial logistic-normal modeling framework and test the degree to which bacterial abundance correlations are consistent across hosts (i.e., "universal") or individualized to each host. We also compare these patterns to two publicly available human data sets. We find that baboon gut microbial relationships are largely universal: correlation patterns within each baboon host reflect a mixture of idiosyncratic and shared patterns, but the shared pattern dominates by almost 2-fold. Surprisingly, the strongest and most consistently correlated bacterial pairs across hosts were overwhelmingly positively correlated and typically belonged to the same family--a 3-fold enrichment compared to pairs drawn from the data set as a whole. The bias towards universal, positive bacterial correlations was also apparent in monthly samples from human infants, and bacterial families that had universal relationships in baboons also tended to be universal in human infants. Together, our results advance our understanding of the relationships that shape gut microbial ecosystems, with implications for microbiome personalization, community assembly and stability, and the feasibility of microbiome interventions to improve host health.

ecology↗

bioRxiv2022

Seeing the future: a better way to model and test for adaptive developmental plasticity

In many species, individuals who experience harsh conditions during development often have poor health and fitness outcomes in adulthood relative to peers who do not. There are two classes of evolutionary hypotheses for the origins of these early life contributors to inequality in adulthood: developmental constraints (DC) models, which focus on the deleterious effects of low-quality early-life environments, and predictive adaptive response (PAR) hypotheses, which emphasize the cost of mismatches between early and adult environments. Distinguishing DC and PAR models empirically is difficult for both conceptual and analytical reasons. Here, we resolve this difficulty by providing explicit mathematical definitions for DC, PARs, and related concepts, and propose a novel, quadratic regression-based statistical test derived from these definitions. Simulations show that this approach improves the ability to discriminate between DC and PAR hypotheses relative to a common alternative based on testing for interaction effects between developmental and adult environments. Simulated data indicate that the interaction effects approach often conflates PARs with DC, while the quadratic regression approach yields high sensitivity and specificity for detecting PARs. Our results highlight the value of linking verbal and visual models to a formal mathematical treatment for understanding the developmental origins of inequitable adult outcomes.

evolutionary biology↗

bioRxiv2021

Synchrony and idiosyncrasy in the gut microbiome of wild primates

Human gut microbial dynamics are highly individualized, making it challenging to link microbiota to health and to design universal microbiome therapies. This individuality is typically attributed to variation in host genetics, diets, environments, and medications, but it could also emerge from fundamental ecological forces that shape microbiota more generally. Here we leverage extensive gut microbial time series from wild baboons--hosts who experience little interindividual dietary and environmental heterogeneity--to test whether gut microbial dynamics are synchronized across hosts or largely idiosyncratic. Despite their shared lifestyles, baboon microbiome dynamics were only weakly synchronized. The strongest synchrony occurred among baboons living in the same social group, likely because group members range over the same habitat and simultaneously encounter the same sources of food and water. However, this synchrony was modest compared to each hosts personalized dynamics. Indeed, host-specific factors, especially host identity, explained 10 times the deviance in longitudinal microbial dynamics, compared to factors shared across hosts. These results contribute to mounting evidence that highly idiosyncratic gut microbiomes are not an artifact of modern human environments, and that synchronizing forces in the gut microbiome (e.g., shared environments, diets, and microbial dispersal) are often not strong enough to overwhelm drivers of microbiome personalization, including host genetics, priority effects, horizontal gene transfer, and functional redundancy.

ecology↗

bioRxiv2021

Selection against admixture and gene regulatory divergence in a long-term primate field study

Admixture has profoundly influenced evolution across the tree of life, including in humans and other primates1,2. However, we have limited insight into the genetic and phenotypic consequences of admixture in primates, especially during its key early stages. Here, we address this gap by combining 50 years of field observations with population and functional genomic data from yellow (Papio cynocephalus) and anubis (P. anubis) baboons in Kenya, in a longitudinally studied population that has experienced both historical and recent admixture3. We use whole-genome sequencing to characterize the extent of the hybrid zone, estimate local ancestry for 442 known individuals, and predict the landscape of introgression across the genome. Despite no major fitness costs to hybrids, we identify signatures of selection against introgression that are strikingly similar to those described for archaic hominins4-6. These signatures are strongest near loci with large ancestry effects on gene expression, supporting the importance of gene regulation in primate evolution and the idea that selection targeted large regulatory effects following archaic hominin admixture7,8. Our results show that genomic data and field observations of hybrids are important and mutually informative. They therefore demonstrate the value of other primates as living models for phenomena that we cannot observe in our own lineage.

evolutionary biology↗

bioRxiv2021

Distinct gene regulatory signatures of dominance rank and social bond strength in wild baboons

The social environment is a major determinant of morbidity, mortality, and Darwinian fitness in social animals. Recent studies have begun to uncover the molecular processes associated with these relationships, but the degree to which they vary across different dimensions of the social environment remains unclear. Here, we draw on a long-term field study of wild baboons to compare the signatures of affiliative and competitive aspects of the social environment in white blood cell gene regulation, under both immune stimulated and non-stimulated conditions. We find that the effects of dominance rank on gene expression are directionally opposite in males versus females, such that high-ranking males resemble low-ranking females, and vice-versa. Among females, rank and social bond strength are both reflected in the activity of cellular metabolism and proliferation genes. However, pronounced rank-related differences in baseline immune gene activity are near-absent for social bond strength, while only bond strength predicts the fold-change response to immune (lipopolysaccharide) stimulation. Together, our results indicate that the directionality and magnitude of social effects on gene regulation depend on the aspect of the social environment under study. This heterogeneity may help explain why social environmental effects on health and longevity can also vary between measures.

genomics↗

bioRxiv2020

Genetic ancestry predicts male-female affiliation in a natural baboon hybrid zone

Opposite-sex social relationships are important predictors of fitness in many animals, including several group-living mammals. Consequently, understanding sources of variance in the tendency to form opposite-sex relationships is important for understanding social evolution. Genetic contributions are of particular interest due to their importance in long-term evolutionary change, but little is known about genetic effects on male-female relationships in social mammals, especially outside of the mating context. Here, we investigate the effects of genetic ancestry on male-female affiliative behavior in a hybrid zone between the yellow baboon (Papio cynocephalus) and the anubis baboon (P. anubis), in a population in which male-female social bonds are known predictors of lifespan. We place our analysis within the context of other social and demographic predictors of affiliative behavior in baboons. Genetic ancestry was the most consistent predictor of opposite-sex affiliative behavior we observed, with the exception of strong effects of dominance rank. Our results show that increased anubis genetic ancestry is associated with subtly, but significantly higher rates of opposite-sex affiliative behavior, in both males and females. Additionally, pairs of anubis-like males and anubis-like females were the most likely to socially affiliate, resulting in moderate assortativity in grooming and proximity behavior as a function of genetic ancestry. Our findings indicate that opposite-sex affiliative behavior partially diverged during baboon evolution to differentiate yellow and anubis baboons, despite overall similarities in their social structures and mating systems. Further, they suggest that affiliative behavior may simultaneously promote and constrain baboon admixture, through additive and assortative effects of ancestry, respectively. HIGHLIGHTSO_LIOpposite-sex social relationships can have important fitness consequences. C_LIO_LIIn hybrid baboons, genetic ancestry predicted male-female affiliative behavior. C_LIO_LIBoth an individuals genetic ancestry and that of its social partner mattered. C_LIO_LIMale-female affiliation was assortative with respect to genetic ancestry. C_LIO_LIDominance rank and group demography also influenced male-female social affiliation. C_LI

evolutionary biology↗

bioRxiv2020

Beyond orphaned infants: novel effects of maternal death in wild primates

Primate offspring often depend on their mothers well beyond the age of weaning, and offspring that experience maternal death in early life can suffer substantial reductions in fitness across the lifespan. Here we leverage data from eight wild primate populations (seven species) to examine two underappreciated pathways linking early maternal death and offspring fitness that are distinct from direct effects of orphaning on offspring survival. First, we show that, for five of the seven species, offspring face reduced survival during the years immediately preceding maternal death, while the mother is still alive. Second, we identify an intergenerational effect of early maternal loss in three species (muriquis, baboons, and blue monkeys), such that early maternal death experienced in one generation leads to reduced offspring survival in the next. Our results have important implications for the evolution of slow life histories in primates, as they suggest that maternal condition and survival are more important for offspring fitness than previously realized.

evolutionary biology↗

bioRxiv2020

Comparing proportional and ordinal dominance ranks reveals multiple competitive landscapes in an animal society

Across group-living animals, linear dominance hierarchies lead to disparities in access to resources, health outcomes, and reproductive performance. Studies of how dominance rank affects these outcomes typically employ one of several dominance rank metrics without examining the assumptions each metric makes about its underlying competitive processes. Here we compare the ability of two dominance rank metrics--ordinal rank and proportional or standardized rank--to predict 20 distinct traits in a well-studied wild baboon population in Amboseli, Kenya. We propose that ordinal rank best predicts outcomes when competition is density-dependent, while proportional rank best predicts outcomes when competition is density-independent. We found that for 75% (15/20) of the traits, one of the two rank metrics performed better than the other. Strikingly, all male traits were better predicted by ordinal than by proportional rank, while female traits were evenly split between being better predicted by proportional or ordinal rank. Hence, male and female traits are shaped by different competitive regimes: males competitive environments are largely driven by density-dependent resource access (e.g., access to estrus females), while females competitive environments are shaped by both density-independent resource access (e.g. distributed food resources) and density-dependent resource access. However, traits related to competition for social and mating partners are an exception to this sex-biased pattern: these traits were better predicted by ordinal rank than by proportional rank for both sexes. We argue that this method of comparing how different rank metrics predict traits of interest can be used as a way to distinguish between different competitive processes operating in animal societies.

animal behavior and cognition↗

bioRxiv2019

Intergenerational effects of early adversity on survival in wild baboons

In humans and nonhuman animals, early life adversity can affect an individuals health, survival, and fertility for many years after the adverse experience. However, whether early life adversity also imposes intergenerational effects on the exposed individuals offspring is not well understood. Here, 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, and this effect is independent of the juveniles own experience of early adversity. Furthermore, our results point towards a strong role for classic parental effects in driving these effects: mothers that experienced early life adversity displayed reduced viability in adulthood, which in turn led to reductions in offspring survival. Importantly, these mothers juvenile offspring often preceded them in death by 1 to 2 years, indicating that, for high adversity mothers, the quality of maternal care declines near the end of life. While we cannot exclude direct effects of a parents environment on offspring quality (e.g., transgenerational epigenetic changes), our results are most consistent with a classic parental effect, in which the environment experienced by a parent affects its future phenotype and therefore its offsprings phenotype. Together, our findings demonstrate that adversity experienced by individuals in one generation can have strong effects on the survival of offspring in the next generation, even if those offspring did not themselves experience early adversity.

zoology↗