Biology subjects

Fogel, A. S.

Publications and source records attributed to Fogel, A. S..

6 recordsLinked to original sources

bioRxiv2025

Admixture influences the genetic architecture of DNA methylation in a wild primate hybrid zone

BackgroundHybrid zones play a central role in evolutionary biology because they serve as natural laboratories for studying how traits and taxa diverge. Changes in gene regulation make important contributions to this process. However, the degree to which admixture shapes gene regulatory variation in hybrid populations remains poorly understood. Here, we combine genome-wide resequencing and DNA methylation data from 295 hybrid baboons--members of a single, intensively studied natural population--to investigate how admixture affects the genetic architecture of this important epigenetic mark. ResultsWe find that local genetic ancestry frequently predicts DNA methylation levels and recapitulates differences between the parent species. By performing methylation quantitative trait locus (meQTL) mapping, we show that these differences predominantly arise due to evolved differences in allele frequencies. Thus, admixture in the hybrid population increases variance in DNA methylation, including by introducing meQTL that would otherwise be invariant. Finally, we integrate massively parallel reporter assay data to show that admixture-derived variation in DNA methylation alters enhancer activity and gene expression. ConclusionsTogether, these results demonstrate how admixture can meaningfully alter the genetic architecture of gene regulatory traits in natural hybrid zones. They also suggest that the genetic architecture of DNA methylation is conserved across closely related primates, suggesting that genetic effects on gene regulation may remain stable over timescales that range into the millions of years.

evolutionary biology↗

bioRxiv2022

Heritable and sex-specific variation in the development of social behavior in a wild primate

Affiliative social bonds are linked to fitness components in many social mammals. However, despite their importance, little is known about how the tendency to form social bonds develops in young animals, or if the development of social behavior is heritable and thus can evolve. Using four decades of longitudinal observational data from a wild baboon population, we assessed the environmental determinants of an important social developmental milestone in baboons--the age at which a young animal first grooms a conspecific--and we assessed how mother-offspring grooming reciprocity develops during the juvenile period. We found that grooming development differs between the sexes: female infants groom at an earlier age and reach reciprocity in grooming with their mother earlier than males. Using the quantitative genetic animal model, we also found that age at first grooming behavior for both sexes is weakly heritable (h2 = 4.3%). These results show that sex differences in grooming emerge at a young age; that strong, reciprocal social relationships between mothers and daughters begin very early in life; and that age at first grooming is heritable and therefore can be shaped by natural selection.

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↗

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↗

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

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↗