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

Abstract

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