Conservation genomic analysis reveals ancient introgression and declining levels of genetic diversity in Madagascar’s hibernating dwarf lemurs

Abstract

Madagascar's biodiversity is notoriously threatened by deforestation and climate change. Many of these organisms are rare, cryptic, and severely threatened, making population-level sampling unrealistic. Such is the case with Madagascar's dwarf lemurs (genus Cheirogaleus), the only obligate hibernating primate. We here apply comparative genomic approaches to generate the first genome-wide estimates of genetic diversity within dwarf lemurs. We generate a reference genome for the fat-tailed dwarf lemur, Cheirogaleus medius, and use this resource to facilitate analyses of high-coverage (~30x) genome sequences for wild-caught individuals representing species: C. sp. cf. medius, C. major, C. crossleyi and C. sibreei. This study represents the largest contribution to date of novel genomic resources for Madagascar's lemurs. We find concordant phylogenetic relationships among the four lineages of Cheirogaleus across most of the genome, and yet detect a number of discordant genomic regions consistent with ancient admixture. We hypothesized that these regions could have resulted from adaptive introgression related to hibernation, indeed finding that genes associated with hibernation are present, though most significantly, that gene ontology categories relating to transcription are over-represented. We estimate levels of heterozygosity and find particularly low levels in an individual sampled from an isolated population of C. medius that we refer to as C. sp. cf. medius. Results are consistent with a recent decline in effective population size, which is evident across species. Our study highlights the power of comparative genomic analysis for identifying species and populations of conservation concern, as well as for illuminating possible mechanisms of adaptive phenotypic evolution.

Admixture in Mammals and How to Understand Its Functional Implications

“…In lemurs, there are a few examples for recent and past hybridization: Sportive lemurs have a reticulate evolution, and several species of lemurs have known hybrid zones (Table S1, Supporting Information), for example, leading to asymmetric introgression in mouse lemurs due to male‐biased dispersal . Ancient introgression has been inferred from high‐coverage genomes of dwarf lemurs . Finally, there is evidence of asymmetric introgression between Sulawesi tarsiers …”

“…In wild mammalian species, adaptive introgression has been observed as well. The winter coat in some populations of snowshoe hares is brown instead of white due to introgression from jackrabbits; in Jaguar, genes putatively involved in optic nerve development introgressed from lion; introgressed fragments from cave bears in brown bears may have been under selection; and gene flow may have spread genes related to hibernation across different dwarf lemur species …”

Limits and Convergence properties of the Sequentially Markovian Coalescent

“…Linking demographic history to climate and environmental data greatly supports the field of conservation genetics (Ekblom et al, 2018;Hendricks et al, 2018;Oh et al, 2019). Indeed, using such approaches can help ecologists in detecting effective population size decrease (Williams et al, 2020), and thus serve as a guide in maintaining or avoiding the erosion of genetic diversity in endangered populations, and potentially predicting the consequences of climate change on genetic diversity (S Li et al, 2014). In addition, studying the demographic histories of different species in relation to one another can unveil latent biological or environmental evolutionary forces (Hecht et al, 2018), unveiling links and changes within entire ecosystems.…”

Elaborate expansion of syntenic V1R hotspots correlates with high species diversity in nocturnal mouse and dwarf lemurs

“…Williams et al 2019). We evaluated assembly completeness using the Benchmarking Universal 154Single-Copy Orthologs tool, BUSCO(Simão et al 2015), which assesses genomes for the 155 presence of complete near-universal single-copy orthologs (SupplementaryFigure S1).…”