Genomics of incipient speciation in a highly vagile marine mammal: genome-wide analysis of demographic history, population structure and local adaptation in the endangered Galápagos sea lion
Evolutionary Cell and Developmental Biology (Zoology)
Ecology and Biodiversity of Animals and Ecosystems, Organismic Interactions
Final Report Abstract
This project set out to explore the genomic basis of genetic differentiation in an endangered marine mammal, the Galápagos sea lion (GSL) using whole genome resequencing data from 80 individuals sampled across the Galápagos archipelago. We accomplished most of our proposed objectives while also embracing new goals that arose during the course of the project. First, we assembled a fur seal reference genome, which was initially proposed to serve as backbone for all of the population genetic analyses in the GSL. However, during the course of the project, the opportunity arose to generate an assembly for the more closely related Californian sea lion (CSL), which greatly facilitated unbiased estimation of population genomic parameters. We also resequenced a total of 95 GSL genomes, while additional funding from the Swedish Research Council enabled us to resequence a further 25 CSL genomes. This added an additional axis to the project by allowing us to consider not only population structure and dynamics within the Galápagos Archipelago, but also to investigate the history of speciation and colonization from a common ancestor shared with the CSL. Population genetic analyses based on 2,828,795 SNPs clearly demonstrated the evolutionary independence of the CSL and GSL by revealing clear evidence for a lack of recent gene flow. This finding highlights the status of the GSL as an endemic species worthy of specific conservation efforts. Within the GSL, populations separated along an ecological contrast between the east and west, with additional population structure at the rim of the species range. Considering that GSL individuals are capable of swimming across the entire archipelago within a matter of days, this sympatric differentiation is remarkable. Comparison of whole mitochondrial genomes and genome-wide nuclear markers also suggested that female philopatry contributes substantially towards restricted gene flow. To explore sex-biased patterns of gene flow in greater detail, we are now developing a panel of Y-chromosomal markers to explicitly quantify male-mediated gene flow using a larger sample of individuals and populations. Contrary to our initial expectations, genome scans among GSL populations did not provide any evidence of genomic regions associated with adaptation to different habitats, suggestive either of phenotypic plasticity or of a highly polygenic genetic architecture. As expected from a source population, the CSL harboured greater genetic diversity than the GSL, which showed signatures of a recent bottleneck followed by population expansion. In ongoing work, we will (i) scrutinize population specific signatures of selection using an improved annotation that is currently being generated for the CSL reference genome; and (ii) trace the demographic consequences of the colonization history of the GSL in greater detail using demographic modelling approaches.
Publications
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(2016). A draft fur seal genome provides insights into factors affecting SNP validation and how to mitigate them. Molecular Ecology Resources, 16: 909–921
Humble, E., Martinez-Barrio, A., Forcada, J., Trathan, P.N., Thorne, M.A.S., Wolf, J.B.W. & Hoffman, J.I.
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(2016). Making sense of genomic islands of differentiation in light of speciation. Nature Reviews Genetics, 18: 87-100
Wolf, J.B.W. & Ellegren, H.
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(2018). RAD sequencing and a hybrid Antarctic fur seal genome assembly reveal rapidly decaying linkage disequilibrium, global population structure and evidence for inbreeding. G3: Genes | Genomes | Genetics, 8: 2709–2722
Humble, E., Dasmahapatra, K.K., Martinez-Barrio, A., Gregorio, I., Forcada, J., Polikeit, A.-C., Goldsworthy, S.D., Goebel, M.E., Kalinowski, J., Wolf, J.B.W. & Hoffman, J.I.