Elucidating the relationship between heterozygosity and fitness in a natural vertebrate population
Evolution, Anthropology
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 heterozygosity fitness correlations (HFCs) by analysing genetic samples from a long-term study of Antarctic fur seals (Arctocephlaus gazella) at Bird Island in the South Atlantic. The main aims were to evaluate how microsatellite heterozygosity influences the recruitment and breeding success of female fur seals, to evaluate whether HFCs are best explained by genome-wide (i.e. inbreeding depression) or more localised effects, and to investigate how immune genes contribute towards fitness variation. In order to address the first objective, we analysed three decades of data from 1,703 closely monitored females, of which 760 were genotyped at nine microsatellites. We found that climate change has steadily reduced prey availability, leading to a 24% decline in the number of breeding females since 1982 as well as a significant decline in pup birth mass. Concurrently, the average heterozygosity of the breeding female population increased by 17% over two decades, suggesting that the strength of selection against relatively homozygous individuals has increased over time. To investigate the role of inbreeding, we developed a high quality chromosome-level Antarctic fur seal reference genome and used restriction site associated DNA (RAD) and transcriptome sequencing to discover large numbers of neutral and candidate gene single nucleotide polymorphisms (SNPs) respectively. We then constructed and validated a high density SNP array carrying approximately 80,000 polymorphic SNPs for deployment in a subsequent funding phase. Finally, we used microsatellite and RAD data in combination with a panel of microsatellites developed from candidate genes to test for inbreeding as well as to evaluate the effects of inbreeding and immune gene variation on neonatal survival. We found that the magnitude of the variance in inbreeding within the study population was far higher than in other polygynous mammals including red deer and soay sheep. However, we were unable to detect any effects of either inbreeding or immune gene heterozygosity on neonatal survival. Taken together, our results suggest that HFCs in this species are probably due to inbreeding, although the fitness costs of inbreeding may not be manifest until pups become nutritionally independent. This project phase resulted in a total of sixteen publications, including papers in Nature, Proc Natl Acad Sci USA and Nature Communications, and laid a firm foundation for the continuation of this long-term study.
Publications
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(2014). Climate change selects for heterozygosity in a declining fur seal population. Nature, 511: 462–465
Forcada, J. & Hoffman, J.I.
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(2015). Chemical fingerprints encode mother-offspring similarity, colony membership, relatedness and genetic quality in fur seals. Proceedings of the National Academy of Sciences of the United States of America, 112: E5005–E5012
Stoffel, M., Caspers, B.A., Forcada, J., Giannakara, A., Baier, M.C., Eberhart-Phillips, L.J., Müller, C. & Hoffman, J.I.
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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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(2018). Demography and genetic diversity across pinnipeds are shaped by human exploitation, ecology and life-history. Nature Communications, 9: 4836
Stoffel, M.A., Humble, E., Paijmans, A.J., Acevedo-Whitehouse, K., Chilvers, B.L, Dickerson, B., Galimberti, F., Gemmell, N., Goldsworthy, S.D., Nichols, H.J., Krüger, O., Negro, S., Osborne, A. , Pastor, T., Robertson, B.C., Sanvito, S., Schultz, J., Shafer, A.B.A., Wolf, J.B.W. & Hoffman, J.I.
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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.
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(2019). Fur seal microbiota are shaped by the social and physical environment, show motheroffspring similarities and are associated with host genetic quality. Molecular Ecology, 28 (9): 2406–2422
Groβer, S., Sauer, J., Paijmans, A., Caspers, B.A., Forcada, J., Wolf, J.B.W. & Hoffman, J.I.
