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Genetic association with boldness and maternal performance in a free-ranging population of grey seals (Halichoerus grypus)

Abstract

Individual variation in quantitative traits clearly influence many ecological and evolutionary processes. Moderate to high heritability estimates of personality and life-history traits suggest some level of genetic control over these traits. Yet, we know very little of the underlying genetic architecture of phenotypic variation in the wild. In this study, we used a candidate gene approach to investigate the association of genetic variants with repeated measures of boldness and maternal performance traits (weaning mass and lactation duration) collected over an 11- and 28-year period, respectively, in a free-ranging population of grey seals on Sable Island National Park Reserve, Canada. We isolated and re-sequenced five genes: dopamine receptor D4 (DRD4), serotonin transporter (SERT), oxytocin receptor (OXTR), and melanocortin receptors 1 (MC1R) and 5 (MC5R). We discovered single nucleotide polymorphisms (SNPs) in each gene; and, after accounting for loci in linkage disequilibrium and filtering due to missing data, we were able to test for genotype-phenotype relationships at seven loci in three genes (DRD4, SERT, and MC1R). We tested for association between these loci and traits of 180 females having extreme shy-bold phenotypes using mixed-effects models. One locus within SERT was significantly associated with boldness (effect size = 0.189) and a second locus within DRD4 with weaning mass (effect size = 0.232). Altogether, genotypes explained 6.52–13.66% of total trait variation. Our study substantiates SERT and DRD4 as important determinants of behaviour, and provides unique insight into the molecular mechanisms underlying maternal performance variation in a marine predator.

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Fig. 1: Map showing the location of Sable Island National Park Reserve of Nova Scotia, Canada.
Fig. 2: Schematics of gene structure for five candidate genes.
Fig. 3: Boldness of female grey seals and the additive allele effect of the serotonin transporter (SERT) gene.
Fig. 4: Relationship between the additive allele effect and grey seal maternal performance at loci of two candidate genes [serotonin transporter (SERT) and dopamine receptor D4 (DRD4)].
Fig. 5: Forest plots of effect size estimates (±95% confidence intervals) for the association of seven loci across three candidate genes with boldness, pup weaning mass, and lactation duration in female grey seals of Sable Island, Nova Scotia (Canada).

Data availability

The genotype and phenotype information used for this study is available on the University of Alberta Dataverse repository (https://doi.org/10.7939/DVN/OPAOMU). Sequence data have been submitted to GenBank (accession numbers MW864572-MW864597).

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Acknowledgements

We thank Anh Dao, Rhiannon Peery, and Amy Johnson for assistance with laboratory protocol, primer, and figure design. We are grateful to the many individuals that helped collect the genetic and life history data from grey seals at Sable Island, but particular thanks go to Shelley Lang and Damian Lidgard for their long-term participation in the research. CMB was partially funded by scholarships from Alberta Innovates Technology Futures (AITF) and through the University of Alberta. This work was supported by NSERC Discovery Grants (DWC: RGPIN-2018-04354; WDB: RGPIN-2018-05403) and long-term funding provided by the Department of Fisheries and Oceans, Canada to WDB and CED.

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Bubac, C.M., Cullingham, C.I., Fox, J.A. et al. Genetic association with boldness and maternal performance in a free-ranging population of grey seals (Halichoerus grypus). Heredity (2021). https://doi.org/10.1038/s41437-021-00439-4

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