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Linking genetic, morphological, and behavioural divergence between inland island and mainland deer mice

Abstract

The island syndrome hypothesis (ISH) stipulates that, as a result of local selection pressures and restricted gene flow, individuals from island populations should differ from individuals within mainland populations. Specifically, island populations are predicted to contain individuals that are larger, less aggressive, more sociable, and that invest more in their offspring. To date, tests of the ISH have mainly compared oceanic islands to continental sites, and rarely smaller spatial scales such as inland watersheds. Here, using a novel set of genome-wide SNP markers in wild deer mice (Peromyscus maniculatus) we conducted a genomic assessment of predictions underlying the ISH in an inland riverine island system: analysing island-mainland population structure, and quantifying heritability of phenotypes thought to underlie the ISH. We found clear genomic differentiation between the island and mainland populations and moderate to high marker-based heritability estimates for overall variation in traits previously found to differ in line with the ISH between mainland and island locations. FST outlier analyses highlighted 12 loci associated with differentiation between mainland and island populations. Together these results suggest that the island populations examined are on independent evolutionary trajectories, the traits considered have a genetic basis (rather than phenotypic variation being solely due to phenotypic plasticity). Coupled with the previous results showing significant phenotypic differentiation between the island and mainland groups in this system, this study suggests that the ISH can hold even on a small spatial scale.

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Fig. 1: Map of the Mikaki study area.
Fig. 2: Genetic structure of 294 deer mice from the Minaki study system.
Fig. 3: Ancestry bar plot from lea (Frichot and François 2015) for K = 2–7.

Data availability

DNA sequencing reads are deposited on the short-read archive (SRA) BioProject ID: PRJNA759202. SNP genotypes along with phenotypic measurements have been deposited in Dryad (https://doi.org/10.5061/dryad.7m0cfxpw3).

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Acknowledgements

We are grateful to Kathy and Barry Hall for the logistical help in the field, and to David Hewlett and Susan Morrow, the MacKays, the Chalkes, the Burrows, the Corbys, and Mark Engebretson, for letting us work on their properties. Jim Hare generously saved us during the first year by giving us 95% alcohol for our sampling. Many thanks to Carolyn Hall, Jean-Patrick Bourbonnière, Emily Brown, Suzie Dubuc, Philippe Heine, Dawson Ogilvie, Catherine Pelletier, Shu-Ting Zhao, Rebecca Pedneault for their help in the field during the four years of the study. We are also thankful to Brian Boyle and his team at IBIS (U. Laval) for library preparation and sequencing. This research was funded by a Fonds de Recherche du Québec - Nature et Technologies (FRQNT) team grant to D. Réale, D. Garant, and L. Bernatchez, and by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grant to D. Réale. We would also like to acknowledge the reviewers and Associate Editor for providing detailed and useful comments on previous drafts of this work.

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JMM conducted genomic analyses and drafted the initial manuscript. The original project was conceived by DR along with DG and LB. Fieldwork was conducted by TJ and JWJ along with DR. Lab work and bioinformatic processing was conducted by EN. All authors contributed to and commented on the manuscript while it was being drafted.

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Correspondence to Joshua M. Miller.

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Miller, J.M., Garant, D., Perrier, C. et al. Linking genetic, morphological, and behavioural divergence between inland island and mainland deer mice. Heredity 128, 97–106 (2022). https://doi.org/10.1038/s41437-021-00492-z

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