A chromosomal inversion contributes to divergence in multiple traits between deer mouse ecotypes

How locally adapted ecotypes are established and maintained within a species is a long-standing question in evolutionary biology. Using forest and prairie ecotypes of deer mice ( ), we characterized the genetic basis of variation in two defining traits-tail length and coat color-and discovered a 41-...

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Published inScience (American Association for the Advancement of Science) Vol. 377; no. 6604; pp. 399 - 405
Main Authors Hager, Emily R, Harringmeyer, Olivia S, Wooldridge, T Brock, Theingi, Shunn, Gable, Jacob T, McFadden, Sade, Neugeboren, Beverly, Turner, Kyle M, Jensen, Jeffrey D, Hoekstra, Hopi E
Format Journal Article
LanguageEnglish
Published United States The American Association for the Advancement of Science 22.07.2022
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Summary:How locally adapted ecotypes are established and maintained within a species is a long-standing question in evolutionary biology. Using forest and prairie ecotypes of deer mice ( ), we characterized the genetic basis of variation in two defining traits-tail length and coat color-and discovered a 41-megabase chromosomal inversion linked to both. The inversion frequency is 90% in the dark, long-tailed forest ecotype; decreases across a habitat transition; and is absent from the light, short-tailed prairie ecotype. We implicate divergent selection in maintaining the inversion at frequencies observed in the wild, despite high levels of gene flow, and explore fitness benefits that arise from suppressed recombination within the inversion. We uncover a key role for a large, previously uncharacterized inversion in the evolution and maintenance of classic mammalian ecotypes.
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These authors contributed equally to this work.
Author contributions: E.R.H. and H.E.H. initially conceived of the project. E.R.H., J.T.G., and K.M.T. planned and conducted the field collections. E.R.H. conducted the QTL mapping experiment and analyzed the forest-prairie phenotypes; E.R.H. and K.M.T. generated genetic data for the cross; and E.R.H., J.T.G., S.T., S.M., B.N., and K.M.T. generated wild and laboratory phenotype data. O.S.H. analyzed genetic data for the F2 cross, E.R.H. and O.S.H. performed QTL mapping analyses, T.B.W. analyzed long-read sequence data, O.S.H. and T.B.W. analyzed wild-caught forest-prairie genetic data, O.S.H. analyzed transect genetic data, and E.R.H. and O.S.H. performed cline analyses. T.B.W. performed demographic simulation, model-fitting, and inference, and O.S.H. performed selection simulations, model-fitting, and inference, both with input from J.D.J. E.R.H., O.S.H., T.B.W., J.D.J., and H.E.H. wrote the manuscript, with input from all authors.
Present address: Department of Biomedical Engineering, Boston University, Boston, MA 02215, USA.
Present address: Centre for Teaching Support & Innovation, University of Toronto, Toronto, ON M5S 3H1, Canada.
ISSN:0036-8075
1095-9203
1095-9203
DOI:10.1126/science.abg0718