[en] Identifying the genetic basis of repeatedly evolved traits provides a way to reconstruct their evolutionary history and ultimately investigate the predictability of evolution. Here, we focus on the oldfield mouse (Peromyscus polionotus), which occurs in the southeastern United States, where it exhibits considerable color variation. Dorsal coats range from dark brown in mainland mice to near white in mice inhabiting sandy beaches; this light pelage has evolved independently on Florida's Gulf and Atlantic coasts as camouflage from predators. To facilitate genomic analyses, we first generated a chromosome-level genome assembly of Peromyscus polionotus subgriseus. Next, in a uniquely variable mainland population (Peromyscus polionotus albifrons), we scored 23 pigment traits and performed targeted resequencing in 168 mice. We find that pigment variation is strongly associated with an ∼2-kb region ∼5 kb upstream of the Agouti signaling protein coding region. Using a reporter-gene assay, we demonstrate that this regulatory region contains an enhancer that drives expression in the dermis of mouse embryos during the establishment of pigment prepatterns. Moreover, extended tracts of homozygosity in this Agouti region indicate that the light allele experienced recent and strong positive selection. Notably, this same light allele appears fixed in both Gulf and Atlantic coast beach mice, despite these populations being separated by >1,000 km. Together, our results suggest that this identified Agouti enhancer allele has been maintained in mainland populations as standing genetic variation and from there, has spread to and been selected in two independent beach mouse lineages, thereby facilitating their rapid and parallel evolution.
Disciplines :
Life sciences: Multidisciplinary, general & others
Author, co-author :
Wooldridge, T Brock ; Department of Organismic & Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138 ; Department of Molecular & Cellular Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138 ; HHMI, Harvard University, Cambridge, MA 02138
Kautt, Andreas F ; Department of Organismic & Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138 ; Department of Molecular & Cellular Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138 ; HHMI, Harvard University, Cambridge, MA 02138
Lassance, Jean-Marc ; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA) > Génomique animale ; Department of Organismic & Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138 ; Department of Molecular & Cellular Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138 ; HHMI, Harvard University, Cambridge, MA 02138
McFadden, Sade ; Department of Organismic & Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138 ; Department of Molecular & Cellular Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138 ; HHMI, Harvard University, Cambridge, MA 02138
Domingues, Vera S ; Department of Organismic & Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138 ; Department of Molecular & Cellular Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138 ; HHMI, Harvard University, Cambridge, MA 02138
Mallarino, Ricardo ; Department of Molecular Biology, Princeton University, Princeton, NJ 08544
Hoekstra, Hopi E ; Department of Organismic & Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138 ; Department of Molecular & Cellular Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138 ; HHMI, Harvard University, Cambridge, MA 02138
Language :
English
Title :
An enhancer of Agouti contributes to parallel evolution of cryptically colored beach mice.
Publication date :
05 July 2022
Journal title :
Proceedings of the National Academy of Sciences of the United States of America
ISSN :
0027-8424
eISSN :
1091-6490
Publisher :
Proceedings of the National Academy of Sciences, United States
HHMI - Howard Hughes Medical Institute [US-MD] [US-MD] European Molecular Biology Organization [DE] DFG - Deutsche Forschungsgemeinschaft [DE] Human Frontier Science Program [FR] BAEF - Belgian American Educational Foundation [BE] FCT - Fundação para a Ciência e a Tecnologia [PT] NIH - National Institutes of Health [US-MD] [US-MD] NSF - National Science Foundation [US-VA] [US-VA]
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