TY - JOUR
T1 - An enhancer of Agouti contributes to parallel evolution of cryptically colored beach mice
AU - Wooldridge, T. Brock
AU - Kautt, Andreas F.
AU - Lassance, Jean Marc
AU - McFadden, Sade
AU - Domingues, Vera S.
AU - Hoekstra, Hopi E.
AU - Mallarino, Ricardo
N1 - Funding Information:
ACKNOWLEDGMENTS. We thank M. Omura of the Harvard MCZ for assistance in preparing and accessioning voucher specimens, N. Bedford for collecting P. p. leucocephalus specimens for WGS, E. Kingsley for providing P. m. nubiterrae samples, and J. Weber and E. Delaney for assistance in the field. C. Hu designed the illustration in Fig. 2A, and T. Capellini provided advice on the reporter assays and feedback on a draft of this manuscript together with S. He, C. Kratochwil, and M. Manceau. A.F.K. was supported by European Molecular Biology Organization (EMBO) Postdoctoral Fellowship ALTF 47-2018 and German Science Foundation Postdoctoral Fellowship KA 5308/1-1. J.-M.L. was supported by EMBO Grant ALTF 379-2011, Human Frontiers Science Program Grant LT001086/2012, and the Belgian American Educational Foundation. V.S.D. was supported by the Portuguese Foundation for Science and Technology. Fieldwork was supported by an MCZ Putnam Grant (to V.S.D. and H.E.H.), and laboratory work was supported by NIH Grant R35GM133758 (to R.M.) and NSF Grant DEB-0919190 (to H.E.H.). H.E.H. is an investigator of the Howard Hughes Medical Institute.
Funding Information:
We thank M. Omura of the Harvard MCZ for assistance in preparing and accessioning voucher specimens, N. Bedford for collecting P. p. leucocephalus specimens for WGS, E. Kingsley for providing P. m. nubiterrae samples, and J. Weber and E. Delaney for assistance in the field. C. Hu designed the illustration in Fig. 2A, and T. Capellini provided advice on the reporter assays and feedback on a draft of this manuscript together with S. He, C. Kratochwil, and M. Manceau. A.F.K. was supported by European Molecular Biology Organization (EMBO) Postdoctoral Fellowship ALTF 47-2018 and German Science Foundation Postdoctoral Fellowship KA 5308/1-1. J.-M.L. was supported by EMBO Grant ALTF 379-2011, Human Frontiers Science Program Grant LT001086/2012, and the Belgian American Educational Foundation. V.S.D. was supported by the Portuguese Foundation for Science and Technology. Fieldwork was supported by an MCZ Putnam Grant (to V.S.D. and H.E.H.), and laboratory work was supported by NIH Grant R35GM133758 (to R.M.) and NSF Grant DEB-0919190 (to H.E.H.). H.E.H. is an investigator of the Howard Hughes Medical Institute.
Publisher Copyright:
Copyright © 2022 the Author(s).
PY - 2022/7/5
Y1 - 2022/7/5
N2 - 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.
AB - 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.
KW - adaptation
KW - camouflage
KW - convergence
KW - deer mice
KW - pigmentation
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U2 - 10.1073/pnas.2202862119
DO - 10.1073/pnas.2202862119
M3 - Article
C2 - 35776547
AN - SCOPUS:85133853550
VL - 119
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
SN - 0027-8424
IS - 27
M1 - e2202862119
ER -