Hybridization underlies localized trait evolution in cavefish

Rachel L. Moran; James B. Jaggard; Emma Y. Roback; Alexander Kenzior; Nicolas Rohner; Johanna E. Kowalko; Claudia Patricia Ornelas-García; Suzanne E. McGaugh; Alex C. Keene

doi:10.1016/j.isci.2022.103778

Hybridization underlies localized trait evolution in cavefish

Rachel L. Moran, James B. Jaggard, Emma Y. Roback, Alexander Kenzior, Nicolas Rohner, Johanna E. Kowalko, Claudia Patricia Ornelas-García, Suzanne E. McGaugh, Alex C. Keene

Ecology, Evolution and Behavior

Research output: Contribution to journal › Article › peer-review

20 Scopus citations

Abstract

Introgressive hybridization may play an integral role in local adaptation and speciation (Taylor and Larson, 2019). In the Mexican tetra Astyanax mexicanus, cave populations have repeatedly evolved traits including eye loss, sleep loss, and albinism. Of the 30 caves inhabited by A. mexicanus, Chica cave is unique because it contains multiple pools inhabited by putative hybrids between surface and cave populations (Mitchell et al., 1977), providing an opportunity to investigate the impact of hybridization on complex trait evolution. We show that hybridization between cave and surface populations may contribute to localized variation in traits associated with cave evolution, including pigmentation, eye development, and sleep. We also uncover an example of convergent evolution in a circadian clock gene in multiple cavefish lineages and burrowing mammals, suggesting a shared genetic mechanism underlying circadian disruption in subterranean vertebrates. Our results provide insight into the role of hybridization in facilitating phenotypic evolution.

Original language	English (US)
Article number	103778
Journal	iScience
Volume	25
Issue number	2
DOIs	https://doi.org/10.1016/j.isci.2022.103778
State	Published - Feb 18 2022

Bibliographical note

Funding Information:
We thank two anonymous reviewers for their comments and feedback which have greatly improved this manuscript. We thank the University of Minnesota Genomics Center for their guidance and for performing the library preparations and sequencing. The Minnesota Supercomputing Institute (MSI) at the University of Minnesota provided resources that contributed to the research results reported within this article. Funding was supported by NIH 1R01GM127872-01 to SEM, ACK, and NR, NSF award IOS-165674 to ACK, a US-Israel BSF award to ACK, NSF award DEB-2147597 to JK and ACK, NSF awards IOS-1933076 and IOS-2202359 to JK, SEM, and NR, and NIH NHLBI sleep training grant T32HL007713-28 to JBJ. Fish were collected under CONAPESCA permit SGPA/DGVS/266/15 to Claudia Patricia Ornelas García.

Funding Information:
We thank two anonymous reviewers for their comments and feedback which have greatly improved this manuscript. We thank the University of Minnesota Genomics Center for their guidance and for performing the library preparations and sequencing. The Minnesota Supercomputing Institute (MSI) at the University of Minnesota provided resources that contributed to the research results reported within this article. Funding was supported by NIH 1R01GM127872-01 to SEM, ACK, and NR, NSF award IOS-165674 to ACK, a US-Israel BSF award to ACK, NSF award DEB-2147597 to JK and ACK, NSF awards IOS-1933076 and IOS-2202359 to JK, SEM, and NR, and NIH NHLBI sleep training grant T32HL007713-28 to JBJ. Fish were collected under CONAPESCA permit SGPA/DGVS/266/15 to Claudia Patricia Ornelas Garc?a. Conceptualization, S.E.M. and A.C.K.; investigation and analysis, R.L.M. J.B.J. E.Y.R. A.K. N.R. J.E.K. P.O.-G. S.E.M. and A.C.K.; visualization, R.L.M. J.B.J. E.Y.R.; writing - original draft, R.L.M. writing - review and editing, R.L.M. J.B.J. E.Y.R. A.K. N.R. J.E.K. P.O.-G. S.E.M. and A.C.K. The authors declare no competing interests.

Publisher Copyright:
© 2022

Keywords

Aquatic biology
Aquatic science
Evolutionary biology

Publisher link

10.1016/j.isci.2022.103778

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@article{ed28b03011764d2c86a185848128cb84,

title = "Hybridization underlies localized trait evolution in cavefish",

abstract = "Introgressive hybridization may play an integral role in local adaptation and speciation (Taylor and Larson, 2019). In the Mexican tetra Astyanax mexicanus, cave populations have repeatedly evolved traits including eye loss, sleep loss, and albinism. Of the 30 caves inhabited by A. mexicanus, Chica cave is unique because it contains multiple pools inhabited by putative hybrids between surface and cave populations (Mitchell et al., 1977), providing an opportunity to investigate the impact of hybridization on complex trait evolution. We show that hybridization between cave and surface populations may contribute to localized variation in traits associated with cave evolution, including pigmentation, eye development, and sleep. We also uncover an example of convergent evolution in a circadian clock gene in multiple cavefish lineages and burrowing mammals, suggesting a shared genetic mechanism underlying circadian disruption in subterranean vertebrates. Our results provide insight into the role of hybridization in facilitating phenotypic evolution.",

keywords = "Aquatic biology, Aquatic science, Evolutionary biology",

author = "Moran, {Rachel L.} and Jaggard, {James B.} and Roback, {Emma Y.} and Alexander Kenzior and Nicolas Rohner and Kowalko, {Johanna E.} and Ornelas-Garc{\'i}a, {Claudia Patricia} and McGaugh, {Suzanne E.} and Keene, {Alex C.}",

note = "Funding Information: We thank two anonymous reviewers for their comments and feedback which have greatly improved this manuscript. We thank the University of Minnesota Genomics Center for their guidance and for performing the library preparations and sequencing. The Minnesota Supercomputing Institute (MSI) at the University of Minnesota provided resources that contributed to the research results reported within this article. Funding was supported by NIH 1R01GM127872-01 to SEM, ACK, and NR, NSF award IOS-165674 to ACK, a US-Israel BSF award to ACK, NSF award DEB-2147597 to JK and ACK, NSF awards IOS-1933076 and IOS-2202359 to JK, SEM, and NR, and NIH NHLBI sleep training grant T32HL007713-28 to JBJ. Fish were collected under CONAPESCA permit SGPA/DGVS/266/15 to Claudia Patricia Ornelas Garc{\'i}a. Funding Information: We thank two anonymous reviewers for their comments and feedback which have greatly improved this manuscript. We thank the University of Minnesota Genomics Center for their guidance and for performing the library preparations and sequencing. The Minnesota Supercomputing Institute (MSI) at the University of Minnesota provided resources that contributed to the research results reported within this article. Funding was supported by NIH 1R01GM127872-01 to SEM, ACK, and NR, NSF award IOS-165674 to ACK, a US-Israel BSF award to ACK, NSF award DEB-2147597 to JK and ACK, NSF awards IOS-1933076 and IOS-2202359 to JK, SEM, and NR, and NIH NHLBI sleep training grant T32HL007713-28 to JBJ. Fish were collected under CONAPESCA permit SGPA/DGVS/266/15 to Claudia Patricia Ornelas Garc?a. Conceptualization, S.E.M. and A.C.K.; investigation and analysis, R.L.M. J.B.J. E.Y.R. A.K. N.R. J.E.K. P.O.-G. S.E.M. and A.C.K.; visualization, R.L.M. J.B.J. E.Y.R.; writing - original draft, R.L.M. writing - review and editing, R.L.M. J.B.J. E.Y.R. A.K. N.R. J.E.K. P.O.-G. S.E.M. and A.C.K. The authors declare no competing interests. Publisher Copyright: {\textcopyright} 2022",

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AU - Jaggard, James B.

AU - Roback, Emma Y.

AU - Kenzior, Alexander

AU - Rohner, Nicolas

AU - Kowalko, Johanna E.

AU - Ornelas-García, Claudia Patricia

AU - McGaugh, Suzanne E.

AU - Keene, Alex C.

N1 - Funding Information: We thank two anonymous reviewers for their comments and feedback which have greatly improved this manuscript. We thank the University of Minnesota Genomics Center for their guidance and for performing the library preparations and sequencing. The Minnesota Supercomputing Institute (MSI) at the University of Minnesota provided resources that contributed to the research results reported within this article. Funding was supported by NIH 1R01GM127872-01 to SEM, ACK, and NR, NSF award IOS-165674 to ACK, a US-Israel BSF award to ACK, NSF award DEB-2147597 to JK and ACK, NSF awards IOS-1933076 and IOS-2202359 to JK, SEM, and NR, and NIH NHLBI sleep training grant T32HL007713-28 to JBJ. Fish were collected under CONAPESCA permit SGPA/DGVS/266/15 to Claudia Patricia Ornelas García. Funding Information: We thank two anonymous reviewers for their comments and feedback which have greatly improved this manuscript. We thank the University of Minnesota Genomics Center for their guidance and for performing the library preparations and sequencing. The Minnesota Supercomputing Institute (MSI) at the University of Minnesota provided resources that contributed to the research results reported within this article. Funding was supported by NIH 1R01GM127872-01 to SEM, ACK, and NR, NSF award IOS-165674 to ACK, a US-Israel BSF award to ACK, NSF award DEB-2147597 to JK and ACK, NSF awards IOS-1933076 and IOS-2202359 to JK, SEM, and NR, and NIH NHLBI sleep training grant T32HL007713-28 to JBJ. Fish were collected under CONAPESCA permit SGPA/DGVS/266/15 to Claudia Patricia Ornelas Garc?a. Conceptualization, S.E.M. and A.C.K.; investigation and analysis, R.L.M. J.B.J. E.Y.R. A.K. N.R. J.E.K. P.O.-G. S.E.M. and A.C.K.; visualization, R.L.M. J.B.J. E.Y.R.; writing - original draft, R.L.M. writing - review and editing, R.L.M. J.B.J. E.Y.R. A.K. N.R. J.E.K. P.O.-G. S.E.M. and A.C.K. The authors declare no competing interests. Publisher Copyright: © 2022

PY - 2022/2/18

Y1 - 2022/2/18

N2 - Introgressive hybridization may play an integral role in local adaptation and speciation (Taylor and Larson, 2019). In the Mexican tetra Astyanax mexicanus, cave populations have repeatedly evolved traits including eye loss, sleep loss, and albinism. Of the 30 caves inhabited by A. mexicanus, Chica cave is unique because it contains multiple pools inhabited by putative hybrids between surface and cave populations (Mitchell et al., 1977), providing an opportunity to investigate the impact of hybridization on complex trait evolution. We show that hybridization between cave and surface populations may contribute to localized variation in traits associated with cave evolution, including pigmentation, eye development, and sleep. We also uncover an example of convergent evolution in a circadian clock gene in multiple cavefish lineages and burrowing mammals, suggesting a shared genetic mechanism underlying circadian disruption in subterranean vertebrates. Our results provide insight into the role of hybridization in facilitating phenotypic evolution.

AB - Introgressive hybridization may play an integral role in local adaptation and speciation (Taylor and Larson, 2019). In the Mexican tetra Astyanax mexicanus, cave populations have repeatedly evolved traits including eye loss, sleep loss, and albinism. Of the 30 caves inhabited by A. mexicanus, Chica cave is unique because it contains multiple pools inhabited by putative hybrids between surface and cave populations (Mitchell et al., 1977), providing an opportunity to investigate the impact of hybridization on complex trait evolution. We show that hybridization between cave and surface populations may contribute to localized variation in traits associated with cave evolution, including pigmentation, eye development, and sleep. We also uncover an example of convergent evolution in a circadian clock gene in multiple cavefish lineages and burrowing mammals, suggesting a shared genetic mechanism underlying circadian disruption in subterranean vertebrates. Our results provide insight into the role of hybridization in facilitating phenotypic evolution.

KW - Aquatic biology

KW - Aquatic science

KW - Evolutionary biology

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Hybridization underlies localized trait evolution in cavefish

Abstract

Bibliographical note

Keywords

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