The role of gene flow in rapid and repeated evolution of cave-related traits in Mexican tetra, Astyanax mexicanus

Adam Herman, Yaniv Brandvain, James Weagley, William R. Jeffery, Alex C. Keene, Thomas J.Y. Kono, Helena Bilandžija, Richard Borowsky, Luis Espinasa, Kelly O'Quin, Claudia P. Ornelas-García, Masato Yoshizawa, Brian Carlson, Ernesto Maldonado, Joshua B. Gross, Reed A. Cartwright, Nicolas Rohner, Wesley C. Warren, Suzanne E. McGaugh

Research output: Contribution to journalArticlepeer-review

32 Scopus citations

Abstract

Understanding the molecular basis of repeatedly evolved phenotypes can yield key insights into the evolutionary process. Quantifying gene flow between populations is especially important in interpreting mechanisms of repeated phenotypic evolution, and genomic analyses have revealed that admixture occurs more frequently between diverging lineages than previously thought. In this study, we resequenced 47 whole genomes of the Mexican tetra from three cave populations, two surface populations and outgroup samples. We confirmed that cave populations are polyphyletic and two Astyanax mexicanus lineages are present in our data set. The two lineages likely diverged much more recently than previous mitochondrial estimates of 5–7 mya. Divergence of cave populations from their phylogenetically closest surface population likely occurred between ~161 and 191 k generations ago. The favoured demographic model for most population pairs accounts for divergence with secondary contact and heterogeneous gene flow across the genome, and we rigorously identified gene flow among all lineages sampled. Therefore, the evolution of cave-related traits occurred more rapidly than previously thought, and trogolomorphic traits are maintained despite gene flow with surface populations. The recency of these estimated divergence events suggests that selection may drive the evolution of cave-derived traits, as opposed to disuse and drift. Finally, we show that a key trogolomorphic phenotype QTL is enriched for genomic regions with low divergence between caves, suggesting that regions important for cave phenotypes may be transferred between caves via gene flow. Our study shows that gene flow must be considered in studies of independent, repeated trait evolution.

Original languageEnglish (US)
Pages (from-to)4397-4416
Number of pages20
JournalMolecular ecology
Volume27
Issue number22
DOIs
StatePublished - Nov 2018

Bibliographical note

Funding Information:
Fish were collected under CONAPESCA permit PPF/DGOPA -106 / 2013 to Claudia Patricia Ornelas GarcD? anad SEMARNAT permit 02241 to Ernesto Maldonado. We thank the Mexican government for providing the collecting permit to R.B. in 2008 (DGOPA.00570.288108-0291). For 2002, the collection permit to R.B. was from fisheries department #01.01.02.613.03.1799 Molino sampleswereobtainedunderMexicanpermit040396-213-05.Animal care protocol numbers include #05-1235 by the New York University Animal Welfare Committee (UAWC) to R.B., UMD R-17-77 to WRJ, and UNAM animal care protocol to POG NOM-062-ZOO-1999. This work was supported by NIH grant 2R24OD011198-04A1 to WCW, The Genome Institute at Washington University School of Medicine, Cave Research Foundation Graduate Student Research Grant to BMC, a grant from the Eppley Foundation for Research to SEM, 5R01EY014619-08 to WRJ, and 1R01GM127872-01 to SEM and ACK. Raw sequence data were submitted to the SRA. Project Accession Number: SRP046999, Bioproject: PRJNA260715. We appreciate the resources provided by the Minnesota Supercomputing Institute, without which this work would not be possible.

Funding Information:
Eppley Foundation for Research, Grant/ Award Number: 1R01GM127872-01 and

Funding Information:
Fish were collected under CONAPESCA permit PPF/DGOPA - 106 / 2013 to Claudia Patricia Ornelas Garc?a and SEMARNAT permit 02241 to Ernesto Maldonado. We thank the Mexican government for providing the collecting permit to R.B. in 2008 (DGOPA.00570.288108-0291). For 2002, the collection permit to R.B. was from fisheries department #01.01.02.613.03.1799 Molino samples were obtained under Mexican permit 040396-213-05. Animal care protocol numbers include #05-1235 by the New York University Animal Welfare Committee (UAWC) to R.B., UMD R-17-77 to WRJ, and UNAM animal care protocol to POG NOM-062-ZOO-1999. This work was supported by NIH grant 2R24OD011198-04A1 to WCW, The Genome Institute at Washington University School of Medicine, Cave Research Foundation Graduate Student Research Grant to BMC, a grant from the Eppley Foundation for Research to SEM, 5R01EY014619-08 to WRJ, and 1R01GM127872-01 to SEM and ACK. Raw sequence data were submitted to the SRA. Project Accession Number: SRP046999, Bioproject: PRJNA260715. We appreciate the resources provided by the Minnesota Supercomputing Institute, without which this work would not be possible.

Publisher Copyright:
© 2018 John Wiley & Sons Ltd

Copyright:
Copyright 2019 Elsevier B.V., All rights reserved.

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