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Edited by John C. Avise, University of California, Irvine, CA, and approved November 9, 2015 (received for review June 19, 2015)
Significance
On several Alaskan islands, phenotypically variable threespine stickleback fish now live in ponds that were formed during uplift caused by the 1964 Great Alaska Earthquake. We analyzed phenotypic and genome-wide genetic divergence of resident freshwater and oceanic threespine stickleback populations from three islands. These data support the hypothesis that the freshwater populations evolved repeatedly from their oceanic ancestors in the past half-century, and have differentiated to nearly the same extent as populations that were founded thousands of years ago. This work raises the possibility that much of the evolution that occurs when oceanic stickleback invade fresh water takes place in fewer than 50 generations after colonization, rather than gradually over thousands of years.
Abstract
How rapidly can animal populations in the wild evolve when faced with sudden environmental shifts? Uplift during the 1964 Great Alaska Earthquake abruptly created freshwater ponds on multiple islands in Prince William Sound and the Gulf of Alaska. In the short time since the earthquake, the phenotypes of resident freshwater threespine stickleback fish on at least three of these islands have changed dramatically from their oceanic ancestors. To test the hypothesis that these freshwater populations were derived from oceanic ancestors only 50 y ago, we generated over 130,000 single-nucleotide polymorphism genotypes from more than 1,000 individuals using restriction site-associated DNA sequencing (RAD-seq). Population genomic analyses of these data support the hypothesis of recent and repeated, independent colonization of freshwater habitats by oceanic ancestors. We find evidence of recurrent gene flow between oceanic and freshwater ecotypes where they co-occur. Our data implicate natural selection in phenotypic diversification and support the hypothesis that the metapopulation organization of this species helps maintain a large pool of genetic variation that can be redeployed rapidly when oceanic stickleback colonize freshwater environments. We find that the freshwater populations, despite population genetic analyses clearly supporting their young age, have diverged phenotypically from oceanic ancestors to nearly the same extent as populations that were likely founded thousands of years ago. Our results support the intriguing hypothesis that most stickleback evolution in fresh water occurs within the first few decades after invasion of a novel environment.
Footnotes
↵1Present address: Private address, Tel Aviv, Israel 6230345.
- ↵2To whom correspondence should be addressed. Email: wcresko{at}uoregon.edu.
Author contributions: E.A.L., S.L.B., F.A.v.H., and W.A.C. designed research; E.A.L., S.L.B., J.C., O.G., M.L.S., and W.A.C. performed research; S.L.B., J.C., and W.A.C. contributed new reagents/analytic tools; E.A.L., S.L.B., J.C., and W.A.C. analyzed data; and E.A.L., S.L.B., J.C., F.A.v.H., and W.A.C. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: Single-nucleotide polymorphism (SNP) data from the sequences generated for this study for the 3,000 loci used in these analyses have been deposited in Dryad (dx.doi.org/10.5061/dryad.pn85t).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1512020112/-/DCSupplemental.
Freely available online through the PNAS open access option.
- Emily A. Lescaka,b,
- Susan L. Basshamc,
- Julian Catchenc,d,
- Ofer Gelmondb,1,
- Mary L. Sherbickb,
- Frank A. von Hippelb, and
- William A. Creskoc,2
- aSchool of Fisheries and Ocean Sciences, University of Alaska Fairbanks, Fairbanks, AK 99775;
- bDepartment of Biological Sciences, University of Alaska Anchorage, Anchorage, AK 99508;
- cInstitute of Ecology and Evolution, University of Oregon, Eugene, OR 97403;
- dDepartment of Animal Biology, University of Illinois at Urbana–Champaign, Urbana, IL 61801
Edited by John C. Avise, University of California, Irvine, CA, and approved November 9, 2015 (received for review June 19, 2015)
Significance
On several Alaskan islands, phenotypically variable threespine stickleback fish now live in ponds that were formed during uplift caused by the 1964 Great Alaska Earthquake. We analyzed phenotypic and genome-wide genetic divergence of resident freshwater and oceanic threespine stickleback populations from three islands. These data support the hypothesis that the freshwater populations evolved repeatedly from their oceanic ancestors in the past half-century, and have differentiated to nearly the same extent as populations that were founded thousands of years ago. This work raises the possibility that much of the evolution that occurs when oceanic stickleback invade fresh water takes place in fewer than 50 generations after colonization, rather than gradually over thousands of years.
Abstract
How rapidly can animal populations in the wild evolve when faced with sudden environmental shifts? Uplift during the 1964 Great Alaska Earthquake abruptly created freshwater ponds on multiple islands in Prince William Sound and the Gulf of Alaska. In the short time since the earthquake, the phenotypes of resident freshwater threespine stickleback fish on at least three of these islands have changed dramatically from their oceanic ancestors. To test the hypothesis that these freshwater populations were derived from oceanic ancestors only 50 y ago, we generated over 130,000 single-nucleotide polymorphism genotypes from more than 1,000 individuals using restriction site-associated DNA sequencing (RAD-seq). Population genomic analyses of these data support the hypothesis of recent and repeated, independent colonization of freshwater habitats by oceanic ancestors. We find evidence of recurrent gene flow between oceanic and freshwater ecotypes where they co-occur. Our data implicate natural selection in phenotypic diversification and support the hypothesis that the metapopulation organization of this species helps maintain a large pool of genetic variation that can be redeployed rapidly when oceanic stickleback colonize freshwater environments. We find that the freshwater populations, despite population genetic analyses clearly supporting their young age, have diverged phenotypically from oceanic ancestors to nearly the same extent as populations that were likely founded thousands of years ago. Our results support the intriguing hypothesis that most stickleback evolution in fresh water occurs within the first few decades after invasion of a novel environment.
- contemporary evolution
- ecological divergence
- population genomics
- adaptation
- metapopulation
Footnotes
↵1Present address: Private address, Tel Aviv, Israel 6230345.
- ↵2To whom correspondence should be addressed. Email: wcresko{at}uoregon.edu.
Author contributions: E.A.L., S.L.B., F.A.v.H., and W.A.C. designed research; E.A.L., S.L.B., J.C., O.G., M.L.S., and W.A.C. performed research; S.L.B., J.C., and W.A.C. contributed new reagents/analytic tools; E.A.L., S.L.B., J.C., and W.A.C. analyzed data; and E.A.L., S.L.B., J.C., F.A.v.H., and W.A.C. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: Single-nucleotide polymorphism (SNP) data from the sequences generated for this study for the 3,000 loci used in these analyses have been deposited in Dryad (dx.doi.org/10.5061/dryad.pn85t).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1512020112/-/DCSupplemental.
Freely available online through the PNAS open access option.
Rapid stickleback evolutionary genomics
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