Evolution of Stickleback in 50 Years on Earthquake-Uplifted Islands

Evolution of stickleback in 50 years on PNAS PLUS earthquake-uplifted islands 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; and 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) How rapidly can animal populations in the wild evolve when faced occur immediately after a habitat shift or environmental distur- with sudden environmental shifts? Uplift during the 1964 Great bance (26, 27). However, because of previous technological lim- Alaska Earthquake abruptly created freshwater ponds on multiple itations, few studies of rapid differentiation in the wild have islands in Prince William Sound and the Gulf of Alaska. In the short included genetic data to fully disentangle evolution from induced time since the earthquake, the phenotypes of resident freshwater phenotypic plasticity. The small numbers of markers previously threespine stickleback fish on at least three of these islands have available for most population genetic studies have not provided changed dramatically from their oceanic ancestors. To test the the necessary precision with which to analyze very recently diverged hypothesis that these freshwater populations were derived from populations (but see refs. 28 and 29). As a consequence, the fre- oceanic ancestors only 50 y ago, we generated over 130,000 single- quency of contemporary evolution in the wild is still poorly defined, nucleotide polymorphism genotypes from more than 1,000 individ- and its genetic and genomic basis remains unclear (30). uals using restriction site-associated DNA sequencing (RAD-seq). Pop- Advances in sequencing technology now allow the precise in- ulation genomic analyses of these data support the hypothesis of ference from genomic data of colonization history and evolu- recent and repeated, independent colonization of freshwater habi- tionary patterns that have occurred over just a few generations tats by oceanic ancestors. We find evidence of recurrent gene flow (31, 32). The threespine stickleback system is ideal for testing EVOLUTION between oceanic and freshwater ecotypes where they co-occur. Our hypotheses about contemporary evolution. Postglacial adaptive data implicate natural selection in phenotypic diversification and radiations over the last 12,000–20,000 y in newly available support the hypothesis that the metapopulation organization of this freshwater habitats have spawned divergent phenotypes that species helps maintain a large pool of genetic variation that can be demonstrate parallel phenotypic evolution (33, 34), with un- redeployed rapidly when oceanic stickleback colonize freshwater en- derlying parallel genetic (35–39) and genomic (40–43) bases. An vironments. We find that the freshwater populations, despite pop- open question, however, is whether this parallel divergence in ulation genetic analyses clearly supporting their young age, have stickleback actually requires thousands of years, or whether it diverged phenotypically from oceanic ancestors to nearly the same can occur in nature over decadal timescales, as is implied by extent as populations that were likely founded thousands of years studies of a small number of recently formed artificial and wild ago. Our results support the intriguing hypothesis that most stickle- stickleback populations (44–50). Also unknown is how often the back evolution in fresh water occurs within the first few decades after invasion of a novel environment. Significance contemporary evolution | ecological divergence | population genomics | On several Alaskan islands, phenotypically variable threespine adaptation | metapopulation stickleback fish now live in ponds that were formed during uplift caused by the 1964 Great Alaska Earthquake. We ana- n March 27, 1964, the largest earthquake ever recorded in lyzed phenotypic and genome-wide genetic divergence of ONorth America struck the south coast of Alaska (1, 2). This resident freshwater and oceanic threespine stickleback pop- catastrophic event uplifted islands in Prince William Sound and ulations from three islands. These data support the hypothesis the Gulf of Alaska in just a few minutes, creating ponds from that the freshwater populations evolved repeatedly from their formerly marine habitat and setting the stage for the diversifi- Gasterosteus aculeatus oceanic ancestors in the past half-century, and have differen- cation of threespine stickleback fish ( )in tiated to nearly the same extent as populations that were these new freshwater sites. This seismic disturbance provides founded thousands of years ago. This work raises the possibility an excellent opportunity to address long-standing evolutionary that much of the evolution that occurs when oceanic stickleback questions regarding how often dramatic phenotypic shifts can – invade fresh water takes place in fewer than 50 generations after happen over contemporary timescales (3 7). colonization, rather than gradually over thousands of years. Despite examples of rapid divergence in wild populations, evolutionary rates may often be constrained by a suite of factors (8). Author contributions: E.A.L., S.L.B., F.A.v.H., and W.A.C. designed research; E.A.L., S.L.B., For example, evolution in new habitats may be limited by waiting J.C., O.G., M.L.S., and W.A.C. performed research; S.L.B., J.C., and W.A.C. contributed new times for new beneficial mutations (9–11). Even when adaptation 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. occurs from standing genetic variation, evolution via selection of The authors declare no conflict of interest. numerous independent loci of small effect may be time consuming This article is a PNAS Direct Submission. (12–16). We know, however, that evolution can occur rapidly, particularly under artificial selection or in human-altered landscapes Freely available online through the PNAS open access option. – — Data deposition: Single-nucleotide polymorphism (SNP) data from the sequences gener- (17 21). In addition, empirical studies in the wild particularly in ated for this study for the 3,000 loci used in these analyses have been deposited in Dryad response to significant environmental changes—have demonstrated (dx.doi.org/10.5061/dryad.pn85t). that strong selection and rapid evolution over decades may be more 1Present address: Private address, Tel Aviv, Israel 6230345. common than once thought (22–24). 2To whom correspondence should be addressed. Email: [email protected]. A rapid evolutionary response is predicted when the intensity This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. of directional selection is strong (11, 25), a scenario likely to 1073/pnas.1512020112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1512020112 PNAS Early Edition | 1of9 Downloaded by guest on September 28, 2021 countless populations of stickleback in geographically close Including Lateral Plates Excluding Lateral Plates Mi13 ponds represent invasion followed by local dispersal or inde- Mi19 Mi23 pendent founding from the sea. Mi08 Mi13 To address these questions, we identified populations from Mi23 Mi09 0 1.0 Mi08 three islands (Middleton, Montague, and Danger) in Prince Mi06 Mi06 SO 0.5 0.5 William Sound and the Gulf of Alaska that could have been − Mi19 SO SI Appendix PC 2 (2% & 16%) Mi09 founded only after the 1964 earthquake (Fig. 1 and , 1.0 − Table S1). Middleton Island was uplifted 3.4 m, creating a new −15 −10 −5 05 −2 −1 0 1 2 terrace with ponds from a previously submarine platform (1). PC 1 (93% & 28%) Similarly, Danger and Montague Islands experienced uplift and Fig. 2. PCAs describe the overall distribution of phenotypic variation in six creation of new ponds (51). Stickleback now can be found in sites from Middleton Island. Each point represents the population mean ± 2 many of the habitats produced by the earthquake (52). We first SE. Points for Mi08, Mi09, Mi13, and Mi19 represent means for only phe- analyzed a subset of populations from Middleton Island to de- notypically freshwater individuals as determined before analysis by visual scribe the pattern of multivariate phenotypic divergence. We inspection (Materials and Methods). Mi23 is a phenotypically oceanic pop- then produced and analyzed restriction site-associated DNA ulation originating from a marine habitat, and SO are oceanic individuals sequencing (RAD-seq) data (53, 54) from 25,000 RAD loci in pooled from all four sympatric sites included in the phenotypic analysis 1,057 individuals collected from a total of 20 populations from (Mi08, Mi09, Mi13, and Mi19). High/partially plated groups are in green, and all three islands and one mainland population. Deep sequencing low plated are in blue. yielded a set of 130,000 single-nucleotide polymorphisms (SNPs) and a total of 146 million genotypes. This large genomic dataset allowed appropriate for defining (and assigning individuals to) genetic us to ask whether phenotypic and genetic divergence in stickleback, groupings across recently formed populations potentially

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