Evolution of stickleback in 50 years on earthquake-uplifted islands

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 singlenucleotide 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. 27, 1964, the largest earthquake ever recorded in North America struck the south coast of Alaska (1, 2). This catastrophic event uplifted islands in Prince William Sound and the Gulf of Alaska in just a few minutes, creating ponds from formerly marine habitat and setting the stage for the diversification of threespine stickleback fish (Gasterosteus aculeatus) in these new freshwater sites. This seismic disturbance provides an excellent opportunity to address long-standing evolutionary questions regarding how often dramatic phenotypic shifts can happen over contemporary timescales (3-7).Despite examples of rapid divergence in wild populations, evolutionary rates may often be constrained by a suite of factors (8). For example, evolution in new habitats may be limited by waiting times for new beneficial mutations (9-11). Even when adaptation occurs from standing genetic variation, evolution via selection of numerous independent loci of small effect may be time consuming (12-16). We know, however, that evolution can occur rapidly, particularly under artificial selection or in human-altered landscapes (17-21). In addition, empirical studies in the wild-particularly in response to significant environmental changes-have demonstrated that strong selection and rapid evolution over decades may be more common than once thought (22-24).A rapid evolutionary response is predict...

The life aquatic: advances in marine vertebrate genomics

“…Divergent taxon pairs of marine and freshwater threespine stickleback, Gasterosteus aculeatus, are an important system for the study of ecological speciation 55,56 . The marine form spends most of its adult life in the sea but returns to freshwater to breed, whereas…”

“…Reuse of standing genetic variation, at multiple markers across the stickleback genome, has been shown to be an important component of rapid parallel evolution of divergent species pairs [56][57][58][59][60] . This standing genetic variation remains at low frequency in marine populations [57][58][59] , suggesting that only a small number of founders contribute these adaptive alleles to freshwater populations.…”

Regulatory Architecture of Gene Expression Variation in the Threespine Stickleback Gasterosteus aculeatus

“…The species is also distributed throughout semimarine environments with large temperature and salinity gradients, such as estuaries and the brackish water Baltic Sea (McCairns and Bernatchez 2010; Guo et al 2015; Konijnendijk et al 2015). Successful colonization of these diverse habitats necessitates behavioral, morphological, and physiological adaptation to novel environmental conditions including changed temperature, salinity, oxygen, light, parasite and predator regimens, a process that can occur rapidly (Kitano et al 2010; Barrett et al 2011; Terekhanova et al 2014; Lescak et al 2015; Huang et al 2016, Rennison et al 2016). Parallel adaptations between independently founded freshwater populations frequently involve the same regions of the genome and arise from preexisting genetic variation in the marine population (Colosimo et al 2005; Hohenlohe et al 2010; Jones et al 2012; Liu et al 2014; Conte et al 2015, but see DeFaveri et al 2011; Leinonen et al 2012; Ellis et al 2015; Ferchaud and Hansen 2016).…”

Regulatory architecture of gene expression variation in the threespine stickleback, Gasterosteus aculeatus

“…The species is also distributed throughout semimarine environments with large temperature and salinity gradients, such as estuaries and the brackish water Baltic Sea (McCairns and Bernatchez 2010;Guo et al 2015;Konijnendijk et al 2015). Successful colonization of these diverse habitats necessitates behavioral, morphological, and physiological adaptation to novel environmental conditions including changed temperature, salinity, oxygen, light, parasite and predator regimens, a process that can occur rapidly (Kitano et al 2010;Barrett et al 2011;Terekhanova et al 2014;Lescak et al 2015;Huang et al 2016, Rennison et al 2016. Parallel adaptations between independently founded freshwater populations frequently involve the same regions of the genome and arise from preexisting genetic variation in the marine population (Colosimo et al 2005;Hohenlohe et al 2010;Jones et al 2012;Liu et al 2014;Conte et al 2015, but see DeFaveri et al 2011Leinonen et al 2012;Ellis et al 2015;Ferchaud and Hansen 2016).…”