skip to main content


The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 5:00 PM ET until 11:00 PM ET on Friday, June 21 due to maintenance. We apologize for the inconvenience.

This content will become publicly available on September 5, 2024

Title: Rapid genetic adaptation to a novel ecosystem despite a large founder event

Introduced and invasive species make excellent natural experiments for investigating rapid evolution. Here, we describe the effects of genetic drift and rapid genetic adaptation in pink salmon (Oncorhynchus gorbuscha) that were accidentally introduced to the Great Lakes via a single introduction event 31 generations ago. Using whole‐genome resequencing for 134 fish spanning five sample groups across the native and introduced range, we estimate that the source population's effective population size was 146,886 at the time of introduction, whereas the founding population's effective population size was just 72—a 2040‐fold decrease. As expected with a severe founder event, we show reductions in genome‐wide measures of genetic diversity, specifically a 37.7% reduction in the number of SNPs and an 8.2% reduction in observed heterozygosity. Despite this decline in genetic diversity, we provide evidence for putative selection at 47 loci across multiple chromosomes in the introduced populations, including missense variants in genes associated with circadian rhythm, immunological response and maturation, which match expected or known phenotypic changes in the Great Lakes. For one of these genes, we use a species‐specific agent‐based model to rule out genetic drift and conclude our results support a strong response to selection occurring in a period gene (per2) that plays a predominant role in determining an organism's daily clock, matching large day length differences experienced by introduced salmon during important phenological periods. Together, these results inform how populations might evolve rapidly to new environments, even with a small pool of standing genetic variation.

more » « less
Award ID(s):
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
Wiley Online Library
Date Published:
Journal Name:
Molecular Ecology
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Identifying genomic signatures of natural selection can be challenging against a background of demographic changes such as bottlenecks and population expansions. Here, we disentangle the effects of demography from selection in the House Finch (Haemorhous mexicanus) using samples collected before and after a pathogen‐induced selection event. Using ddRADseq, we genotyped over 18,000SNPs across the genome in native pre‐epizootic westernUSbirds, introduced birds from Hawaii and the eastern United States, post‐epizootic eastern birds, and western birds sampled across a similar time span. We found 14% and 7% reductions in nucleotide diversity, respectively, in Hawaiian and pre‐epizootic eastern birds relative to pre‐epizootic western birds, as well as elevated levels of linkage disequilibrium and other signatures of founder events. Despite finding numerous significant frequency shifts (outlier loci) between pre‐epizootic native and introduced populations, we found no signal of reduced genetic diversity, elevated linkage disequilibrium, or outlier loci as a result of the epizootic. Simulations demonstrate that the proportion of outliers associated with founder events could be explained by genetic drift. This rare view of genetic evolution across time in an invasive species provides direct evidence that demographic shifts like founder events have genetic consequences more widespread across the genome than natural selection.

    more » « less
  2. Abstract

    Obovaria olivariais a species of freshwater mussel native to the Mississippi River and Laurentian Great Lakes‐St. Lawrence River drainages of North America. This mussel has experienced population declines across large parts of its distribution and is imperiled in many jurisdictions.Obovaria olivariauses the similarly imperiledAcipenser fulvescens(Lake Sturgeon) as a host for its glochidia. We employed mitochondrial DNA sequencing and restriction site‐associated DNA sequencing (RAD‐seq) to assess patterns of genetic diversity and population structure ofOolivariafrom 19 collection locations including the St. Lawrence River drainage, the Great Lakes drainage, the Upper Mississippi River drainage, the Ohioan River drainage, and the Mississippi Embayment. Heterozygosity was highest in Upper Mississippi and Great Lakes populations, followed by a reduction in diversity and relative effective population size in the St. Lawrence populations. PairwiseFSTranged from 0.00 to 0.20, and analyses of genetic structure revealed two major ancestral populations, one including all St. Lawrence River/Ottawa River sites and the other including remaining sites; however, significant admixture and isolation by river distance across the range were evident. The genetic diversity and structure ofOolivariais consistent with the existing literature onAcipenser fulvescensand suggests that, although northern and southernOolivariapopulations are genetically distinct, genetic structure inOolivariais largely clinal rather than discrete across its range. Conservation and restoration efforts ofOolivariashould prioritize the maintenance and restoration of locations whereOolivariaremain, especially in northern rivers, and to ensure connectivity that will facilitate dispersal ofAcipenser fulvescensand movement of encysted glochidia.

    more » « less
  3. Abstract

    The successes of introduced populations in novel habitats often provide powerful examples of evolution and adaptation. In the 1950s, opossum shrimp (Mysis diluviana) individuals from Clearwater Lake in Minnesota, USA were transported and introduced to Twin Lakes in Colorado, USA by fisheries managers to supplement food sources for trout.Mysiswere subsequently introduced from Twin Lakes into numerous lakes throughout Colorado. Because managers kept detailed records of the timing of the introductions, we had the opportunity to test for evolutionary divergence within a known time interval. Here, we used reduced representation genomic data to investigate patterns of genetic diversity, test for genetic divergence between populations, and for evidence of adaptive evolution within the introduced populations in Colorado. We found very low levels of genetic diversity across all populations, with evidence for some genetic divergence between the Minnesota source population and the introduced populations in Colorado. There was little differentiation among the Colorado populations, consistent with the known provenance of a single founding population, with the exception of the population from Gross Reservoir, Colorado. Demographic modeling suggests that at least one undocumented introduction from an unknown source population hybridized with the population in Gross Reservoir. Despite the overall low genetic diversity we observed,FSToutlier and environmental association analyses identified multiple loci exhibiting signatures of selection and adaptive variation related to elevation and lake depth. The success of introduced species is thought to be limited by genetic variation, but our results imply that populations with limited genetic variation can become established in a wide range of novel environments. From an applied perspective, the observed patterns of divergence between populations suggest that genetic analysis can be a useful forensic tool to determine likely sources of invasive species.

    more » « less
  4. Abstract

    Species introductions provide opportunities to quantify rates and patterns of evolutionary change in response to novel environments. Alewives (Alosa pseudoharengus) are native to the East Coast of North America where they ascend coastal rivers to spawn in lakes and then return to the ocean. Some populations have become landlocked within the last 350 years and diverged phenotypically from their ancestral marine population. More recently, alewives were introduced to the Laurentian Great Lakes (~150 years ago), but these populations have not been compared to East Coast anadromous and landlocked populations. We quantified 95 years of evolution in foraging traits and overall body shape of Great Lakes alewives and compared patterns of phenotypic evolution of Great Lakes alewives to East Coast anadromous and landlocked populations. Our results suggest that gill raker spacing in Great Lakes alewives has evolved in a dynamic pattern that is consistent with responses to strong but intermittent eco‐evolutionary feedbacks with zooplankton size. Following their initial colonization of Lakes Ontario and Michigan, dense alewife populations likely depleted large‐bodied zooplankton, which drove a decrease in alewife gill raker spacing. However, the introduction of large, non‐native zooplankton to the Great Lakes in later decades resulted in an increase in gill raker spacing, and present‐day Great Lakes alewives have gill raker spacing patterns that are similar to the ancestral East Coast anadromous population. Conversely, contemporary Great Lakes alewife populations possess a gape width consistent with East Coast landlocked populations. Body shape showed remarkable parallel evolution with East Coast landlocked populations, likely due to a shared response to the loss of long‐distance movement or migrations. Our results suggest the colonization of a new environment and cessation of migration can result in rapid parallel evolution in some traits, but contingency also plays a role, and a dynamic ecosystem can also yield novel trait combinations.

    more » « less
  5. The influence of genetic drift on population dynamics during Pleistocene glacial cycles is well understood, but the role of selection in shaping patterns of genomic variation during these events is less explored. We resequenced whole genomes to investigate how demography and natural selection interact to generate the genomic landscapes of Downy and Hairy Woodpecker, species codistributed in previously glaciated North America. First, we explored the spatial and temporal patterns of genomic diversity produced by neutral evolution. Next, we tested (i) whether levels of nucleotide diversity along the genome are correlated with intrinsic genomic properties, such as recombination rate and gene density, and (ii) whether different demographic trajectories impacted the efficacy of selection. Our results revealed cycles of bottleneck and expansion, and genetic structure associated with glacial refugia. Nucleotide diversity varied widely along the genome, but this variation was highly correlated between the species, suggesting the presence of conserved genomic features. In both taxa, nucleotide diversity was positively correlated with recombination rate and negatively correlated with gene density, suggesting that linked selection played a role in reducing diversity. Despite strong fluctuations in effective population size, the maintenance of relatively large populations during glaciations may have facilitated selection. Under these conditions, we found evidence that the individual demographic trajectory of populations modulated linked selection, with purifying selection being more efficient in removing deleterious alleles in large populations. These results highlight that while genome-wide variation reflects the expected signature of demographic change during climatic perturbations, the interaction of multiple processes produces a predictable and highly heterogeneous genomic landscape. 
    more » « less