A lack of genetic diversity and minimal adaptive evolutionary divergence in introduced Mysis shrimp after 50 years

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. Mysis were 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, F _ST outlier 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.

Keywords: Mysis diluviana; biological introduction; genotype‐by‐environment association; population genetics; rapid evolution.

FIGURE 1

Study area of the southern Rocky Mountains of Colorado, USA. Sampled lakes are shaded in blue and labeled with the lake name and elevation in meters. Genomic analyses of the 168 individuals that passed our quality control thresholds included the source population of Mysis from Clearwater Lake, Minnesota (black dot, inset; elevation = 507 m; n = 23), and the Colorado source population from Twin Lakes (n = 16). Six stocked populations of Mysis included individuals from Ruedi Reservoir (n = 20), Dillon Reservoir (n = 20), Jefferson Reservoir (n = 20), Grand Lake (n = 20), Carter Lake (n = 20), and Gross Reservoir (n = 29).

FIGURE 2

Principal component analyses (PCA) of 168 Mysis and 18,220 imputed neutral SNPs (a) show individuals from Gross Reservoir clustering on PC1, while PC2 shows some divergence within, but not between remaining populations. Colors represent the lake from which the Mysis was sampled. The finding that the Gross Reservoir is distinct from all other sampled populations was consistent after restricting the dataset to 1371 SNPs with less than 20% missing data according to PCA (b). Discriminant analysis of principal components (DAPC) using 73 PCs, which explained 51.4% of the genetic variation (c), suggests additional structure between the Clearwater Lake source population and all other sampled Mysis populations. Repeating the DAPC using 20 PCs, which explained 50.3% of the genetic variation, shows individuals from Gross Reservoir forming a distinct genetic cluster (d). Inset image shows an adult Mysis diluviana (illustration by J. F. McLaughlin).

FIGURE 3

Population‐based redundancy analysis (RDA) using allele frequencies of 168 Mysis from eight sampled lakes shows some population‐based genetic association with environment (a). Colored points show where populations from different lakes load on for RDA axes 1 and 2 using 18,441 genetic markers (SNPs) as the response and elevation and maximum lake depth as the predictors (black arrows). Individual‐based PCA (b) using the 221 candidate adaptive markers identified by RDA and PCADAPT shows limited differentiation across adaptive loci. While PC1 and PC2 show some variation between and within populations, there is no clear signature of adaptive divergence between lake populations in the top 10 PC axes. Discriminant analysis of principal components (DAPC) of the 221 candidate adaptive markers using 20 PCs, which explained 50.3% of the genetic variation (c), suggests some additional structure across lakes. Points are shaded by which lake they were sampled matching Figure 2.