Genomics reveal the origins and current structure of a genetically depauperate freshwater species in its introduced Alaskan range

Abstract

Invasive species are a major threat to global biodiversity, yet also represent large-scale unplanned ecological and evolutionary experiments to address fundamental questions in nature. Here we analyzed both native and invasive populations of predatory northern pike (Esox lucius) to characterize landscape genetic variation, determine the most likely origins of introduced populations, and investigate a presumably postglacial population from Southeast Alaska of unclear provenance. Using a set of 4329 SNPs from 351 individual Alaskan northern pike representing the most widespread geographic sampling to date, our results confirm low levels of genetic diversity in native populations (average 𝝅 of 3.18 × 10^-4) and even less in invasive populations (average 𝝅 of 2.68 × 10^-4) consistent with bottleneck effects. Our analyses indicate that invasive northern pike likely came from multiple introductions from different native Alaskan populations and subsequently dispersed from original introduction sites. At the broadest scale, invasive populations appear to have been founded from two distinct regions of Alaska, indicative of two independent introduction events. Genetic admixture resulting from introductions from multiple source populations may have mitigated the negative effects associated with genetic bottlenecks in this species with naturally low levels of genetic diversity. Genomic signatures strongly suggest an excess of rare, population-specific alleles, pointing to a small number of founding individuals in both native and introduced populations consistent with a species' life history of limited dispersal and gene flow. Lastly, the results strongly suggest that a small isolated population of pike, located in Southeast Alaska, is native in origin rather than stemming from a contemporary introduction event. Although theory predicts that lack of genetic variation may limit colonization success of novel environments, we detected no evidence that a lack of standing variation limited the success of this genetically depauperate apex predator.

Keywords: Esox lucius; dispersal; gene flow; invasive species; northern pike; population genetics.

FIGURE 1

Sampling sites of pike sequenced in this study as detailed in Table 1. Pike are native to Alaska north and west of the Alaska Range indicated by squares, except for a putative relictual population in Southeast Alaska represented by Antlen River in this study indicated by a triangle (Morrow, 1980). Sampling sites in Southcentral Alaska are bounded by a box and indicated by circles in the main figure are considered introduced (Dunker et al., 2020). The inset shows Southcentral Alaska sampling sites with the size of points scaled to sample size. Sample site names are prefaced with labels corresponding to genetic grouping as explained in the text: I – Southcentral I; II – Southcentral II, K – Kenai Peninsula. Eagle Lake (diamond) is a geographically distant site from Alaska with a pike population representative of non‐Beringian pike.

FIGURE 2

(a) Mean estimates of genetic diversity (Pi) calculated on a chromosome by chromosome approach. (b) Mean estimates of Tajima's D calculated on a chromosome by chromosome approach. Populations are colored to represent origin. Southcentral populations are representative of the introduced range of pike in Alaska.

FIGURE 3

Scatter plot showing F_ST (FST) values as a function of mean distance between populations. Comparisons within the introduced range are indicated as circles with those between Stormy Lake (Kenai Peninsula) and all other locations colored in blue. Pairwise comparisons with Antlen River are indicated by red triangles.

FIGURE 4

Admixture plots generated by NGSadmix of Alaska pike at K = 2 and K = 6. Sampling locations are subdivided by status (introduced vs. native) and then by geography, that is, Interior, Western Alaska, Kenai peninsular, then other Southcentral locations. Note that the classification of genetic clusters as Southcentral I vs. Southcentral II was based on allele sharing rather than geography (see Figure 1). Introduced populations were further subdivided, based on allele sharing, into either two genetic clusters (Southcentral I) or three genetic clusters (Southcentral II). Values of K were chosen based on the lowest log‐likelihood as implemented in NGSadmix software within ANGSD.

FIGURE 5

Discriminant Analysis of Principal Components (DAPC) of Alaska pike. (a) The largest division (K = 2) is shown. (b) The Bayesian information criterion (BIC) supported K = 8 genetic clusters of Alaska pike. (c) The Anderson Lake, Bulchitna Lake, Tukallah Lake, and Yentna River (Southcentral II) genetic cluster is further subdivided in a separate analysis of samples only in this cluster to K = 2.

FIGURE 6

Geographic distribution of genetic clusters of introduced Alaskan pike in Southcentral Alaska. The averages of individuals for posterior assignment to eight genetic clusters (K = 8) from Discriminant Analysis of Principal Components in Figure 5b across collection sites are presented as pie charts. Four genetic clusters are present in Southcentral Alaska; genetic cluster 2 is shared between Stormy Lake and Tiny Lake (Kenai sites) and Lake Clark and Lake Nerka (Western Alaska). Other genetic clusters are found in introduced pike only.

FIGURE 7

Individual phylogeny of pike sequenced in this study (Alaska and Eagle Lake, n = 358) with nodal support <75 not shown, ≥75 but less than 90 as light grey circles and ≥ 90 as black circles. Tip shapes and colors correspond to Figure 1. (a) The entire tree is pictured with colors of tips corresponding locations in Figure 1. (b) The subtree containing introduced pike from the Anchorage and Matanuska‐Susitna area is removed and colors are the same as the inset of Figure 1. (c) The Kenai Peninsula subtree is shown with colors matching the inset of Figure 1.

FIGURE 8

Placement of Antlen River pike. Additional sequence data from GenBank are analyzed with the RADseq from natural populations from this study. The whole‐genome sequence data (WGS) are indicated by triangles in the figure and RADseq by circles. The geographic origin of samples is indicated by color in the Region legend. (a) Principal component (PC) analysis of genetic variation showing the first two axes of variation. (b) Principal component analysis of genetic variation showing the first and third axes of variation. (c) Species tree from SVDQuartets. Nodal support is indicated on the tree.