Investigating the effects of Pleistocene events on genetic divergence within Richardsonius balteatus, a widely distributed western North American minnow

Abstract

Background: Biogeographers seek to understand the influences of global climate shifts and geologic changes to the landscape on the ecology and evolution of organisms. Across both longer and shorter timeframes, the western North American landscape has experienced dynamic transformations related to various geologic processes and climatic oscillations, including events as recently as the Last Glacial Maximum (LGM; ~20 Ka) that have impacted the evolution of the North American biota. Redside shiner is a cyprinid species that is widely distributed throughout western North America. The species' native range includes several well-documented Pleistocene refugia. Here we use mitochondrial DNA sequence data to assess phylogeography, and to test two biogeographic hypotheses regarding post-glacial colonization by redside shiner: 1) Redside shiner entered the Bonneville Basin at the time of the Bonneville Flood (Late Pleistocene; 14.5 Ka), and 2) redside shiner colonized British Columbia post-glacially from a single refugium in the Upper Columbia River drainage.

Results: Genetic diversification in redside shiner began in the mid to late Pleistocene, but was not associated with LGM. Different clades of redside shiner were distributed in multiple glacial age refugia, and each clade retains a signature of population expansion, with clades having secondary contact in some areas.

Conclusions: Divergence times between redside shiner populations in the Bonneville Basin and the Upper Snake/Columbia River drainage precedes the Bonneville Flood, thus it is unlikely that redside shiner invaded the Bonneville Basin during this flooding event. All but one British Columbia population of redside shiner are associated with the Upper Columbia River drainage with the lone exception being a population near the coast, suggesting that the province as a whole was colonized from multiple refugia, but the inland British Columbia redside shiner populations are affiliated with a refugium in the Upper Columbia River drainage.

Figure 1

Distribution map for R. balteatus. The dashed lines represent subspecies distribution boundaries. Circles represent sampling localities, and are color coded according to clade: Bonneville/Upper Snake (red), Northern Inland (yellow), and Pacific Northwestern lineages (blue). Population abbreviations correspond to those listed in Table 1. Six populations show a mixture of haplotypes, and the proportions are represented as pie charts. Documented Pleistocene refugia and major rivers are also labeled.

Figure 2

Redside Shiner Phylogeny. Phylogeny showing three major clades of redside shiner. Maximum likelihood bootstrap support values are listed above branches, and Bayesian posterior probabilities are listed below branches. The three clades are expanded for viewing in Figures 3, 4 and 5.

Figure 3

Pacific Northwestern Lineages. Phylogeny showing the relationships of the Pacific Northwestern lineages. Numbers above branches represent ML bootstrap values, and numbers below are posterior probabilities. Taxa are labeled with a two-letter population abbreviation (see Table 1) followed by individual LVT ID numbers. The shaded box on the left illustrates the section of the overall phylogeny that is enlarged.

Figure 4

Bonneville Basin/Upper Snake Clade. Phylogeny showing the relationships of individuals from the Bonneville Basin/Upper Snake River drainages. Numbers above branches represent ML bootstrap values, and numbers below are posterior probabilities. Taxa are labeled with a two-letter population abbreviation (see Table 1) followed by individual LVT ID numbers. The shaded box on the left illustrates the section of the overall phylogeny that is enlarged.

Figure 5

Northern Inland Clade. Phylogeny showing the relationships of individuals from the Upper Columbia drainages (including the lower Snake River) and inland British Columbia. Numbers above branches represent ML bootstrap values, and numbers below are posterior probabilities. Taxa are labeled with a two-letter population abbreviation (see Table 1) followed by individual LVT ID numbers. The shaded box on the left illustrates the section of the overall phylogeny that is enlarged.

Figure 6

Redside shiner mtDNA haplotype network. Haplotype network showing the intraspecific genetic diversity for R. balteatus. Circles represent unique mtDNA haplotypes, and are color-coded corresponding to phylogenetic position. Circle size represents the number of individuals carrying each haplotype. Hash marks represent nucleotide base changes between haplotypes.

Figure 7

Divergence time estimates. Tree showing divergence time estimates for redside shiner clades. The Bonneville Clade contains two distinct clades, one corresponding to northern Bonneville/Upper Snake populations (N), and one corresponding to southern Bonneville populations (S). Mean divergence time estimates are listed above branches and 95% credible intervals are in parentheses below branches. All divergence time estimates are given in millions of years, and thus all intraspecific divergences are Pleistocene in age.

Figure 8

Skyline plots. Bayesian skyline plots showing the demographic history for each of the three clades of redside shiner. Black lines represent mean population sizes plotted over time, and blue lines represent 95% confidence intervals surrounding those means. All three clades show a signature of population expansion, albeit beginning at different times in the Pleistocene. The Northern Inland Clade shows the most recent (and most pronounced) expansion beginning ~50,000 years ago.