A Nuclear DNA Perspective on Delineating Evolutionarily Significant Lineages in Polyploids: The Case of the Endangered Shortnose Sturgeon (Acipenser brevirostrum)

The shortnose sturgeon, Acipenser brevirostrum, oft considered a phylogenetic relic, is listed as an “endangered species threatened with extinction” in the US and “Vulnerable” on the IUCN Red List. Effective conservation of A. brevirostrum depends on understanding its diversity and evolutionary processes, yet challenges associated with the polyploid nature of its nuclear genome have heretofore limited population genetic analysis to maternally inherited haploid characters. We developed a suite of polysomic microsatellite DNA markers and characterized a sample of 561 shortnose sturgeon collected from major extant populations along the North American Atlantic coast. The 181 alleles observed at 11 loci were scored as binary loci and the data were subjected to multivariate ordination, Bayesian clustering, hierarchical partitioning of variance, and among-population distance metric tests. The methods uncovered moderately high levels of gene diversity suggesting population structuring across and within three metapopulations (Northeast, Mid-Atlantic, and Southeast) that encompass seven demographically discrete and evolutionarily distinct lineages. The predicted groups are consistent with previously described behavioral patterns, especially dispersal and migration, supporting the interpretation that A. brevirostrum exhibit adaptive differences based on watershed. Combined with results of prior genetic (mitochondrial DNA) and behavioral studies, the current work suggests that dispersal is an important factor in maintaining genetic diversity in A. brevirostrum and that the basic unit for conservation management is arguably the local population

Microsatellite allele (a.k.a. pseudodominant locus) counts, percentage of loci (alleles) polymorphic, number of private alleles, and number of common alleles across all loci for shortnose sturgeon (<i>Acipenser brevirostrum</i>) populations across the North American range.

<p>The analyses were conducted on the binary character matrix.</p>1<p>Number of different fragments.</p>2<p>Number of bands unique to a single population.</p>3<p>Number of common alleles with frequency ≤25%.</p><p>Microsatellite allele (a.k.a. pseudodominant locus) counts, percentage of loci (alleles) polymorphic, number of private alleles, and number of common alleles across all loci for shortnose sturgeon (<i>Acipenser brevirostrum</i>) populations across the North American range.</p

Combined graphical representation of sequential principal coordinates (scatter plots) and STRUCTURE (histograms) analyses of 561 shortnose sturgeon (<i>Acipenser brevirostrum</i>) surveyed at 11 polysomic microsatellite DNA loci.

<p>For the STRUCTURE histograms, each individual is represented by a single vertical bar, broken into <i>k</i> colored segments, the length of which is proportional to the membership fraction in each of the <i>k</i> clusters. Black lines partition the river samples. A) Northeast region collections; B) Mid-Atlantic region collections; C) Southeast region collections.</p

Assignment to three groupings of origin model consisting of 17 collections of shortnose sturgeon (<i>Acipenser brevirostrum</i>) surveyed at 11 polysomic microsatellite DNA markers.

<p>Mis-assigned individuals are distributed vertically.</p><p>Assignment to three groupings of origin model consisting of 17 collections of shortnose sturgeon (<i>Acipenser brevirostrum</i>) surveyed at 11 polysomic microsatellite DNA markers.</p

Pair-wise Φ_PT among putative shortnose sturgeon populations (above diagonal) and estimates of the effective number of migrants per generation, <i>N_em</i> (below diagonal), for 17 collections of shortnose sturgeon (<i>Acipenser brevirostrum</i>) surveyed at 11 polysomic microsatellite loci.

<p>Non-significant pair-wise Φ_PT probability values (H₀ = No genetic difference among populations; Φ_PT = 0) based on 10,000 permutations values are in bold italics. Cape Fear River sample is not included due to inadequate sample size.</p><p>Pair-wise Φ_PT among putative shortnose sturgeon populations (above diagonal) and estimates of the effective number of migrants per generation, <i>N_em</i> (below diagonal), for 17 collections of shortnose sturgeon (<i>Acipenser brevirostrum</i>) surveyed at 11 polysomic microsatellite loci.</p

Map of a portion of the North American Atlantic Coast depicting the general location and sample size of 17 river and estuary collections of shortnose sturgeon (<i>Acipenser brevirostrum</i>) surveyed at 11 polysomic microsatellite DNA loci.

<p>Sample sizes are in parentheses.</p

Hierarchical AMOVA results for biogeographically relevant groups among 17 collections of shortnose sturgeon (<i>Acipenser brevirostrum</i>) surveyed at 11 polysomic microsatellite DNA markers.

<p>Hierarchical AMOVA results for biogeographically relevant groups among 17 collections of shortnose sturgeon (<i>Acipenser brevirostrum</i>) surveyed at 11 polysomic microsatellite DNA markers.</p

Combined graphical representation of principal coordinates (scatter plot) and STRUCTURE (histogram) analyses of 561 shortnose sturgeon (<i>Acipenser brevirostrum</i>) from 17 locations along the North American coast, surveyed at 11 polysomic microsatellite DNA loci.

<p>For the STRUCTURE histograms, each individual is represented by a single vertical bar, broken into <i>k</i> colored segments, the length of which is proportional to the membership fraction in each of the <i>k</i> clusters. Black lines partition the river samples.</p

Results of independent multidimensional scaling analyses of pair-wise a) Φ_PT (nuclear DNA; Table 4, this study) and b) Φ_ST (mitochondrial DNA; Table 5 of Wirgin et al. [30]) matrices for 14 <i>Acipenser brevirostrum</i> collections that are in common between the two studies.

<p>Results of independent multidimensional scaling analyses of pair-wise a) Φ_PT (nuclear DNA; <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0102784#pone-0102784-t004" target="_blank">Table 4</a>, this study) and b) Φ_ST (mitochondrial DNA; Table 5 of Wirgin et al. <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0102784#pone.0102784-Kruskal1" target="_blank">[30]</a>) matrices for 14 <i>Acipenser brevirostrum</i> collections that are in common between the two studies.</p