The importance of comparative phylogeography in diagnosing introduced species: a lesson from the seal salamander, Desmognathus monticola

Abstract

Background: In most regions of the world human influences on the distribution of flora and fauna predate complete biotic surveys. In some cases this challenges our ability to discriminate native from introduced species. This distinction is particularly critical for isolated populations, because relicts of native species may need to be conserved, whereas introduced species may require immediate eradication. Recently an isolated population of seal salamanders, Desmognathus monticola, was discovered on the Ozark Plateau, approximately 700 km west of its broad continuous distribution in the Appalachian Mountains of eastern North America. Using Nested Clade Analysis (NCA) we test whether the Ozark isolate results from population fragmentation (a natural relict) or long distance dispersal (a human-mediated introduction).

Results: Despite its broad distribution in the Appalachian Mountains, the primary haplotype diversity of D. monticola is restricted to less than 2.5% of the distribution in the extreme southern Appalachians, where genetic diversity is high for other co-distributed species. By intensively sampling this genetically diverse region we located haplotypes identical to the Ozark isolate. Nested Clade Analysis supports the hypothesis that the Ozark population was introduced, but it was necessary to include haplotypes that are less than or equal to 0.733% divergent from the Ozark population in order to arrive at this conclusion. These critical haplotypes only occur in < 1.2% of the native distribution and NCA excluding them suggest that the Ozark population is a natural relict.

Conclusion: Our analyses suggest that the isolated population of D. monticola from the Ozarks is not native to the region and may need to be extirpated rather than conserved, particularly because of its potential negative impacts on endemic Ozark stream salamander communities. Diagnosing a species as introduced may require locating nearly identical haplotypes in the known native distribution, which may be a major undertaking. Our study demonstrates the importance of considering comparative phylogeographic information for locating critical haplotypes when distinguishing native from introduced species.

Figure 1

Distribution and species richness of Desmognathus. A. Species richness of the genus Desmognathus, with the highest species diversity in the southern Appalachian Mountains. Note: Desmognathus are absent from the Ozark Plateau. B. Geographic distribution of Desmognathus monticola outlined in blue overlaid on an elevation map of eastern North America. The isolated population of D. monticola in the Ozarks is designated with a blue star. Inset is a photograph of an adult D. monticola from the Ozarks.

Figure 2

Geographic distribution and unrooted statistical parsimony networks for D. monticola haplotypes. The large majority of the geographic distribution contains only a few haplotypes (K, L, M, N, O, & P). The Ozark haplotype (F, red) occurs in the southern Appalachians of northern Georgia amongst a great diversity of related haplotypes. Labels on the network indicate the haplotype and the number of counties where it was found (sizes of circles are also drawn proportional to this number). Colors of haplotypes correspond to pie diagrams on the map and show the frequency of haplotyope in each county sampled. Black dots on haplotype network indicate hypothetical unsampled haplotypes.

Figure 3

Graphical summary of the nested haplotype structure and NCA. Individual haplotypes are listed across the top, with increasingly more inclusive nested groups extending to the bottom. Interior haplotypes/nested groups are depicted in bold italics. Significant D_C, D_N, and I-T values are reported. Distances that are significantly small or large are indicated with S or L, respectively. The path taken through the most recent version of the inference key is shown; RGF, restricted gene flow; PF, past fragmentation; LDC, long-distance colonization; RE w/PF, range expansion coupled with past fragmentation. NCA results directly relevant to the diagnosis of the Ozark population (haplotype F) are highlighted in blue.

Figure 4

Percent divergence of Appalachian haplotypes to the Ozark population and their geographic distribution. Inset graph depicts the % sequence of the Appalachian haplotypes to the Ozark population and the % of the area of the distribution that they occur. The map shows the genetic landscape of haplotypes in relation to their divergence from the Ozark population. Note that it is necessary to include haplotypes that are ≤ 0.733% divergent from the Ozark population in order to diagnose it as introduced.