Genetic Structure of the Blue Ridge Dusky Salamander (Desmognathus Orestes): Inferences From Allozymes, Mitochondrial Dna, and Behavior

Abstract

The plethodontid salamander Desmognathus orestes, a member of the D. ochrophaeus species complex, is distributed in southwestern Virginia, eastern Tennessee, and western North Carolina. Previous allozyme analyses indicate that D. orestes consists of two distinct groups of populations (D. orestes 'B' and D. orestes 'C') with extensive intergradation and probable gene flow between these two groups. Spatially varying allele frequencies can reflect historical associations, current gene flow, or a combination of population-level processes. To differentiate among these processes, we use multiple markers to further characterize divergence among populations of D. orestes and assess the degree of intergradation between D. orestes 'B' and D. orestes 'C', specifically investigating variation in allozymes, mitochondrial DNA (mtDNA), and reproductive behavior among populations. On a broad scale, the mtDNA genealogies reconstruct haplotype clades that correspond to the species identified from previous allozyme analyses. However, at a finer geographic scale, the distributions of the allozyme and mtDNA markers for D. orestes 'B' and D. orestes 'C' are discordant. MtDNA haplotypes corresponding to D. orestes 'B' are more broadly distributed across western North Carolina than predicted by allozyme data, and the region of intergradation with D. orestes 'C' indicates asymmetric gene flow of these markers. Asymmetric mating may contribute to observed discordance in nuclear versus cytoplasmic markers. Results support describing D. orestes as a single species and emphasize the importance of using multiple markers to examine fine-scale patterns and elucidate evolutionary processes affecting gene flow when making species-level taxonomic decisions.

Does Niche Conservatism Promote Speciation? A Case Study in North American Salamanders

“…Second, periods of allopatric isolation have been accompanied by the evolution of intrinsic reproductive isolation, at least in some lineages. In courtship encounters staged between sister species and genetically divergent populations of Plethodon and Desmognathus, those encounters between individuals from populations that are geographically isolated in different mountain ranges exhibit reduced insemination rates when compared to those involving populations from the same geographic isolate (Tilley et al 1990;Reagan 1992;Mead et al 2001). Sister species within Plethodon and Desmognathus also show divergence in male courtship behaviors and pheromones that contribute to mate recognition and successful courtship (Reagan 1992;Houck et al 1998;Rollman et al 1999Rollman et al , 2000Verrell and Mabry 2000;Mead and Verrell 2002).…”

“…Many closely related species are endemic to geographically disjunct montane areas in the eastern North American temperate zone (Highton 1995;Tilley and Mahoney 1996;Crespi et al 2003), where there has been a dramatic history of climate-driven forest contraction, fragmentation, and expansion since the Miocene (Delcourt and Delcourt 1988;Webb and Bartlein 1992;Webb et al 1995;Jansson and Dynesius 2002). Geographic patterns of genetic variation have been described across hundreds of populations and geographic boundaries of many cryptic species have been studied (e.g., Tilley and Schwertdfeger 1981;Karlin and Guttman 1986;Highton et al 1989;Highton 1995Highton , 1997Highton , 1999Tilley and Mahoney 1996;Bonett 2000;Highton and Peabody 2000;Tilley 2000;Mead et al 2001;Anderson and Tilley 2003;Weisrock et al 2005;Weisrock and Larson 2006). In addition, recent phylogenetic analyses provide a robust framework for identifying extant sister species (Mahoney 2001;Rissler and Taylor 2003;Chippindale et al 2004;Kozak et al 2005Kozak et al , 2006Wiens et al 2006).…”

Genetic diversity in a narrowly endemic, recently described dusky salamander, Desmognathus folkertsi, from the southern Appalachian Mountains

“…imitator, each of these desmognathan species, however, has a considerably larger geographic distribution. Desmognathus folkertsi exhibited 4.29% divergence from populations of D. quadramaculatus, a level typical of sequence divergence between desmognathan species (Mead et al 2001). Many freshwater species, including amphibians and fishes, exhibit patterns of genetic diversity that can be explained by historical drainage connections (Mayden 1988;Burridge et al 2006;Jones et al 2006;Kozak et al 2006b).…”

“…For amphibians, especially lungless salamanders (Plethodontidae), morphologically cryptic species are common (Larson et al 1981;Wake et al 1983;Larson 1984;Carr 1996;Adams and Rohlf 2000;Highton and Peabody 2000;Camp et al 2002;Mueller et al 2004;Rissler and Apodaca 2007). As a consequence, many new species have been described from what had been previously believed to be single, geographically widespread species (Tilley and Mahoney 1996;Mead et al 2001;Parra-Olea and Wake 2001;Jockusch and Wake 2002;Martínez-Solano et al 2007). In light of declining amphibian species worldwide (Carey and Alexander 2003;Collins and Storfer 2003;Stokstad 2004;Stuart et al 2004;Ricketts et al 2005) and the ubiquity of their cryptic diversity, it is critical for researchers to understand geographic patterns of genetic diversity to ensure the conservation of unique evolutionary units (Frankel 1974;Cowling and Pressey 2001;Moritz 2002;Rissler et al 2006;Davis et al 2008;Gienapp et al 2008;Mace and Purvis 2008).…”

“…Other reported levels of divergence for desmognathan salamanders include 2.69% for D. monticola(Bonett et al 2007), andMead et al (2001) reported 3.29% for D. carolinensis, 0.95% for D. ochrophaeus, 2.80% for D. orestes, and 1.20% for D. imitator. Except for D. carolinensis and D.…”