Rapid Diversification, Incomplete Isolation, and the "Speciation Clock" in North American Salamanders (Genus Plethodon): Testing the Hybrid Swarm Hypothesis of Rapid Radiation

Abstract

The history of life has been marked by several spectacular radiations, in which many lineages arise over a short period of time. A possible consequence of such rapid splitting in the recent past is that the intrinsic barriers that prevent gene flow between many species may have too little time to develop fully, leading to extensive hybridization among recently evolved lineages. The salamander genus Plethodon in eastern North America has been proposed as a possible example of this scenario, but without explicit statistical tests. In this paper, we present a nearly comprehensive phylogeny for the 45 extant species of eastern Plethodon, based on DNA sequences of mitochondrial (two genes, 1335 base pairs) and nuclear genes (two genes, up to 3481 base pairs). We then use this phylogeny to examine rates and patterns of diversification and hybridization. We find significantly rapid diversification within the glutinosus species group. Examining patterns of natural hybridization in light of the phylogeny shows considerable hybridization within this clade, including introgression between species that are morphologically distinct and distantly related. Reproductive isolation increases over time and may be very weak among the most recently diverged species. These results suggest that the origin of species and the evolution of intrinsic reproductive isolating mechanisms, rather than being synonymous, may be decoupled in some cases (i.e., rapid origin of lineages outstrips the “;speciation clock”). In contrast to the conclusions of a recent review of adaptive radiation and hybridization, we suggest that extensive hybridization sometimes may be a consequence, rather than a cause, of rapid diversification.

What are the consequences of combining nuclear and mitochondrial data for phylogenetic analysis? Lessons from Plethodonsalamanders and 13 other vertebrate clades

“…The separate data sets generally agree on the major clades (eastern, western) and species groups ( cinereus, wehrlei-welleri, glutinosus ) recognized in previous studies [e.g., [13,52,56,57]]. Nevertheless, the mtDNA and nucDNA conflict with each other at 34 of 51 nodes, and conflicts at 19 of the 34 discordant nodes are strongly supported by both data types (Table 1).…”

“…[52,53]] and mtDNA [e.g. [56]], whereas more recent studies have combined mtDNA and nucDNA data [e.g., [13,57]]. In general, these studies have yielded similar estimates of higher-level Plethodon phylogeny (e.g., most agree on a split between eastern and western species, and on the species groups in eastern North America).…”

“…However, there have been substantive disagreements between studies regarding some species-level relationships (e.g., within the cinereus group; [13]). Furthermore, all previous studies used relatively few nuclear loci (two or three; [13,57,61]). Here we obtain new data from five nuclear loci and combine these with existing data from four nuclear genes and three mitochondrial genes, and use these data to address Plethodon phylogeny and general questions about combining mtDNA and nucDNA in phylogenetic studies.…”

Rapid diversification and dispersal during periods of global warming by plethodontid salamanders

“…Plethodon and Desmognathus are the most speciose genera among the Plethodontinae, with centers of diversity in the Appalachian Mountains. However, these are relatively recent and rapid radiations, with high lineage accumulation in recent geologic times (6,37), probably favored by the uplift of Appalachia in the Cenozoic and the reacquisition of aquatic larvae by desmognathines (2). The high species diversity in Appalachia corresponds mainly to recent radiations, but the ancestor of the family could have been distributed anywhere in North America.…”

Heterochrony repolarized: a phylogenetic analysis of developmental timing in plethodontid salamanders

“…Rag1 was chosen because it is a conserved nuclear locus that was already available for most taxa included in this study, and provides a close approximation to the topologies and branch lengths of previously reconstructed salamander phylogenies [25,28,34,39-43]. The sequences were primarily derived from previous phylogenetic datasets of plethodontids [28], spelerpines [25], Plethodon [44], and additional sequences for nine species from the genus Desmognathus that we collected for this study (Additional file 2). …”