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

Abstract

A phylogeny and timescale derived from analyses of multilocus nuclear DNA sequences for Holarctic genera of plethodontid salamanders reveal them to be an old radiation whose common ancestor diverged from sister taxa in the late Jurassic and underwent rapid diversification during the late Cretaceous. A North American origin of plethodontids was followed by a continentalwide diversification, not necessarily centered only in the Appalachian region. The colonization of Eurasia by plethodontids most likely occurred once, by dispersal during the late Cretaceous. Subsequent diversification in Asia led to the origin of Hydromantes and Karsenia, with the former then dispersing both to Europe and back to North America. Salamanders underwent rapid episodes of diversification and dispersal that coincided with major global warming events during the late Cretaceous and again during the Paleocene-Eocene thermal optimum. The major clades of plethodontids were established during these episodes, contemporaneously with similar phenomena in angiosperms, arthropods, birds, and mammals. Periods of global warming may have promoted diversification and both inter-and transcontinental dispersal in northern hemisphere salamanders by making available terrain that shortened dispersal routes and offered new opportunities for adaptive and vicariant evolution.historical biogeography ͉ paleogeography ͉ Plethodontidae dispersal ͉ salamander phylogeny ͉ phylogeny P lethodontidae, the most speciose family of salamanders, is also the most differentiated in morphology, ecology, and behavior. The family includes Ϸ68% of the extant described species of caudate amphibians (1). New analyses of mtDNA, nuclear DNA, and morphology (2-6) have achieved consensus on many aspects of phylogenetic relationships, but unresolved conflicts remain. The disjunct and highly asymmetric Holarctic distribution of the family, with Ϸ98% of the species in the Americas and a few in the Mediterranean region, has long been a biogeographic puzzle (7-9), with the debate centered on the timing and route of colonization of Eurasia (reinvigorated with the recent discovery of Karsenia, the first East Asian plethodontid; ref. 10

Cytogenetic analysis of the Asian Plethodontid salamander, Karsenia koreana: Evidence for karyotypic conservation, chromosome repatterning, and genome size evolution

“…The recent discovery of an Asian plethodontid from South Korea, Karsenia koreana (Min et al 2005), has helped to clarify the phylogenetic relationships and historical biogeography of Holarctic plethodontids. Molecular phylogenetic studies of these species have led to a reassessment of their taxonomy and phylogenetic relationships (Mueller et al 2004, Wiens et al 2005Vieites et al 2007). In conflict with traditional taxonomy (Wake 1966), molecular evidence from complete mitochondrial genomes and multiple nuclear loci identifies two distinct subfamilies: Plethodontinae and Hemidactyliinae ( Figure 1) (Vieites et al 2007).…”

“…Molecular phylogenetic studies of these species have led to a reassessment of their taxonomy and phylogenetic relationships (Mueller et al 2004, Wiens et al 2005Vieites et al 2007). In conflict with traditional taxonomy (Wake 1966), molecular evidence from complete mitochondrial genomes and multiple nuclear loci identifies two distinct subfamilies: Plethodontinae and Hemidactyliinae ( Figure 1) (Vieites et al 2007). This study found that Karsenia is most closely related to members of the subfamily Plethodontinae.…”

“…Hydromantes. The common ancestor of Karsenia and Hydromantes is estimated to have diverged from other plethodontids in the Late Cretaceous, and these two diverged from each other õ69 million years ago (Mya) (Vieites et al 2007).…”

“…Not only do species of Sg. Hydromantes have the largest genome sizes of any terrestrial salamanders (Green & Sessions 2007), but the clade also experienced the fastest rates of molecular evolution among Holarctic plethodontids (Vieites et al 2007). These unusual features of salamanders of the Sg.…”

Embryonic Staging Table for a Direct‐Developing Salamander, Plethodon cinereus (Plethodontidae)

“…Development of the genus Plethodon is particularly interesting given recent phylogenetic studies, which consistently nest the super-genus Desmognathus within a larger direct-developing clade that includes Plethodon (Chippindale et al, 2004;Mueller et al, 2004;Kozak et al, 2005Kozak et al, , 2009Macey, 2005;Vieites et al, 2007). These studies strongly suggest a reacquisition of larvae within the genus Desmognathus (see also Wake et al, 2011;Fig.…”