Phylogenetic Evidence for a Major Reversal of Life-History Evolution in Plethodontid Salamanders

Abstract

Abstract. The transition from aquatic to terrestrial eggs is a key evolutionary change that has allowed vertebrates to successfully colonize and exploit the land. Although most amphibians retain the primitive biphasic life cycle (eggs deposited in water that hatch into free-living aquatic larvae), direct development of terrestrial eggs has evolved repeatedly and may have been critical to the evolutionary success of several amphibian groups. We provide the first conclusive evidence for evolutionary reversal of direct development in vertebrates. The family Plethodontidae (lungless salamanders) contains the majority of salamander species, including major radiations of direct developers. We reconstruct the higher level phylogenetic relationships of plethodontid salamanders using molecular and morphological data and use this phylogeny to examine the evolution of direct development. We show that the predominantly biphasic desmognathines, previously considered the sister group of other plethodontids, are nested inside a group of directdeveloping species (Plethodontini) and have re-evolved the aquatic larval stage. Rather than being an evolutionary dead end, the reversal from direct developing to biphasic life history may have helped communities in eastern North America to achieve the highest local diversity of salamander species in the world.

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

“…The proximal cause for this phenomenon is likely related to the presence of large, slowly dividing cells and reduced metabolic rates in species with very large genomes, which retard the rapid developmental changes demanded during amphibian metamorphosis. From this perspective, the relatively small genomes of Desmognathus may have enabled the homoplasic evolution of larvae in this genus (Chippindale et al 2004, Mueller et al 2004. The spelerpines and Hemidactylium, all of which have a larval stage, also have relatively small genomes ( Figure 6).…”

Limb regeneration in a direct‐developing terrestrial salamander, Bolitoglossa ramosi (Caudata: Plethodontidae)

“…They also undergo direct development, where the embryos develop to an adult without any larval stages (Chippindale, Bonett, Baldwin, & Wiens, 2004). …”

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

“…In particular, it emphasizes larval structures that were previously reported as ''missing'' from the direct-developing ontogeny of P. cinereus (Dent, 1942), but that are apparently re-gained in metamorphosing species of the genus Desmognathus (Chippindale et al, 2004). Further comparative embryological research may shed light on the apparent re-acquisition of these larval features in metamorphosing species of Desmognathus.…”

“…This cranial bone is absent from the directdeveloping Desmognathus aeneus but is found in the metamorphosing D. quadramaculatus (Marks, 2000) and other metamorphosing and paedomorphic plethodontids (Wake, 1966). The appearance of this larval dermal bone in metamorphosing plethodontids suggests that a precursor to the element existed in direct-developing ancestors of Desmognathus (see Chippindale et al, 2004), yet this larval bone is apparently absent in the direct-developing out-group represented by Plethodon cinereus.…”

“…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.…”