Evolution of Paedomorphosis in Plethodontid Salamanders: Ecological Correlates and Re-Evolution of Metamorphosis

Abstract

Life-history modes can profoundly impact the biology of a species, and a classic example is the dichotomy between metamorphic(biphasic) and paedomorphic (permanently aquatic) life-history strategies in salamanders. However, despite centuries of research on this system, several basic questions about the evolution of paedomorphosis in salamanders have not been addressed. Here, we use a nearly comprehensive, time-calibrated phylogeny of spelerpine plethodontids to reconstruct the evolution of paedomorphosis and to test if paedomorphosis is (1) reversible; (2) associated with living in caves; (3) associated with relatively dry climatic conditions on the surface; and (4) correlated with limited range size and geographic dispersal. We find that paedomorphosis arose multiple times in spelerpines. We also find evidence for re-evolution of metamorphosis after several million years of paedomorphosis in a lineage of Eurycea from the Edwards Plateau region of Texas. We also show for the first time using phylogenetic comparative methods that paedomorphosis is highly correlated with cave-dwelling, arid surface environments, and small geographic range sizes, providing insights into both the causes and consequences of this major life history transition. K E Y W O R D S :Amphibians, biogeography, climate, development, life history, phylogeny.

Larval masquerade: a new species of paedomorphic salamander (Caudata: Plethodontidae: Eurycea) from the Ouachita Mountains of North America

“…Outgroups included other representatives from the "Interior Highland clade" (E. tynerensis and E. spelaea), all other major lineages of Eurycea (E. bislineata, E. longicauda, E. neotenes, and E. quadridigitata), and a distant spelerpine outgroup (Pseudotriton ruber; Bonett et al 2014). Sequences were edited and aligned using Sequencher v4.8 (Gene Codes, Ann Arbor, MI).…”

“…Highton 1989;Chippindale et al 2000;Garcia-Paris et al 2000;Jockusch et al 2002). Plethodontids are known to exhibit a wide diversity of life histories and developmental modes (Wake 1966;Chippindale et al 2004;Mueller et al 2004;Bonett et al 2014), but ecologically and developmentally distinct new species are extremely rare, especially within North America, which has been extensively surveyed (Dunn 1926;Highton 1989;Camp et al 2009). …”

“…1). While most spelerpines have a biphasic (metamorphic) life history, typical of amphibians, several members of this clade display paedomorphosis (Wake 1966;Ryan & Bruce 2000;Bonett et al 2014), the phenomenon where adults retain ancestral juvenile characteristics throughout life (e.g. gills, tailfin, larval throat structure; Duellman & Trueb 1986).…”

“…gills, tailfin, larval throat structure; Duellman & Trueb 1986). Paedomorphosis in spelerpines has likely evolved independently in the Ozark Plateau, Edwards Plateau, Cumberland Plateau, and Gulf Coastal Plain (Wake 1966;Niemiller et al 2008;Bonett et al 2014). However, despite the Ouachita Mountains being a major biogeographic feature of eastern North America, the only spelerpine known to occur there is the widespread metamorphic Eurycea multiplicata.…”

The importance of phenotypic diversity in conservation: Resilience of palmate newt morphotypes after fish removal in Larzac ponds (France)

“…This is a crucial pattern to determine the value of conservation efforts for maintaining such uncommon or endangered phenotypes. Moreover, studying the potential for the re-expression of the paedomorphs after their extinction would then also allow a better understanding of the evolution of facultative paedomorphosis across environmental pressures (see also Bonett et al 2014). …”