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

Abstract

BackgroundDisentangling evolutionary shifts in developmental timing (heterochony) is dependent upon accurate estimates of ancestral patterns. However, many classic assessments of heterochronic patterns predate robust phylogenetic hypotheses and methods for trait reconstruction, and therefore may have been polarized with untested ‘primitive’ conditions. Here we revisit the heterochronic modes of development that underlie the evolution of metamorphosis, maturation, and paedomorphosis in plethodontid salamanders. We focus on the tribe Spelerpini, which is a diverse clade that exhibits tremendous variation in timing of metamorphosis and maturation, as well as multiple independent instances of larval form paedomorphosis. Based on morphology and biogeography, early investigators concluded that the most recent common ancestors of plethodontids, and also spelerpines, were large salamanders, with very long larval periods and late maturation times. This prevailing assumption influenced subsequent heterochronic assessments, which concluded that most modern spelerpines (with shorter larval periods) were derived through multiple independent accelerations in larval development. It was also concluded that most occurrences of larval form paedomorphosis in this clade resulted from progenesis (acceleration of gonadal development relative to metamorphosis).ResultsBy reconstructing the time to metamorphosis on a molecular-based phylogeny of plethodontids, we find that ancestral spelerpines likely had relatively shorter larval periods than previously proposed. Taken together with the credibility interval from our ancestral state estimation we show that very long larval periods are likely derived decelerations, only a few lineages have undergone appreciable accelerations in metamorphic timing, and the remaining taxa have lower probabilities of being different than the ancestral condition (possibly due to stasis). Reconstructing maturation age across nodes concomitant with the evolution of larval form paedomorphosis in one large radiation does not show clear evidence of progenesis, but more likely indicates a case of neoteny (delayed metamorphosis).ConclusionsThis study demonstrates cases in plethodontid salamanders where phylogenetic-based character reconstructions reject previously hypothesized ancestral life history conditions. As a result, several prior hypotheses of heterochronic evolution in this family are reversed.

Transposons, Genome Size, and Evolutionary Insights in Animals

“…In urodeles the increase in the genome allowed the transition from a biphasic life cycle to increasingly frequent cases of paedomorphosis or even to obliged neoteny [Gregory, 2002a[Gregory, , 2005. In plethodontids it was observed that the ancestral forms probably had a shorter larval period than current forms [Bonett et al, 2014], implying a co-evolution between genome increase and paedomorphosis/neoteny. The progressive development of paedomorphosis and neoteny characterizes also the evolution of the current lungfishes harboring very large genomes [Joss, 2006].…”

How Metamorphosis Is Different in Plethodontids: Larval Life History Perspectives on Life-Cycle Evolution

“…Biphasic life cycles occur in three different clades (the subfamily Spelerpinae, Hemidactylium and some Desmognathus ). Several spelerpine lineages express obligate paedomorphosis (Bonett et al 2014a,b), but facultative paedomorphosis is uncommon. Direct-developing lineages collectively represent the greatest diversity of salamanders (Wake and Hanken 1996), and range from western North America into South America, with relict species in the Mediterranean and Asia (Dunn 1926; Wake 1966; Min et al 2005).…”

“…Analyses based on molecular phylogenies have indicated that life-cycle evolution is reversible, however, with complex life cycles secondarily derived from direct-developing and paedomorphic ancestors (Titus and Larson 1996; Chippindale et al 2004; Mueller et al 2004; Bonett et al 2014a,b). With regard to direct development, there are either (1) multiple episodes of direct development from biphasic ancestors, or (2) re-evolution of free-living larvae from direct-developing ancestors, including the possibility that a direct-developing life cycle could be the ancestral life cycle for plethodontids (Chippindale et al 2004; Mueller et al 2004).…”

“…With regard to direct development, there are either (1) multiple episodes of direct development from biphasic ancestors, or (2) re-evolution of free-living larvae from direct-developing ancestors, including the possibility that a direct-developing life cycle could be the ancestral life cycle for plethodontids (Chippindale et al 2004; Mueller et al 2004). Indeed, ancestral-state reconstruction suggests the possibility that the ancestral plethodontid was direct developing (Bonett et al 2014b). Also, over a much shorter time frame there is evidence of a reversal from paedomorphosis to a biphasic life cycle in one clade of Eurycea from the Edwards Plateau of central Texas (Bonett et al 2014a).…”

Persistent Plethodontid Themes: Species, Phylogenies, and Biogeography

“…This is a serious problem for the Beachy-Bruce (1992) hypothesis that lunglessness is a rheotropic adaptation to larval life (an extension of the older idea: lungs would buoy the larvae into flowing water, causing them to be swept away). Desmognathus is deeply nested, not sister to all remaining plethodontids, and Bonett et al (2014) argued that direct development may well have been ancestral for Plethodontidae. Finally, based on arguments by and Shen et al (2016), plethodontids might have arisen in northwestern North America, not Appalachia, or it is at least as probable as Appalachia.…”