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.
Highlights
IntroductionDisentangling evolutionary shifts in developmental timing (heterochony) is dependent upon accurate estimates of ancestral patterns
Disentangling evolutionary shifts in developmental timing is dependent upon accurate estimates of ancestral patterns
Following Ryan and Bruce [26] and other studies [8], we use the terms neoteny and progenesis primarily to refer to somatic deceleration and reproductive acceleration, respectively, which are processes that can result in larval form paedomorphosis
Summary
Disentangling evolutionary shifts in developmental timing (heterochony) is dependent upon accurate estimates of ancestral patterns. Based on morphology and biogeography, early investigators concluded that the most recent common ancestors of plethodontids, and 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. Conducting comparative analyses of heterochronic patterns can be challenging and confounded This is because these analyses rely on knowledge of the timing of developmental events for multiple taxa, an understanding of their phylogenetic relationships, and methods to deduce ancestral patterns of development [11,12,13,14,15,16,17,18,19]. This suggests that some non-phylogenetically (or non-paleontologically) polarized heterochronic assessments may need to be reconsidered in light of more refined phylogenetic hypotheses and/or ancestral state reconstruction methods
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