Dataset Information

Developmental basis of evolutionary lung loss in plethodontid salamanders.

ABSTRACT: One or more members of four living amphibian clades have independently dispensed with pulmonary respiration and lack lungs, but little is known of the developmental basis of lung loss in any taxon. We use morphological, molecular, and experimental approaches to examine the Plethodontidae, a dominant family of salamanders, all of which are lungless as adults. We confirm an early anecdotal report that plethodontids complete early stages of lung morphogenesis: Transient embryonic lung primordia form but regress by apoptosis before hatching. Initiation of pulmonary development coincides with expression of the lung-specification gene Wnt2b in adjacent mesoderm, and the lung rudiment expresses pulmonary markers Nkx2.1 and Sox9. Lung developmental-genetic pathways are at least partially conserved despite the absence of functional adult lungs for at least 25 and possibly exceeding 60 million years. Adult lung loss appears associated with altered expression of signaling molecules that mediate later stages of tracheal and pulmonary development.

SUBMITTER: Lewis ZR

PROVIDER: S-EPMC9385146 | biostudies-literature | 2022 Aug

REPOSITORIES: biostudies-literature

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Developmental basis of evolutionary lung loss in plethodontid salamanders.

Lewis Zachary R ZR Kerney Ryan R Hanken James J

Science advances 20220817 33

One or more members of four living amphibian clades have independently dispensed with pulmonary respiration and lack lungs, but little is known of the developmental basis of lung loss in any taxon. We use morphological, molecular, and experimental approaches to examine the Plethodontidae, a dominant family of salamanders, all of which are lungless as adults. We confirm an early anecdotal report that plethodontids complete early stages of lung morphogenesis: Transient embryonic lung primordia for ...[more]

PMID: 35977024

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Project description:BACKGROUND:Disentangling 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). RESULTS:By 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). CONCLUSIONS:This 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.

Project description:Plethodontid salamanders are diverse and widely distributed taxa and play critical roles in ecosystem processes. Due to salamander use of structurally complex habitats, and because only a portion of a population is available for sampling, evaluation of sampling designs and estimators is critical to provide strong inference about Plethodontid ecology and responses to conservation and management activities. We conducted a simulation study to evaluate the effectiveness of multi-scale and hierarchical single-scale occupancy models in the context of a Before-After Control-Impact (BACI) experimental design with multiple levels of sampling. Also, we fit the hierarchical single-scale model to empirical data collected for Oregon slender and Ensatina salamanders across two years on 66 forest stands in the Cascade Range, Oregon, USA. All models were fit within a Bayesian framework. Estimator precision in both models improved with increasing numbers of primary and secondary sampling units, underscoring the potential gains accrued when adding secondary sampling units. Both models showed evidence of estimator bias at low detection probabilities and low sample sizes; this problem was particularly acute for the multi-scale model. Our results suggested that sufficient sample sizes at both the primary and secondary sampling levels could ameliorate this issue. Empirical data indicated Oregon slender salamander occupancy was associated strongly with the amount of coarse woody debris (posterior mean = 0.74; SD = 0.24); Ensatina occupancy was not associated with amount of coarse woody debris (posterior mean = -0.01; SD = 0.29). Our simulation results indicate that either model is suitable for use in an experimental study of Plethodontid salamanders provided that sample sizes are sufficiently large. However, hierarchical single-scale and multi-scale models describe different processes and estimate different parameters. As a result, we recommend careful consideration of study questions and objectives prior to sampling data and fitting models.

Dataset Information

Developmental basis of evolutionary lung loss in plethodontid salamanders.

Publications

Developmental basis of evolutionary lung loss in plethodontid salamanders.

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