Dataset Information

LTR retrotransposons contribute to genomic gigantism in plethodontid salamanders.

ABSTRACT: Among vertebrates, most of the largest genomes are found within the salamanders, a clade of amphibians that includes 613 species. Salamander genome sizes range from ~14 to ~120 Gb. Because genome size is correlated with nucleus and cell sizes, as well as other traits, morphological evolution in salamanders has been profoundly affected by genomic gigantism. However, the molecular mechanisms driving genomic expansion in this clade remain largely unknown. Here, we present the first comparative analysis of transposable element (TE) content in salamanders. Using high-throughput sequencing, we generated genomic shotgun data for six species from the Plethodontidae, the largest family of salamanders. We then developed a pipeline to mine TE sequences from shotgun data in taxa with limited genomic resources, such as salamanders. Our summaries of overall TE abundance and diversity for each species demonstrate that TEs make up a substantial portion of salamander genomes, and that all of the major known types of TEs are represented in salamanders. The most abundant TE superfamilies found in the genomes of our six focal species are similar, despite substantial variation in genome size. However, our results demonstrate a major difference between salamanders and other vertebrates: salamander genomes contain much larger amounts of long terminal repeat (LTR) retrotransposons, primarily Ty3/gypsy elements. Thus, the extreme increase in genome size that occurred in salamanders was likely accompanied by a shift in TE landscape. These results suggest that increased proliferation of LTR retrotransposons was a major molecular mechanism contributing to genomic expansion in salamanders.

SUBMITTER: Sun C

PROVIDER: S-EPMC3318908 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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LTR retrotransposons contribute to genomic gigantism in plethodontid salamanders.

Sun Cheng C Shepard Donald B DB Chong Rebecca A RA López Arriaza José J Hall Kathryn K Castoe Todd A TA Feschotte Cédric C Pollock David D DD Mueller Rachel Lockridge RL

Genome biology and evolution 20111226 2

Among vertebrates, most of the largest genomes are found within the salamanders, a clade of amphibians that includes 613 species. Salamander genome sizes range from ~14 to ~120 Gb. Because genome size is correlated with nucleus and cell sizes, as well as other traits, morphological evolution in salamanders has been profoundly affected by genomic gigantism. However, the molecular mechanisms driving genomic expansion in this clade remain largely unknown. Here, we present the first comparative anal ...[more]

PMID: 22200636

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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

LTR retrotransposons contribute to genomic gigantism in plethodontid salamanders.

Publications

LTR retrotransposons contribute to genomic gigantism in plethodontid salamanders.

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