The origin of modern frogs (Neobatrachia) was accompanied by acceleration in mitochondrial and nuclear substitution rates

Abstract

BackgroundUnderstanding the causes underlying heterogeneity of molecular evolutionary rates among lineages is a long-standing and central question in evolutionary biology. Although several earlier studies showed that modern frogs (Neobatrachia) experienced an acceleration of mitochondrial gene substitution rates compared to non-neobatrachian relatives, no further characterization of this phenomenon was attempted. To gain new insights on this topic, we sequenced the complete mitochondrial genomes and nine nuclear loci of one pelobatoid (Pelodytes punctatus) and five neobatrachians, Heleophryne regis (Heleophrynidae), Lechriodus melanopyga (Limnodynastidae), Calyptocephalella gayi (Calyptocephalellidae), Telmatobius bolivianus (Ceratophryidae), and Sooglossus thomasseti (Sooglossidae). These represent major clades not included in previous mitogenomic analyses, and most of them are remarkably species-poor compared to other neobatrachians.ResultsWe reconstructed a fully resolved and robust phylogeny of extant frogs based on the new mitochondrial and nuclear sequence data, and dated major cladogenetic events. The reconstructed tree recovered Heleophryne as sister group to all other neobatrachians, the Australasian Lechriodus and the South American Calyptocephalella formed a clade that was the sister group to Nobleobatrachia, and the Seychellois Sooglossus was recovered as the sister group of Ranoides. We used relative-rate tests and direct comparison of branch lengths from mitochondrial and nuclear-based trees to demonstrate that both mitochondrial and nuclear evolutionary rates are significantly higher in all neobatrachians compared to their non-neobatrachian relatives, and that such rate acceleration started at the origin of Neobatrachia.ConclusionsThrough the analysis of the selection coefficient (ω) in different branches of the tree, we found compelling evidence of relaxation of purifying selection in neobatrachians, which could (at least in part) explain the observed higher mitochondrial and nuclear substitution rates in this clade. Our analyses allowed us to discard that changes in substitution rates could be correlated with increased mitochondrial genome rearrangement or diversification rates observed in different lineages of neobatrachians.

Targeted Enrichment: Maximizing Orthologous Gene Comparisons across Deep Evolutionary Time

“…Our inferred phylogeny (Figure 4) is congruent with other published phylogenies of frogs [47], [48], [49], [50]. Both the complete concatenated data set (13 species, 497,239 bp, 74% missing) as well as the data set with no missing data (13 species, 8,494 bp, 0% missing) generated the same maximum-likelihood topology, regardless of partitioning scheme.…”

“…For this node, the Bayesian concordance factors based on 23 exons sampled for all 13 taxa was 0.817. Rhinophrynus dorsalis is widely accepted on the basis of morphological and molecular data as sister to Pipidae [47], [48], [49], [50], [51], and gene trees that place this taxon elsewhere in the tree could indicate lack of orthology or systematic error affecting phylogenetic reconstruction for that exon. After excluding exons that failed to infer Rhinophrynus dorsalis as sister to pipid frogs, a maximum-likelihood analysis of the remaining exons (n = 718) returned a bootstrap proportion of 1.0 supporting X. tropicalis+X.…”

Intraspecific rearrangement of mitochondrial genome suggests the prevalence of the tandem duplication-random loss (TDLR) mechanism in Quasipaa boulengeri

“…A hotspot of gene rearrangement has been reported in the “WANCY” region ( trnW , trnA , trnN , origin of light strand replication (O L ), trnC , and trnY ) [6, 24]. Because many amphibians have gene rearrangements in their WANCY region [17, 25, 26], reorganizations in this group facilitate testing hypotheses on how gene-rearrangement occurs. Each of the above hypotheses predicts a unique arrangement of five short tRNA genes in the WANCY region (Fig.…”

A novel mitogenomic rearrangement for Odorrana schmackeri (Anura: Ranidae) and phylogeny of Ranidae inferred from thirteen mitochondrial protein-coding genes

“…Four tRNA genes (tRNA-Leu (CUN)/tRNA-Thr/tRNA-Pro/ tRNA-Phe) are located between CR and 12S rRNA producing a LTPF tRNA cluster. This re arrangement is common not only in ranids, but also in Neobatrachia (Su et al, 2007;Zhou et al, 2009;Alam et al, 2010;Kurabayashi et al, 2010;Irisarri et al, 2012). In the WANCY tRNA cluster, the positions of the origin of light-strand replication (OL) and the tRNA-Asn are exchanged, and OL is located be tween the tRNA-Ala and tRNA-Asn (from the typical 5/-WANOLCY-3' to 5'-WAOLNCY-3') ( fig.…”

“…For all Neobatrachia frog sequences, the tRNA-Leu (CUN), tRNA-Thr, and tRNAPro genes form a concatenation unit and lo cate upstream to tRNA-Phe gene. This situation of tRNA gene rearrangement is only found in published Neobatrachia frog sequences, which could be called the typical neobatrachian-type arrangement (Sumida et al, 2001;Zhang et al, 2005;Irisarri et al, 2012;Zhang et al, 2013). The mitogenome arrangements are gen erally thought to reflect phylogenetic relation ships (Macey et al, 1997;Boore and Brown, 1998).…”