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. 2017 Oct 1;34(10):2522-2536.
doi: 10.1093/molbev/msx167.

Adaptive Patterns of Mitogenome Evolution Are Associated with the Loss of Shell Scutes in Turtles

Tibisay Escalona  1   2 , Cameron J Weadick  3 , Agostinho Antunes  1   2
Affiliations

Adaptive Patterns of Mitogenome Evolution Are Associated with the Loss of Shell Scutes in Turtles

Tibisay Escalona et al. Mol Biol Evol. .

Abstract

The mitochondrial genome encodes several protein components of the oxidative phosphorylation (OXPHOS) pathway and is critical for aerobic respiration. These proteins have evolved adaptively in many taxa, but linking molecular-level patterns with higher-level attributes (e.g., morphology, physiology) remains a challenge. Turtles are a promising system for exploring mitochondrial genome evolution as different species face distinct respiratory challenges and employ multiple strategies for ensuring efficient respiration. One prominent adaptation to a highly aquatic lifestyle in turtles is the secondary loss of keratenized shell scutes (i.e., soft-shells), which is associated with enhanced swimming ability and, in some species, cutaneous respiration. We used codon models to examine patterns of selection on mitochondrial protein-coding genes along the three turtle lineages that independently evolved soft-shells. We found strong evidence for positive selection along the branches leading to the pig-nosed turtle (Carettochelys insculpta) and the softshells clade (Trionychidae), but only weak evidence for the leatherback (Dermochelys coriacea) branch. Positively selected sites were found to be particularly prevalent in OXPHOS Complex I proteins, especially subunit ND2, along both positively selected lineages, consistent with convergent adaptive evolution. Structural analysis showed that many of the identified sites are within key regions or near residues involved in proton transport, indicating that positive selection may have precipitated substantial changes in mitochondrial function. Overall, our study provides evidence that physiological challenges associated with adaptation to a highly aquatic lifestyle have shaped the evolution of the turtle mitochondrial genome in a lineage-specific manner.

Keywords: Cryptodira; ecomorphology; mitochondria; molecular evolution; respiratory physiology.

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Figures

<sc>Fig</sc>. 1.
Fig. 1.
Maximum Likelihood (ML) phylogenetic tree for Cryptodiran turtles. The tree was estimated using the concatenated data set of 12 mtDNA protein-coding genes (with Pleurodira as the outgroup; thin dashed branches). Species codes and NCBI Genbank accession numbers are provided alongside the phylogeny. Paleontological evidence indicates that soft-shells evolved 3 times independently, as denoted by the thicker branches (Trionychidae (Trio)-black, Carettochelyidae (Care)-gray, Dermochelyidae (Der)-dashed). Branch lengths and the scale bar indicate the number of nucleotide substitutions per site. Numbers adjacent to nodes represent ML bootstrap values (1,000 replicates).
<sc>Fig</sc>. 2.
Fig. 2.
Codon-wise dN/dS estimates for the concatenated data set of 12 mtDNA protein-coding genes. Codon-wise dN/dS estimates were calculated using the M8 random-site model. The y-axis shows the BEB posterior mean estimate of dN/dS for each site (±standard error). Horizontal solid lines show the mean estimate for each gene.
<sc>Fig</sc>. 3.
Fig. 3.
Spatial distribution of the positively selected sites identified along soft-shelled turtle lineages. Sites identified by branch-site analysis of the 12 heavy chain mitochondrially encoded proteins of the OXPHOS pathway were mapped onto homologous solved protein structures from Sus scrofa (Complexes CI, CIII, CIV; PDB 5GUP) and Bos taurus (Complexes CV; PDB 5ARA). Grey structures represent nuclear-encoded subunits, and no structure currently exists for CV subunit ATP8. Only positively selected sites with PP ≥ 0.90 are considered; no sites met this threshold for the ND3, COX1, and COX2 subunits. (a) The CI–CIII–CIV supercomplex. The supercomplex is shown in two differently rotated views along the membrane. CIII is present twice as a homodimer. Mitochondrially encoded subunits are represented in different colors, as indicated in (b). (b) Individual OXPHOS complexes, with mitochondrially encoded subunits colored as follows (from L to R): CI-ND5 in green: CI-ND4 in purple; CI-ND2 in orange; CI-ND4L in cyan; CI-ND1 in light magenta; CIII (homodimer)–CYTB in aquamarine; CIV-COX2 in green; CIV-COX1 in purple, CIV-COX3 in yellow; CV-ATP6 in blue. (c) Individual core subunits with positively selected sites shown as stick models, with the color indicating the branch along which the site was identified: the softshells (Trionychidae) branch in blue; the pig-nose turtle branch (Carettochelyidae) branch in green; the leatherback branch (Dermochelyidae) in orange. Abbreviations: OXPHOS Complex I (CI), Complex III (CIII), Complex IV (CIV), Complex V (CV); Long horizontal α-helix coupling element (HL); β hairpin coupling element (βh); Quinone-binding site (QN); C-terminus (C); N-terminus (N); V-shaped cleft (V-Cleft); Bound cofactors HemebH and HemebL; Complex V subunits (a and b-subunit). Site numbering follows that of the relevant crystal structure.
<sc>Fig</sc>. 4.
Fig. 4.
Positively selected sites and the proton translocation pathway in OXPHOS Complex I. The figure illustrates the position of positively selected sites in relation to the proposed proton translocation pathway that runs throughout Complex I. Subunits with positively selected sites (with PP ≥0.90) are colored (from left-to-right: ND5 in green; ND4 in purple; ND2 in orange; ND4L in blue; ND1 in magenta); for clarity, only relevant structural elements are colored. Positively selected sites are shown as stick models, with the color indicating the branch along which the site was identified: blue represents the softshell clade (Trionychidae), green the pig-nose turtle branch (Carettochelyidae), and orange the leatherback sea turtle branch (Dermochelyidae). The proposed proton translocation pathway is indicated by double-headed arrows, and essential residues that line the channel are shown in red (Sazanov 2015; Fiedorczuk etal. 2016). Also noted on the structure: 1) relevant transmembrane (TM) helices; 2) the coupling elements HL and βh; 3) the quinone-binding cavity (QN). The structure is derived from Sus scrofa (PDB 5GUP) and residue and TM numbering follows that of the original structure.
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