Evidence for an ancient adaptive episode of convergent molecular evolution

Abstract

Documented cases of convergent molecular evolution due to selection are fairly unusual, and examples to date have involved only a few amino acid positions. However, because convergence mimics shared ancestry and is not accommodated by current phylogenetic methods, it can strongly mislead phylogenetic inference when it does occur. Here, we present a case of extensive convergent molecular evolution between snake and agamid lizard mitochondrial genomes that overcomes an otherwise strong phylogenetic signal. Evidence from morphology, nuclear genes, and most sites in the mitochondrial genome support one phylogenetic tree, but a subset of mostly amino acid-altering substitutions (primarily at the first and second codon positions) across multiple mitochondrial genes strongly supports a radically different phylogeny. The relevant sites generally evolved slowly but converged between ancient lineages of snakes and agamids. We estimate that Ϸ44 of 113 predicted convergent changes distributed across all 13 mitochondrial protein-coding genes are expected to have arisen from nonneutral causes-a remarkably large number. Combined with strong previous evidence for adaptive evolution in snake mitochondrial proteins, it is likely that much of this convergent evolution was driven by adaptation. These results indicate that nonneutral convergent molecular evolution in mitochondria can occur at a scale and intensity far beyond what has been documented previously, and they highlight the vulnerability of standard phylogenetic methods to the presence of nonneutral convergent sequence evolution.adaptation ͉ convergence ͉ phylogenetics ͉ reptile

Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory

“…6). By comparing convergent substitution numbers and empirically calculated background-level expectations 21 , we found that GH19 chitinases (Fig. 3a,b), purple acid phosphatases ( Supplementary Fig.…”

“…Branch lengths of reconciled trees were optimized using RAxML 51 . Finally, the numbers of convergent and divergent substitutions were estimated from the inferred tree topologies and the original simulated alignments using CodeMLancestral 21 ( Supplementary Fig. 10).…”

“…10). Substitution pairs that result in the same descendant amino acid at the same alignment position in both branches were categorized as convergent changes, whereas the remaining substitution pairs were counted as divergent changes 21,28 .…”

“…The trees were subsequently used for Bayesian ancestral state reconstruction using PhyloBayes 97 over 12,000 generations (2,000 generations of burn-in) with an infinite mixture of GTR substitution models (CAT-GTR model) of amino acid substitution and five discrete gamma categories of rate heterogeneity to calculate posterior numbers of convergent and divergent substitution pairs. Background levels (null hypothesis) of convergent substitution pairs were estimated by a linear regression in which the posterior numbers of convergent changes were predicted by divergent changes 21 . Over-accumulation of convergent changes in a tree was examined by one-sided single-sample proportion tests 98 with Yate's continuity correction 99 and subsequent Bonferroni adjustment for multiple comparisons 100 .…”

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“…Snakes and other lizards underwent major evolutionary redesign of core oxidative metabolism genes, presumably driven by selection for low resting metabolic rates and the ability to fluctuate widely among metabolic rates [8,9]. Similar but less extreme genetic shifts also occurred in cetaceans [10] and primates [11].…”