Genome-wide signatures of convergent evolution in echolocating mammals

Abstract

Evolution is typically thought to proceed through divergence of genes, proteins and ultimately phenotypes. However, similar traits might also evolve convergently in unrelated taxa owing to similar selection pressures. Adaptive phenotypic convergence is widespread in nature, and recent results from several genes have suggested that this phenomenon is powerful enough to also drive recurrent evolution at the sequence level. Where homoplasious substitutions do occur these have long been considered the result of neutral processes. However, recent studies have demonstrated that adaptive convergent sequence evolution can be detected in vertebrates using statistical methods that model parallel evolution, although the extent to which sequence convergence between genera occurs across genomes is unknown. Here we analyse genomic sequence data in mammals that have independently evolved echolocation and show that convergence is not a rare process restricted to several loci but is instead widespread, continuously distributed and commonly driven by natural selection acting on a small number of sites per locus. Systematic analyses of convergent sequence evolution in 805,053 amino acids within 2,326 orthologous coding gene sequences compared across 22 mammals (including four newly sequenced bat genomes) revealed signatures consistent with convergence in nearly 200 loci. Strong and significant support for convergence among bats and the bottlenose dolphin was seen in numerous genes linked to hearing or deafness, consistent with an involvement in echolocation. Unexpectedly, we also found convergence in many genes linked to vision: the convergent signal of many sensory genes was robustly correlated with the strength of natural selection. This first attempt to detect genome-wide convergent sequence evolution across divergent taxa reveals the phenomenon to be much more pervasive than previously recognized.

Figure 1. Convergence hypotheses, and genomic distribution of support

a) For each locus, the goodness-of-fit of three separate phylogenetic hypotheses was considered: (i) H₀, the accepted species phylogeny based on recent findings e.g.^,-; (ii) H₁, or ‘bat-bat convergence’, in which echolocating bat lineages (shown in brown) are forced to form a monophyletic group to the exclusion of non-echolocating Old World fruit bats (shown in orange); and (iii) H₂, or ‘bat-dolphin convergence’, in which the echolocating bat lineages and the dolphin (blue) form a monophyletic group to the exclusion of all non-echolocating mammals. See Supplementary Information for details of model fitting and topologies. b) The distribution of convergence signal across 2,326 loci in 14–22 representative mammalian taxa, as measured by locus-wise mean site-specific likelihood support for the species topology (H₀) over (i) the ‘bat-bat’ hypothesis uniting echolocating bats (i.e. ΔSSLS (H₁) and (ii) bat-dolphin hypothesis (i.e. ΔSSLS (H₂). Representative hearing and vision loci are shown in green and blue, respectively; for each locus significance levels based on simulation denote whether it had significant counts of convergent sites after correcting for expected counts in random (control) phylogenies (*) and whether strength of positive selection (dN/dS) and convergence (ΔSSLS) at sites under selection in echolocators were correlated (**); see Table S4, Supplementary Information.

Figure 2. Relationship between strength of convergence signal and adaptive selection

For hypotheses (a) H₁ and (b) H₂ (n = 2,030 and 1,876 loci, respectively), the 95% confidence intervals of the coefficient (slope) for locus-wise regressions between site-wise support for convergence and site-wise ω for sites under diversifying selection are plotted. In each plot, loci showing a negative relationship, as characterised by a slope significantly below zero, are consistent with an evolutionary trajectory of adaptive convergence (purple line; filled circle indicating upper 95% limit) and loci showing a positive relationship, with a slope of greater than zero, are consistent with an evolutionary trajectory adaptive divergence (orange line with filled circle indicating lower 95% limit). Insets show two examples of adaptive convergence and divergence under each hypothesis. Full details of ω estimation and regression fitting are given in the Supplementary Information.