Genome-wide signatures of convergent evolution in echolocating mammals

Journal name:
Nature
Volume:
502,
Pages:
228–231
Date published:
DOI:
doi:10.1038/nature12511
Received
Accepted
Published online

Evolution is typically thought to proceed through divergence of genes, proteins and ultimately phenotypes1, 2, 3. However, similar traits might also evolve convergently in unrelated taxa owing to similar selection pressures4, 5. 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 level6, 7, 8, 9. 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 evolution9, 10, 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.

At a glance

Figures

  1. Convergence hypotheses and genomic distribution of support.
    Figure 1: Convergence hypotheses and genomic distribution of support.

    a, For each locus, the goodness-of-fit of three separate phylogenetic hypotheses was considered: (left) H0, the accepted species phylogeny based on recent findings (for example, refs 14, 23, 24, 25); (top-right panel) 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 (bottom-right panel) 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 Methods 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 (left) the ‘bat–bat’ hypothesis uniting echolocating bats (that is, ΔSSLS (H1)) and (right) bat–dolphin hypothesis (that is, 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 additionally whether strength of positive selection (dN/dS) and convergence (ΔSSLS) at sites under selection in echolocators were correlated (**); see Supplementary Table 4 and Methods.

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

    a, b, For hypotheses H1(a) and H2(b) (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 characterized by a slope significantly below zero, are consistent with an evolutionary trajectory of adaptive convergence (purple line, with 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 of 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 Methods.

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Referenced accessions

Sequence Read Archive

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Author information

  1. These authors contributed equally to this work.

    • Joe Parker &
    • Georgia Tsagkogeorga

Affiliations

  1. School of Biological and Chemical Sciences, Queen Mary, University of London, London E1 4NS, UK

    • Joe Parker,
    • Georgia Tsagkogeorga,
    • James A. Cotton &
    • Stephen J. Rossiter
  2. BGI-Europe, Ole Maaløes Vej 3, DK-2200 Copenhagen N, Denmark

    • Yuan Liu
  3. Center for Translational Genomics and Bioinformatics, San Raffaele Scientific Institute, Via Olgettina 58, 20132 Milano, Italy

    • Paolo Provero &
    • Elia Stupka
  4. Department of Molecular Biotechnology and Health Sciences, University of Turin, Via Nizza 52, I-10126 Torino, Italy

    • Paolo Provero
  5. Present address: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.

    • James A. Cotton

Contributions

S.J.R. conceived the study and secured funding together with J.A.C. and E.S. J.P. conducted all phylogenetic, convergence and selection analyses with input from S.J.R., G.T. and J.A.C. Processing and analyses of sequence data was undertaken by G.T., with input from E.S., who also conducted gene ontology analyses with P.P. Raw sequence data was generated under direction of Y.L. and S.J.R. The paper was written and figures prepared by J.P. and S.J.R. with input from G.T., J.A.C. and E.S.

Competing financial interests

The authors declare no competing financial interests.

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Short-read data have been deposited into the Short Read Archive under accession numbers SRR924356, SRR924359, SRR924361 and SRR924427.

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    This file contains Supplementary Tables 1-13, Supplementary Figures 1- 9, Supplementary Methods and Supplementary References.

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