Genome-wide signatures of convergent evolution in echolocating mammals

Joe Parker, Georgia Tsagkogeorga, James A. Cotton, Yuan Liu, Paolo Provero, Elia Stupka, Stephen J. Rossiter

Research output: Contribution to journalArticle

172 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)228-231
Number of pages4
JournalNature
Volume502
Issue number7470
DOIs
Publication statusPublished - 2013

Fingerprint

Mammals
Genome
Echolocation
Genes
Genetic Selection
Sequence Analysis
Bottle-Nosed Dolphin
Statistical Models
Deafness
Hearing
Vertebrates
Phenotype
Amino Acids
Pressure
Proteins

ASJC Scopus subject areas

  • General

Cite this

Parker, J., Tsagkogeorga, G., Cotton, J. A., Liu, Y., Provero, P., Stupka, E., & Rossiter, S. J. (2013). Genome-wide signatures of convergent evolution in echolocating mammals. Nature, 502(7470), 228-231. https://doi.org/10.1038/nature12511

Genome-wide signatures of convergent evolution in echolocating mammals. / Parker, Joe; Tsagkogeorga, Georgia; Cotton, James A.; Liu, Yuan; Provero, Paolo; Stupka, Elia; Rossiter, Stephen J.

In: Nature, Vol. 502, No. 7470, 2013, p. 228-231.

Research output: Contribution to journalArticle

Parker, J, Tsagkogeorga, G, Cotton, JA, Liu, Y, Provero, P, Stupka, E & Rossiter, SJ 2013, 'Genome-wide signatures of convergent evolution in echolocating mammals', Nature, vol. 502, no. 7470, pp. 228-231. https://doi.org/10.1038/nature12511
Parker J, Tsagkogeorga G, Cotton JA, Liu Y, Provero P, Stupka E et al. Genome-wide signatures of convergent evolution in echolocating mammals. Nature. 2013;502(7470):228-231. https://doi.org/10.1038/nature12511
Parker, Joe ; Tsagkogeorga, Georgia ; Cotton, James A. ; Liu, Yuan ; Provero, Paolo ; Stupka, Elia ; Rossiter, Stephen J. / Genome-wide signatures of convergent evolution in echolocating mammals. In: Nature. 2013 ; Vol. 502, No. 7470. pp. 228-231.
@article{c4897697e83743268a81152ec0cc3967,
title = "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.",
author = "Joe Parker and Georgia Tsagkogeorga and Cotton, {James A.} and Yuan Liu and Paolo Provero and Elia Stupka and Rossiter, {Stephen J.}",
year = "2013",
doi = "10.1038/nature12511",
language = "English",
volume = "502",
pages = "228--231",
journal = "Nature",
issn = "0028-0836",
publisher = "Nature Publishing Group",
number = "7470",

}

TY - JOUR

T1 - Genome-wide signatures of convergent evolution in echolocating mammals

AU - Parker, Joe

AU - Tsagkogeorga, Georgia

AU - Cotton, James A.

AU - Liu, Yuan

AU - Provero, Paolo

AU - Stupka, Elia

AU - Rossiter, Stephen J.

PY - 2013

Y1 - 2013

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84885574505&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84885574505&partnerID=8YFLogxK

U2 - 10.1038/nature12511

DO - 10.1038/nature12511

M3 - Article

VL - 502

SP - 228

EP - 231

JO - Nature

JF - Nature

SN - 0028-0836

IS - 7470

ER -