Comparative Genomics Reveals Accelerated Evolution in Conserved Pathways during the Diversification of Anole Lizards

Marc Tollis, Elizabeth D. Hutchins, Jessica Stapley, Shawn M. Rupp, Walter L. Eckalbar, Inbar Maayan, Eris Lasku, Carlos R. Infante, Stuart R. Dennis, Joel A. Robertson, Catherine M. May, Michael R. Crusoe, Eldredge Bermingham, Dale Denardo, Shi Tong Tonia Hsieh, Rob J. Kulathinal, William Owen McMillan, Douglas B. Menke, Stephen Pratt, Jeffery RawlsOris Sanjur, Norma Wilson-Rawls, Melissa Wilson Sayres, Rebecca E. Fisher, Kenro Kusumi

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

Squamates include all lizards and snakes, and display some of the most diverse and extreme morphological adaptations among vertebrates. However, compared with birds and mammals, relatively few resources exist for comparative genomic analyses of squamates, hampering efforts to understand the molecular bases of phenotypic diversification in such a speciose clade. In particular, the ∼400 species of anole lizard represent an extensive squamate radiation. Here, we sequence and assemble the draft genomes of three anole species - Anolis frenatus, Anolis auratus, and Anolis apletophallus - for comparison with the available reference genome of Anolis carolinensis. Comparative analyses reveal a rapid background rate of molecular evolution consistent with a model of punctuated equilibrium, and strong purifying selection on functional genomic elements in anoles. We find evidence for accelerated evolution in genes involved in behavior, sensory perception, and reproduction, as well as in genes regulating limb bud development and hindlimb specification. Morphometric analyses of anole fore and hindlimbs corroborated these findings. We detect signatures of positive selection across several genes related to the development and regulation of the forebrain, hormones, and the iguanian lizard dewlap, suggesting molecular changes underlying behavioral adaptations known to reinforce species boundaries were a key component in the diversification of anole lizards.

Original languageEnglish (US)
Pages (from-to)489-506
Number of pages18
JournalGenome Biology and Evolution
Volume10
Issue number2
DOIs
StatePublished - Feb 1 2018

Fingerprint

Lizards
Genomics
lizard
Anolis
lizards
genomics
Squamata
Hindlimb
gene
genome
punctuated equilibrium
Genome
Genes
Anolis carolinensis
limb bud
Limb Buds
genes
Molecular Evolution
Snakes
Prosencephalon

Keywords

  • adaptation
  • Anolis
  • genomes
  • molecular evolution
  • phenotypic evolution
  • substitution rates

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

Cite this

Comparative Genomics Reveals Accelerated Evolution in Conserved Pathways during the Diversification of Anole Lizards. / Tollis, Marc; Hutchins, Elizabeth D.; Stapley, Jessica; Rupp, Shawn M.; Eckalbar, Walter L.; Maayan, Inbar; Lasku, Eris; Infante, Carlos R.; Dennis, Stuart R.; Robertson, Joel A.; May, Catherine M.; Crusoe, Michael R.; Bermingham, Eldredge; Denardo, Dale; Hsieh, Shi Tong Tonia; Kulathinal, Rob J.; McMillan, William Owen; Menke, Douglas B.; Pratt, Stephen; Rawls, Jeffery; Sanjur, Oris; Wilson-Rawls, Norma; Wilson Sayres, Melissa; Fisher, Rebecca E.; Kusumi, Kenro.

In: Genome Biology and Evolution, Vol. 10, No. 2, 01.02.2018, p. 489-506.

Research output: Contribution to journalArticle

Tollis, M, Hutchins, ED, Stapley, J, Rupp, SM, Eckalbar, WL, Maayan, I, Lasku, E, Infante, CR, Dennis, SR, Robertson, JA, May, CM, Crusoe, MR, Bermingham, E, Denardo, D, Hsieh, STT, Kulathinal, RJ, McMillan, WO, Menke, DB, Pratt, S, Rawls, J, Sanjur, O, Wilson-Rawls, N, Wilson Sayres, M, Fisher, RE & Kusumi, K 2018, 'Comparative Genomics Reveals Accelerated Evolution in Conserved Pathways during the Diversification of Anole Lizards', Genome Biology and Evolution, vol. 10, no. 2, pp. 489-506. https://doi.org/10.1093/gbe/evy013
Tollis, Marc ; Hutchins, Elizabeth D. ; Stapley, Jessica ; Rupp, Shawn M. ; Eckalbar, Walter L. ; Maayan, Inbar ; Lasku, Eris ; Infante, Carlos R. ; Dennis, Stuart R. ; Robertson, Joel A. ; May, Catherine M. ; Crusoe, Michael R. ; Bermingham, Eldredge ; Denardo, Dale ; Hsieh, Shi Tong Tonia ; Kulathinal, Rob J. ; McMillan, William Owen ; Menke, Douglas B. ; Pratt, Stephen ; Rawls, Jeffery ; Sanjur, Oris ; Wilson-Rawls, Norma ; Wilson Sayres, Melissa ; Fisher, Rebecca E. ; Kusumi, Kenro. / Comparative Genomics Reveals Accelerated Evolution in Conserved Pathways during the Diversification of Anole Lizards. In: Genome Biology and Evolution. 2018 ; Vol. 10, No. 2. pp. 489-506.
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