Molecular adaptations for sensing and securing prey and insight into amniote genome diversity from the garter snake genome

Blair W. Perry; Daren C. Card; Joel W. Mcglothlin; Giulia I.M. Pasquesi; Richard H. Adams; Drew R. Schield; Nicole R. Hales; Andrew B. Corbin; Jeffery P. Demuth; Federico G. Hoffmann; Michael W. Vandewege; Ryan K. Schott; Nihar Bhattacharyya; Belinda S.W. Chang; Nicholas R. Casewell; Gareth Whiteley; Jacobo Reyes-Velasco; Stephen P. Mackessy; Tony Gamble; Kenneth B. Storey; Kyle K. Biggar; Courtney Passow; Chih Horng Kuo; Suzanne E McGaugh; Anne M. Bronikowski; A. P.Jason De Koning; Scott V. Edwards; Michael E. Pfrender; Patrick Minx; Edmund D. Brodie; Edmund D. Brodie; Wesley C. Warren; Todd A. Castoe

doi:10.1093/gbe/evy157

Molecular adaptations for sensing and securing prey and insight into amniote genome diversity from the garter snake genome

Blair W. Perry
, Daren C. Card
, Joel W. Mcglothlin
, Giulia I.M. Pasquesi
, Richard H. Adams
, Drew R. Schield
, Nicole R. Hales
, Andrew B. Corbin
, Jeffery P. Demuth
, Federico G. Hoffmann
, Michael W. Vandewege
, Ryan K. Schott
, Nihar Bhattacharyya
, Belinda S.W. Chang
, Nicholas R. Casewell
, Gareth Whiteley
, Jacobo Reyes-Velasco
, Stephen P. Mackessy
, Tony Gamble
, Kenneth B. Storey

Kyle K. Biggar, Courtney Passow, Chih Horng Kuo, Suzanne E McGaugh, Anne M. Bronikowski, A. P.Jason De Koning, Scott V. Edwards, Michael E. Pfrender, Patrick Minx, Edmund D. Brodie, Edmund D. Brodie, Wesley C. Warren, Todd A. Castoe

Research output: Contribution to journal › Article › peer-review

84 Scopus citations

Abstract

Colubridae represents themost phenotypically diverse and speciose family of snakes, yet nowell-assembled and annotated genome exists for this lineage. Here, we report and analyze the genome of the garter snake, Thamnophis sirtalis, a colubrid snake that is an important model species for research in evolutionary biology, physiology, genomics, behavior, and the evolution of toxin resistance. Using the garter snake genome, we show how snakes have evolved numerous adaptations for sensing and securing prey, and identify features of snake genomestructure that provide insight into the evolution of amniote genomes.Analyses of the garter snake andother squamate reptile genomes highlight shifts in repeat element abundance andexpansionwithin snakes, uncover evidence of genes under positive selection, and provide revised neutral substitution rate estimates for squamates. Our identification of Z andW sex chromosome-specific scaffolds provides evidence for multiple origins of sex chromosome systems in snakes and demonstrates the value of this genome for studying sex chromosome evolution. Analysis of gene duplication and loss in visual and olfactory gene families supports a dim-light ancestral condition in snakes and indicates that olfactory receptor repertoires underwent an expansion early in snake evolution. Additionally, we provide some of the first links between secreted venom proteins, the genes that encode them, and their evolutionaryorigins ina rear-fanged colubridsnake, togetherwith newgenomic insight into the coevolutionary arms race between garter snakes and highly toxic newt prey that led to toxin resistance in garter snakes.

Original language	English (US)
Pages (from-to)	2110-2129
Number of pages	20
Journal	Genome biology and evolution
Volume	10
Issue number	8
DOIs	https://doi.org/10.1093/gbe/evy157
State	Published - Aug 1 2018

Bibliographical note

Funding Information:
We thank the production sequencing group at the McDonnell Genome Institute for assistance with genome sequencing, assembly and annotation, and John Abramyan for assistance with SCNA annotations in the chicken and turtle. The work was supported by funding from the National Human Genome Research Institute at National Institutes of Health [5U54HG00307907 to W.C.W.]; the National Science Foundation [DEB-1655571 and IOS-1655735 to T.A.C.]; a Natural Sciences and Engineering Research Council of Canada Discovery Grant [to B.S.W.C., K.B.S., and K.K.B.]; an Academia Sinica award [to C.H.K.]; a Minnesota Supercomputing Institute award [to S.E.M.]; and a Grand Challenges in Biology Postdoctoral Fellowship [to C.N.P.].

Publisher Copyright:
© The Author(s) 2018.

Keywords

Co-evolution
Sex chromosomes
Thamnophis sirtalis
Venom
Vision

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10.1093/gbe/evy157

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Perry, B. W., Card, D. C., Mcglothlin, J. W., Pasquesi, G. I. M., Adams, R. H., Schield, D. R., Hales, N. R., Corbin, A. B., Demuth, J. P., Hoffmann, F. G., Vandewege, M. W., Schott, R. K., Bhattacharyya, N., Chang, B. S. W., Casewell, N. R., Whiteley, G., Reyes-Velasco, J., Mackessy, S. P., Gamble, T., ... Castoe, T. A. (2018). Molecular adaptations for sensing and securing prey and insight into amniote genome diversity from the garter snake genome. Genome biology and evolution, 10(8), 2110-2129. https://doi.org/10.1093/gbe/evy157

Perry, BW, Card, DC, Mcglothlin, JW, Pasquesi, GIM, Adams, RH, Schield, DR, Hales, NR, Corbin, AB, Demuth, JP, Hoffmann, FG, Vandewege, MW, Schott, RK, Bhattacharyya, N, Chang, BSW, Casewell, NR, Whiteley, G, Reyes-Velasco, J, Mackessy, SP, Gamble, T, Storey, KB, Biggar, KK, Passow, C, Kuo, CH, McGaugh, SE, Bronikowski, AM, De Koning, APJ, Edwards, SV, Pfrender, ME, Minx, P, Brodie, ED, Brodie, ED, Warren, WC & Castoe, TA 2018, 'Molecular adaptations for sensing and securing prey and insight into amniote genome diversity from the garter snake genome', Genome biology and evolution, vol. 10, no. 8, pp. 2110-2129. https://doi.org/10.1093/gbe/evy157

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title = "Molecular adaptations for sensing and securing prey and insight into amniote genome diversity from the garter snake genome",

abstract = "Colubridae represents themost phenotypically diverse and speciose family of snakes, yet nowell-assembled and annotated genome exists for this lineage. Here, we report and analyze the genome of the garter snake, Thamnophis sirtalis, a colubrid snake that is an important model species for research in evolutionary biology, physiology, genomics, behavior, and the evolution of toxin resistance. Using the garter snake genome, we show how snakes have evolved numerous adaptations for sensing and securing prey, and identify features of snake genomestructure that provide insight into the evolution of amniote genomes.Analyses of the garter snake andother squamate reptile genomes highlight shifts in repeat element abundance andexpansionwithin snakes, uncover evidence of genes under positive selection, and provide revised neutral substitution rate estimates for squamates. Our identification of Z andW sex chromosome-specific scaffolds provides evidence for multiple origins of sex chromosome systems in snakes and demonstrates the value of this genome for studying sex chromosome evolution. Analysis of gene duplication and loss in visual and olfactory gene families supports a dim-light ancestral condition in snakes and indicates that olfactory receptor repertoires underwent an expansion early in snake evolution. Additionally, we provide some of the first links between secreted venom proteins, the genes that encode them, and their evolutionaryorigins ina rear-fanged colubridsnake, togetherwith newgenomic insight into the coevolutionary arms race between garter snakes and highly toxic newt prey that led to toxin resistance in garter snakes.",

keywords = "Co-evolution, Sex chromosomes, Thamnophis sirtalis, Venom, Vision",

author = "Perry, \{Blair W.\} and Card, \{Daren C.\} and Mcglothlin, \{Joel W.\} and Pasquesi, \{Giulia I.M.\} and Adams, \{Richard H.\} and Schield, \{Drew R.\} and Hales, \{Nicole R.\} and Corbin, \{Andrew B.\} and Demuth, \{Jeffery P.\} and Hoffmann, \{Federico G.\} and Vandewege, \{Michael W.\} and Schott, \{Ryan K.\} and Nihar Bhattacharyya and Chang, \{Belinda S.W.\} and Casewell, \{Nicholas R.\} and Gareth Whiteley and Jacobo Reyes-Velasco and Mackessy, \{Stephen P.\} and Tony Gamble and Storey, \{Kenneth B.\} and Biggar, \{Kyle K.\} and Courtney Passow and Kuo, \{Chih Horng\} and McGaugh, \{Suzanne E\} and Bronikowski, \{Anne M.\} and \{De Koning\}, \{A. P.Jason\} and Edwards, \{Scott V.\} and Pfrender, \{Michael E.\} and Patrick Minx and Brodie, \{Edmund D.\} and Brodie, \{Edmund D.\} and Warren, \{Wesley C.\} and Castoe, \{Todd A.\}",

note = "Funding Information: We thank the production sequencing group at the McDonnell Genome Institute for assistance with genome sequencing, assembly and annotation, and John Abramyan for assistance with SCNA annotations in the chicken and turtle. The work was supported by funding from the National Human Genome Research Institute at National Institutes of Health [5U54HG00307907 to W.C.W.]; the National Science Foundation [DEB-1655571 and IOS-1655735 to T.A.C.]; a Natural Sciences and Engineering Research Council of Canada Discovery Grant [to B.S.W.C., K.B.S., and K.K.B.]; an Academia Sinica award [to C.H.K.]; a Minnesota Supercomputing Institute award [to S.E.M.]; and a Grand Challenges in Biology Postdoctoral Fellowship [to C.N.P.]. Publisher Copyright: {\textcopyright} The Author(s) 2018.",

year = "2018",

month = aug,

day = "1",

doi = "10.1093/gbe/evy157",

language = "English (US)",

volume = "10",

pages = "2110--2129",

journal = "Genome biology and evolution",

issn = "1759-6653",

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number = "8",

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T1 - Molecular adaptations for sensing and securing prey and insight into amniote genome diversity from the garter snake genome

AU - Perry, Blair W.

AU - Card, Daren C.

AU - Mcglothlin, Joel W.

AU - Pasquesi, Giulia I.M.

AU - Adams, Richard H.

AU - Schield, Drew R.

AU - Hales, Nicole R.

AU - Corbin, Andrew B.

AU - Demuth, Jeffery P.

AU - Hoffmann, Federico G.

AU - Vandewege, Michael W.

AU - Schott, Ryan K.

AU - Bhattacharyya, Nihar

AU - Chang, Belinda S.W.

AU - Casewell, Nicholas R.

AU - Whiteley, Gareth

AU - Reyes-Velasco, Jacobo

AU - Mackessy, Stephen P.

AU - Gamble, Tony

AU - Storey, Kenneth B.

AU - Biggar, Kyle K.

AU - Passow, Courtney

AU - Kuo, Chih Horng

AU - McGaugh, Suzanne E

AU - Bronikowski, Anne M.

AU - De Koning, A. P.Jason

AU - Edwards, Scott V.

AU - Pfrender, Michael E.

AU - Minx, Patrick

AU - Brodie, Edmund D.

AU - Warren, Wesley C.

AU - Castoe, Todd A.

N1 - Funding Information: We thank the production sequencing group at the McDonnell Genome Institute for assistance with genome sequencing, assembly and annotation, and John Abramyan for assistance with SCNA annotations in the chicken and turtle. The work was supported by funding from the National Human Genome Research Institute at National Institutes of Health [5U54HG00307907 to W.C.W.]; the National Science Foundation [DEB-1655571 and IOS-1655735 to T.A.C.]; a Natural Sciences and Engineering Research Council of Canada Discovery Grant [to B.S.W.C., K.B.S., and K.K.B.]; an Academia Sinica award [to C.H.K.]; a Minnesota Supercomputing Institute award [to S.E.M.]; and a Grand Challenges in Biology Postdoctoral Fellowship [to C.N.P.]. Publisher Copyright: © The Author(s) 2018.

PY - 2018/8/1

Y1 - 2018/8/1

N2 - Colubridae represents themost phenotypically diverse and speciose family of snakes, yet nowell-assembled and annotated genome exists for this lineage. Here, we report and analyze the genome of the garter snake, Thamnophis sirtalis, a colubrid snake that is an important model species for research in evolutionary biology, physiology, genomics, behavior, and the evolution of toxin resistance. Using the garter snake genome, we show how snakes have evolved numerous adaptations for sensing and securing prey, and identify features of snake genomestructure that provide insight into the evolution of amniote genomes.Analyses of the garter snake andother squamate reptile genomes highlight shifts in repeat element abundance andexpansionwithin snakes, uncover evidence of genes under positive selection, and provide revised neutral substitution rate estimates for squamates. Our identification of Z andW sex chromosome-specific scaffolds provides evidence for multiple origins of sex chromosome systems in snakes and demonstrates the value of this genome for studying sex chromosome evolution. Analysis of gene duplication and loss in visual and olfactory gene families supports a dim-light ancestral condition in snakes and indicates that olfactory receptor repertoires underwent an expansion early in snake evolution. Additionally, we provide some of the first links between secreted venom proteins, the genes that encode them, and their evolutionaryorigins ina rear-fanged colubridsnake, togetherwith newgenomic insight into the coevolutionary arms race between garter snakes and highly toxic newt prey that led to toxin resistance in garter snakes.

AB - Colubridae represents themost phenotypically diverse and speciose family of snakes, yet nowell-assembled and annotated genome exists for this lineage. Here, we report and analyze the genome of the garter snake, Thamnophis sirtalis, a colubrid snake that is an important model species for research in evolutionary biology, physiology, genomics, behavior, and the evolution of toxin resistance. Using the garter snake genome, we show how snakes have evolved numerous adaptations for sensing and securing prey, and identify features of snake genomestructure that provide insight into the evolution of amniote genomes.Analyses of the garter snake andother squamate reptile genomes highlight shifts in repeat element abundance andexpansionwithin snakes, uncover evidence of genes under positive selection, and provide revised neutral substitution rate estimates for squamates. Our identification of Z andW sex chromosome-specific scaffolds provides evidence for multiple origins of sex chromosome systems in snakes and demonstrates the value of this genome for studying sex chromosome evolution. Analysis of gene duplication and loss in visual and olfactory gene families supports a dim-light ancestral condition in snakes and indicates that olfactory receptor repertoires underwent an expansion early in snake evolution. Additionally, we provide some of the first links between secreted venom proteins, the genes that encode them, and their evolutionaryorigins ina rear-fanged colubridsnake, togetherwith newgenomic insight into the coevolutionary arms race between garter snakes and highly toxic newt prey that led to toxin resistance in garter snakes.

KW - Co-evolution

KW - Sex chromosomes

KW - Thamnophis sirtalis

KW - Venom

KW - Vision

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DO - 10.1093/gbe/evy157

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SN - 1759-6653

VL - 10

SP - 2110

EP - 2129

JO - Genome biology and evolution

JF - Genome biology and evolution

IS - 8

ER -

Molecular adaptations for sensing and securing prey and insight into amniote genome diversity from the garter snake genome

Abstract

Bibliographical note

Keywords

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