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Title: Conservation genetics of the eastern yellow-bellied racer (Coluber constrictor flaviventris) and bullsnake (Pituophis catenifer sayi): River valleys are critical features for snakes at northern range limits

Abstract

On the North American Great Plains, several snake species reach their northern range limit where they rely on sparsely distributed hibernacula located in major river valleys. Independent colonization histories for the river valleys and barriers to gene flow caused by the lack of suitable habitat between them may have produced genetically differentiated snake populations. To test this hypothesis, we used 10 microsatellite loci to examine the population structure of two species of conservation concern in Canada: the eastern yellow-bellied racer (Coluber constrictor flaviventris) and bullsnake (Pituophis catenifer sayi) in 3 major river valleys in southern Saskatchewan. Fixation indices (F ST) showed that populations in river valleys were significantly differentiated for both species (racers, F ST = 0.096, P = 0.001; bullsnakes FST = 0.045–0.157, P = 0.001). Bayesian assignment (STRUCTURE) and ordination (DAPC) strongly supported genetically differentiated groups in the geographically distinct river valleys. Finer-scale subdivision of populations within river valleys was not apparent based on our data, but is a topic that should be investigated further. Our findings highlight the importance of major river valleys for snakes at the northern extent of their ranges, and raise the possibility that populations in each river valley may warrant separate management strategies.

Authors:
ORCiD logo [1];  [1];  [1];  [2];  [3];  [1];  [4];  [5]
  1. Univ. of Regina, Regina, Saskatchewan (Canada). Dept. of Biology
  2. Saint Mary's Univ., Halifax, Nova Scotia (Canada). Dept. of Biology
  3. Univ. of Georgia, Aiken, SC (United States). Savannah River Ecology Lab.
  4. Royal Saskatchewan Museum, Regina, Saskatchewan (Canada)
  5. National Cheng Kung Univ., Tainan City (Taiwan)
Publication Date:
Research Org.:
Univ. of Georgia Research Foundation, Inc., Athens, GA (United States)
Sponsoring Org.:
USDOE; Natural Sciences and Engineering Research Council of Canada (NSERC)
OSTI Identifier:
1406661
Alternate Identifier(s):
OSTI ID: 1499891
Grant/Contract Number:  
FC09-07SR22506
Resource Type:
Published Article
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 12; Journal Issue: 11; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Somers, Christopher M., Graham, Carly F., Martino, Jessica A., Frasier, Timothy R., Lance, Stacey L., Gardiner, Laura E., Poulin, Ray G., and Chiang, Tzen-Yuh. Conservation genetics of the eastern yellow-bellied racer (Coluber constrictor flaviventris) and bullsnake (Pituophis catenifer sayi): River valleys are critical features for snakes at northern range limits. United States: N. p., 2017. Web. doi:10.1371/journal.pone.0187322.
Somers, Christopher M., Graham, Carly F., Martino, Jessica A., Frasier, Timothy R., Lance, Stacey L., Gardiner, Laura E., Poulin, Ray G., & Chiang, Tzen-Yuh. Conservation genetics of the eastern yellow-bellied racer (Coluber constrictor flaviventris) and bullsnake (Pituophis catenifer sayi): River valleys are critical features for snakes at northern range limits. United States. doi:10.1371/journal.pone.0187322.
Somers, Christopher M., Graham, Carly F., Martino, Jessica A., Frasier, Timothy R., Lance, Stacey L., Gardiner, Laura E., Poulin, Ray G., and Chiang, Tzen-Yuh. Thu . "Conservation genetics of the eastern yellow-bellied racer (Coluber constrictor flaviventris) and bullsnake (Pituophis catenifer sayi): River valleys are critical features for snakes at northern range limits". United States. doi:10.1371/journal.pone.0187322.
@article{osti_1406661,
title = {Conservation genetics of the eastern yellow-bellied racer (Coluber constrictor flaviventris) and bullsnake (Pituophis catenifer sayi): River valleys are critical features for snakes at northern range limits},
author = {Somers, Christopher M. and Graham, Carly F. and Martino, Jessica A. and Frasier, Timothy R. and Lance, Stacey L. and Gardiner, Laura E. and Poulin, Ray G. and Chiang, Tzen-Yuh},
abstractNote = {On the North American Great Plains, several snake species reach their northern range limit where they rely on sparsely distributed hibernacula located in major river valleys. Independent colonization histories for the river valleys and barriers to gene flow caused by the lack of suitable habitat between them may have produced genetically differentiated snake populations. To test this hypothesis, we used 10 microsatellite loci to examine the population structure of two species of conservation concern in Canada: the eastern yellow-bellied racer (Coluber constrictor flaviventris) and bullsnake (Pituophis catenifer sayi) in 3 major river valleys in southern Saskatchewan. Fixation indices (FST) showed that populations in river valleys were significantly differentiated for both species (racers, FST = 0.096, P = 0.001; bullsnakes FST = 0.045–0.157, P = 0.001). Bayesian assignment (STRUCTURE) and ordination (DAPC) strongly supported genetically differentiated groups in the geographically distinct river valleys. Finer-scale subdivision of populations within river valleys was not apparent based on our data, but is a topic that should be investigated further. Our findings highlight the importance of major river valleys for snakes at the northern extent of their ranges, and raise the possibility that populations in each river valley may warrant separate management strategies.},
doi = {10.1371/journal.pone.0187322},
journal = {PLoS ONE},
number = 11,
volume = 12,
place = {United States},
year = {2017},
month = {11}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1371/journal.pone.0187322

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Works referenced in this record:

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Biogeography of the smooth snake ( Coronella austriaca ): origin and conservation of the northernmost population : Distribution/Conservation of the Smooth Snake
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Population genetics of the Halys pit viper (Gloydius halys) at the northern distribution limit in Siberia
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Detecting the number of clusters of individuals using the software structure: a simulation study
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Spatial Ecology and Habitat Selection of Bullsnakes (Pituophis catenifer sayi) at the Northern Periphery of Their Geographic Range
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    Works referencing / citing this record:

    Microsatellite and major histocompatibility complex variation in an endangered rattlesnake, the Eastern Massasauga ( Sistrurus catenatus )
    journal, May 2016

    • Jaeger, Collin P.; Duvall, Melvin R.; Swanson, Bradley J.
    • Ecology and Evolution, Vol. 6, Issue 12
    • DOI: 10.1002/ece3.2159

    Habitat selection by grassland snakes at northern range limits: Implications for conservation
    journal, December 2011

    • Martino, Jessica A.; Poulin, Ray G.; Parker, Dennilyn L.
    • The Journal of Wildlife Management, Vol. 76, Issue 4
    • DOI: 10.1002/jwmg.313

    Balancing the dumbbell: Summer habitats need protection in addition to winter dens for northern snake communities: Summer Habitat Use by Snakes
    journal, June 2013

    • Gardiner, Laura E.; Somers, Christopher M.; Martino, Jessica A.
    • The Journal of Wildlife Management, Vol. 77, Issue 5
    • DOI: 10.1002/jwmg.555

    Limited genetic diversity and high differentiation among the remnant adder (Vipera berus) populations in the Swiss and French Jura Mountains
    journal, April 2008

    • Ursenbacher, Sylvain; Monney, Jean-Claude; Fumagalli, Luca
    • Conservation Genetics, Vol. 10, Issue 2
    • DOI: 10.1007/s10592-008-9580-7

    Microsatellite variation, population structure, and bottlenecks in the threatened copperbelly water snake
    journal, June 2008

    • Marshall, John C.; Kingsbury, Bruce A.; Minchella, Dennis J.
    • Conservation Genetics, Vol. 10, Issue 2
    • DOI: 10.1007/s10592-008-9624-z

    Population genetic structure at the northern range limit of the threatened eastern hog-nosed snake (Heterodon platirhinos)
    journal, June 2015

    • Xuereb, Amanda T. J.; Rouse, Jeremy D.; Cunnington, Glenn
    • Conservation Genetics, Vol. 16, Issue 6
    • DOI: 10.1007/s10592-015-0737-x

    Development and characterization of 16 microsatellite markers for the Louisiana pine snake, Pituophis ruthveni, and two congeners of conservation concern
    journal, March 2010

    • Kwiatkowski, Matthew A.; Somers, Christopher M.; Poulin, Ray G.
    • Conservation Genetics Resources, Vol. 2, Issue 1
    • DOI: 10.1007/s12686-010-9208-3

    STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method
    journal, October 2011


    Diet and snake venom evolution
    journal, February 1996

    • Daltry, Jennifer C.; Wüster, Wolfgang; Thorpe, Roger S.
    • Nature, Vol. 379, Issue 6565
    • DOI: 10.1038/379537a0

    Fine-scale population genetic structure and sex-biased dispersal in the smooth snake (Coronella austriaca) in southern England
    journal, February 2011

    • Pernetta, A. P.; Allen, J. A.; Beebee, T. J. C.
    • Heredity, Vol. 107, Issue 3
    • DOI: 10.1038/hdy.2011.7

    distruct: a program for the graphical display of population structure: PROGRAM NOTE
    journal, December 2003


    GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research--an update
    journal, July 2012


    FSTAT (Version 1.2): A Computer Program to Calculate F-Statistics
    journal, November 1995


    Spatial genetic analysis and long-term mark–recapture data demonstrate male-biased dispersal in a snake
    journal, November 2006

    • Keogh, J. Scott; Webb, Jonathan K.; Shine, Richard
    • Biology Letters, Vol. 3, Issue 1
    • DOI: 10.1098/rsbl.2006.0570

    Biogeography of the smooth snake ( Coronella austriaca ): origin and conservation of the northernmost population : Distribution/Conservation of the Smooth Snake
    journal, December 2014

    • Galarza, Juan A.; Mappes, Johanna; Valkonen, Janne K.
    • Biological Journal of the Linnean Society, Vol. 114, Issue 2
    • DOI: 10.1111/bij.12424

    Spatial genetic analysis of the grass snake, Natrix natrix (Squamata: Colubridae), in an intensively used agricultural landscape: SPATIAL GENETIC ANALYSIS OF NATRIX NATRIX
    journal, August 2010


    micro-checker: software for identifying and correcting genotyping errors in microsatellite data
    journal, September 2004


    genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms
    journal, December 2004


    genepop’007: a complete re-implementation of the genepop software for Windows and Linux
    journal, January 2008


    Inferring weak population structure with the assistance of sample group information
    journal, September 2009


    Permanent Genetic Resources added to Molecular Ecology Resources Database 1 May 2009-31 July 2009
    journal, November 2009


    The influence of landscape on gene flow in the eastern massasauga rattlesnake ( Sistrurus c. catenatus ): insight from computer simulations
    journal, July 2013

    • DiLeo, Michelle F.; Rouse, Jeremy D.; Dávila, José A.
    • Molecular Ecology, Vol. 22, Issue 17
    • DOI: 10.1111/mec.12411

    Conservation Genetics and Genomics of Amphibians and Reptiles
    journal, February 2015


    Discriminant analysis of principal components: a new method for the analysis of genetically structured populations
    journal, January 2010

    • Jombart, Thibaut; Devillard, Sébastien; Balloux, François
    • BMC Genetics, Vol. 11, Issue 1
    • DOI: 10.1186/1471-2156-11-94