Mitochondrial Genomes of the United States Distribution of Gray Fox (Urocyon cinereoargenteus) Reveal a Major Phylogeographic Break at the Great Plains Suture Zone
Abstract
We examined phylogeographic structure in gray fox (Urocyon cinereoargenteus) across the United States to identify the location of secondary contact zone(s) between eastern and western lineages and investigate the possibility of additional cryptic intraspecific divergences. We generated and analyzed complete mitochondrial genome sequence data from 75 samples and partial control region mitochondrial DNA sequences from 378 samples to investigate levels of genetic diversity and structure through population- and individual-based analyses including estimates of divergence (FST and SAMOVA), median joining networks, and phylogenies. We used complete mitochondrial genomes to infer phylogenetic relationships and date divergence times of major lineages of Urocyon in the United States. Despite broad-scale sampling, we did not recover additional major lineages of Urocyon within the United States, but identified a deep east-west split (~0.8 million years) with secondary contact at the Great Plains Suture Zone and confirmed the Channel Island fox (Urocyon littoralis) is nested within U. cinereoargenteus. Genetic diversity declined at northern latitudes in the eastern United States, a pattern concordant with post-glacial recolonization and range expansion. Beyond the east-west divergence, morphologically-based subspecies did not form monophyletic groups, though unique haplotypes were often geographically limited. Gray foxes in the United States displayed a deep, cryptic divergencemore »
- Authors:
-
- Luther College, Decorah, IA (United States). Dept. of Biology
- National Zoological Park, Washington, DC (United States). Smithsonian Conservation Biology Inst. Center for Conservation Genomics; George Mason Univ., Fairfax, VA (United States). Dept. of Biology; Smithsonian-Mason School of Conservation, Front Royal, VA (United States)
- National Zoological Park, Washington, DC (United States). Smithsonian Conservation Biology Inst. Center for Conservation Genomics
- Univ. of Delaware, Newark, DE (United States). Dept. of Entomology and Wildlife Ecology
- Savannah River Site (SRS), Aiken, SC (United States). Savannah River Ecology Lab. (SREL)
- Missouri Department of Conservation, Columbia, MO (United States)
- Iowa State Univ., Ames, IA (United States). Dept. o fEcology, Evolution, and Organismal Biology
- National Zoological Park, Washington, DC (United States). Smithsonian Conservation Biology Inst. Center for Conservation Genomics; George Mason Univ., Fairfax, VA (United States). Dept. of Biology
- Publication Date:
- Research Org.:
- Univ. of Georgia, Athens, GA (United States)
- Sponsoring Org.:
- USDOE Office of Environmental Management (EM)
- OSTI Identifier:
- 1848976
- Grant/Contract Number:
- EM0004391
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Ecology and Evolution
- Additional Journal Information:
- Journal Volume: 9; Journal ID: ISSN 2296-701X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; environmental sciences & ecology; Great Plains Suture Zone, mammal; mitogenome; phylogeography; secondary contact; subspecies
Citation Formats
Reding, Dawn M., Castañeda-Rico, Susette, Shirazi, Sabrina, Hofman, Courtney A., Cancellare, Imogene A., Lance, Stacey L., Beringer, Jeff, Clark, William R., and Maldonado, Jesus E. Mitochondrial Genomes of the United States Distribution of Gray Fox (Urocyon cinereoargenteus) Reveal a Major Phylogeographic Break at the Great Plains Suture Zone. United States: N. p., 2021.
Web. doi:10.3389/fevo.2021.666800.
Reding, Dawn M., Castañeda-Rico, Susette, Shirazi, Sabrina, Hofman, Courtney A., Cancellare, Imogene A., Lance, Stacey L., Beringer, Jeff, Clark, William R., & Maldonado, Jesus E. Mitochondrial Genomes of the United States Distribution of Gray Fox (Urocyon cinereoargenteus) Reveal a Major Phylogeographic Break at the Great Plains Suture Zone. United States. https://doi.org/10.3389/fevo.2021.666800
Reding, Dawn M., Castañeda-Rico, Susette, Shirazi, Sabrina, Hofman, Courtney A., Cancellare, Imogene A., Lance, Stacey L., Beringer, Jeff, Clark, William R., and Maldonado, Jesus E. Tue .
"Mitochondrial Genomes of the United States Distribution of Gray Fox (Urocyon cinereoargenteus) Reveal a Major Phylogeographic Break at the Great Plains Suture Zone". United States. https://doi.org/10.3389/fevo.2021.666800. https://www.osti.gov/servlets/purl/1848976.
@article{osti_1848976,
title = {Mitochondrial Genomes of the United States Distribution of Gray Fox (Urocyon cinereoargenteus) Reveal a Major Phylogeographic Break at the Great Plains Suture Zone},
author = {Reding, Dawn M. and Castañeda-Rico, Susette and Shirazi, Sabrina and Hofman, Courtney A. and Cancellare, Imogene A. and Lance, Stacey L. and Beringer, Jeff and Clark, William R. and Maldonado, Jesus E.},
abstractNote = {We examined phylogeographic structure in gray fox (Urocyon cinereoargenteus) across the United States to identify the location of secondary contact zone(s) between eastern and western lineages and investigate the possibility of additional cryptic intraspecific divergences. We generated and analyzed complete mitochondrial genome sequence data from 75 samples and partial control region mitochondrial DNA sequences from 378 samples to investigate levels of genetic diversity and structure through population- and individual-based analyses including estimates of divergence (FST and SAMOVA), median joining networks, and phylogenies. We used complete mitochondrial genomes to infer phylogenetic relationships and date divergence times of major lineages of Urocyon in the United States. Despite broad-scale sampling, we did not recover additional major lineages of Urocyon within the United States, but identified a deep east-west split (~0.8 million years) with secondary contact at the Great Plains Suture Zone and confirmed the Channel Island fox (Urocyon littoralis) is nested within U. cinereoargenteus. Genetic diversity declined at northern latitudes in the eastern United States, a pattern concordant with post-glacial recolonization and range expansion. Beyond the east-west divergence, morphologically-based subspecies did not form monophyletic groups, though unique haplotypes were often geographically limited. Gray foxes in the United States displayed a deep, cryptic divergence suggesting taxonomic revision is needed. Secondary contact at a common phylogeographic break, the Great Plains Suture Zone, where environmental variables show a sharp cline, suggests ongoing evolutionary processes may reinforce this divergence. Follow-up study with nuclear markers should investigate whether hybridization is occurring along the suture zone and characterize contemporary population structure to help identify conservation units. Comparative work on other wide-ranging carnivores in the region should test whether similar evolutionary patterns and processes are occurring.},
doi = {10.3389/fevo.2021.666800},
journal = {Frontiers in Ecology and Evolution},
number = ,
volume = 9,
place = {United States},
year = {Tue Jun 08 00:00:00 EDT 2021},
month = {Tue Jun 08 00:00:00 EDT 2021}
}
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Works referenced in this record:
Potential of Multivariate Quantitative Methods for Delineation and Visualization of Ecoregions
journal, April 2004
- Hargrove, William W.; Hoffman, Forrest M.
- Environmental Management, Vol. 34, Issue S1
Morphological Variation and Evolution in Some North American Orioles
journal, December 1970
- Rising, James D.
- Systematic Zoology, Vol. 19, Issue 4
Phylogeography of striped skunks ( Mephitis mephitis ) in North America: Pleistocene dispersal and contemporary population structure
journal, February 2012
- Barton, Heather D.; Wisely, Samantha M.
- Journal of Mammalogy, Vol. 93, Issue 1
Ice sheets promote speciation in boreal birds
journal, September 2004
- Weir, Jason T.; Schluter, Dolph
- Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 271, Issue 1551
The Neotoma Paleoecology Database, a multiproxy, international, community-curated data resource
journal, January 2018
- Williams, John W.; Grimm, Eric C.; Blois, Jessica L.
- Quaternary Research, Vol. 89, Issue 1
Predicting dispersal distance in mammals: a trait-based approach
journal, August 2012
- Whitmee, Sarah; Orme, C. David L.
- Journal of Animal Ecology, Vol. 82, Issue 1
Phylogeography and pleistocene evolution in the North American black bear
journal, November 1997
- Wooding, S.; Ward, R.
- Molecular Biology and Evolution, Vol. 14, Issue 11
Phylogeography of the North American red fox: vicariance in Pleistocene forest refugia
journal, June 2009
- Aubry, Keith B.; Statham, Mark J.; Sacks, Benjamin N.
- Molecular Ecology, Vol. 18, Issue 12
Genetic Diversity and Conservation Units: Dealing With the Species-Population Continuum in the Age of Genomics
journal, October 2018
- Coates, David J.; Byrne, Margaret; Moritz, Craig
- Frontiers in Ecology and Evolution, Vol. 6
The role of historical and contemporary processes on phylogeographic structure and genetic diversity in the Northern Cardinal, Cardinalis cardinalis
journal, May 2011
- Smith, Brian Tilston; Escalante, Patricia; Hernández Baños, Blanca E.
- BMC Evolutionary Biology, Vol. 11, Issue 1
Mitogenomics of the Speartooth Shark challenges ten years of control region sequencing
journal, November 2014
- Feutry, Pierre; Kyne, Peter M.; Pillans, Richard D.
- BMC Evolutionary Biology, Vol. 14, Issue 1
The Importance of Recent Ice Ages in Speciation: A Failed Paradigm
journal, September 1997
- Klicka, John; Zink, Robert M.
- Science, Vol. 277, Issue 5332
Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7
journal, April 2018
- Rambaut, Andrew; Drummond, Alexei J.; Xie, Dong
- Systematic Biology, Vol. 67, Issue 5
Combining ecological niche modelling and morphology to assess the range-wide population genetic structure of bobcats ( Lynx rufus )
journal, November 2015
- Loveless, Allison M.; Reding, Dawn M.; Kapfer, Paul M.
- Biological Journal of the Linnean Society, Vol. 117, Issue 4
Phylogeographic Analyses of American Black Bears ( Ursus americanus ) Suggest Four Glacial Refugia and Complex Patterns of Postglacial Admixture
journal, May 2015
- Puckett, Emily E.; Etter, Paul D.; Johnson, Eric A.
- Molecular Biology and Evolution, Vol. 32, Issue 9
BEAST 2: A Software Platform for Bayesian Evolutionary Analysis
journal, April 2014
- Bouckaert, Remco; Heled, Joseph; Kühnert, Denise
- PLoS Computational Biology, Vol. 10, Issue 4
Convenient single-step, one tube purification of PCR products for direct sequencing
journal, January 1994
- Werle, E.; Schneider, C.; Renner, M.
- Nucleic Acids Research, Vol. 22, Issue 20
Genetic structure of raccoons in eastern North America based on mtDNA: implications for subspecies designation and rabies disease dynamics
journal, September 2008
- Cullingham, C. I.; Kyle, C. J.; Pond, B. A.
- Canadian Journal of Zoology, Vol. 86, Issue 9
Mitochondrial Genomes Suggest Rapid Evolution of Dwarf California Channel Islands Foxes (Urocyon littoralis)
journal, February 2015
- Hofman, Courtney A.; Rick, Torben C.; Hawkins, Melissa T. R.
- PLOS ONE, Vol. 10, Issue 2
Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows
journal, May 2010
- Excoffier, Laurent; Lischer, Heidi E. L.
- Molecular Ecology Resources, Vol. 10, Issue 3
An Evaluation of Narrow Hybrid Zones in Vertebrates
journal, September 1977
- Moore, William S.
- The Quarterly Review of Biology, Vol. 52, Issue 3
Phylogeography of the deer mouse (Peromyscus maniculatus) provides a predictive framework for research on hantaviruses
journal, July 2006
- Dragoo, Jerry W.; Lackey, J. Alden; Moore, Kathryn E.
- Journal of General Virology, Vol. 87, Issue 7
Spatial mixing of mitochondrial lineages and greater genetic diversity in some invasive populations of the American mink (Neovison vison) compared to native populations
journal, June 2017
- García, Karla; Melero, Yolanda; Palazón, Santiago
- Biological Invasions, Vol. 19, Issue 9
Global Changes During the Last 3 Million Years: Climatic Controls and Biotic Responses
journal, November 1992
- Webb, T.; Bartlein, P. J.
- Annual Review of Ecology and Systematics, Vol. 23, Issue 1
Phylogeography of the gray fox (Urocyon cinereoargenteus) in the eastern United States
journal, April 2011
- Bozarth, Christine A.; Lance, Stacey L.; Civitello, David J.
- Journal of Mammalogy, Vol. 92, Issue 2
The tempo of avian diversification during the Quaternary
journal, February 2004
- Zink, Robert M.; Klicka, John; Barber, Brian R.
- Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 359, Issue 1442
Post-glacial colonization of northwestern North America by the forest-associated American marten (Martes americana, Mammalia: Carnivora: Mustelidae)
journal, October 2002
- Stone, Karen D.; Flynn, Rodney W.; Cook, Joseph A.
- Molecular Ecology, Vol. 11, Issue 10
Urocyon cinereoargenteus
journal, November 1982
- Fritzell, Erik K.; Haroldson, Kurt J.
- Mammalian Species, Issue 189
Mitochondrial genome sequences illuminate maternal lineages of conservation concern in a rare carnivore
journal, April 2011
- Knaus, Brian J.; Cronn, Richard; Liston, Aaron
- BMC Ecology, Vol. 11, Issue 1
Genetic variation in the eastern spotted skunk (Spilogale putorius) with emphasis on the plains spotted skunk (S. p. interrupta)
journal, August 2018
- Shaffer, Alexandra A.; Dowler, Robert C.; Perkins, J. Clint
- Journal of Mammalogy, Vol. 99, Issue 5
Pleistocene Refugia and Holocene Expansion of a Grassland-Dependent Species, the Black-Footed Ferret ( Mustela nigripes )
journal, February 2008
- Wisely, Samantha M.; Statham, Mark J.; Fleischer, Robert C.
- Journal of Mammalogy, Vol. 89, Issue 1
Median-joining networks for inferring intraspecific phylogenies
journal, January 1999
- Bandelt, H. J.; Forster, P.; Rohl, A.
- Molecular Biology and Evolution, Vol. 16, Issue 1
Some genetic consequences of ice ages, and their role in divergence and speciation
journal, July 1996
- Hewitt, G.
- Biological Journal of the Linnean Society, Vol. 58, Issue 3
Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers.
journal, August 1989
- Kocher, T. D.; Thomas, W. K.; Meyer, A.
- Proceedings of the National Academy of Sciences, Vol. 86, Issue 16
Do Suture Zones Exist?
journal, January 2004
- Swenson, Nathan G.; Howard, Daniel J.
- Evolution, Vol. 58, Issue 11
Mitochondrial Analysis of the Most Basal Canid Reveals Deep Divergence between Eastern and Western North American Gray Foxes (Urocyon spp.) and Ancient Roots in Pleistocene California
journal, August 2015
- Goddard, Natalie S.; Statham, Mark J.; Sacks, Benjamin N.
- PLOS ONE, Vol. 10, Issue 8
Integrating Fossils with Molecular Phylogenies Improves Inference of Trait Evolution: Fossils, Phylogenies, and Models of Trait Evolution
journal, July 2012
- Slater, Graham J.; Harmon, Luke J.; Alfaro, Michael E.
- Evolution, Vol. 66, Issue 12
MRBAYES: Bayesian inference of phylogenetic trees
journal, August 2001
- Huelsenbeck, J. P.; Ronquist, F.
- Bioinformatics, Vol. 17, Issue 8
Small-scale genetic structure of American black bears illustrates potential postglacial recolonization routes
journal, June 2011
- Pelletier, Agnès; Obbard, Martyn E.; White, Bradley N.
- Journal of Mammalogy, Vol. 92, Issue 3
DnaSP v5: a software for comprehensive analysis of DNA polymorphism data
journal, April 2009
- Librado, P.; Rozas, J.
- Bioinformatics, Vol. 25, Issue 11
The genetic legacy of the Quaternary ice ages
journal, June 2000
- Hewitt, Godfrey
- Nature, Vol. 405, Issue 6789
Whole mitochondrial genomes illuminate ancient intercontinental dispersals of grey wolves ( Canis lupus )
journal, June 2016
- Koblmüller, Stephan; Vilà, Carles; Lorente-Galdos, Belen
- Journal of Biogeography, Vol. 43, Issue 9
Genetic consequences of climatic oscillations in the Quaternary
journal, February 2004
- Hewitt, G. M.
- Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 359, Issue 1442
Genetic footprints of demographic expansion in North America, but not Amazonia, during the Late Quaternary
journal, August 2003
- Lessa, E. P.; Cook, J. A.; Patton, J. L.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 18
The impact of global climate change on genetic diversity within populations and species
journal, December 2012
- Pauls, Steffen U.; Nowak, Carsten; Bálint, Miklós
- Molecular Ecology, Vol. 22, Issue 4
GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research--an update
journal, July 2012
- Peakall, R.; Smouse, P. E.
- Bioinformatics, Vol. 28, Issue 19
A test of the Endogenous and Exogenous Selection Hypotheses for the Maintenance of a Narrow Avian Hybrid zone
journal, March 2003
- Bronson, C. L.; Grubb, Thomas C.; Braun, Michael J.
- Evolution, Vol. 57, Issue 3
Spatial Response of Mammals to Late Quaternary Environmental Fluctuations
journal, June 1996
- FAUNMAP Working Group:, ; Graham, R. W.; Lundelius, E. L.
- Science, Vol. 272, Issue 5268
Impact of Quaternary climatic changes and interspecific competition on the demographic history of a highly mobile generalist carnivore, the coyote
journal, April 2012
- Koblmüller, Stephan; Wayne, Robert K.; Leonard, Jennifer A.
- Biology Letters, Vol. 8, Issue 4
A comparison of metabolism and evaporative water loss of baltimore and bullock orioles
journal, December 1969
- Rising, James D.
- Comparative Biochemistry and Physiology, Vol. 31, Issue 6
Pleistocene and ecological effects on continental-scale genetic differentiation in the bobcat ( Lynx rufus ): CONTINENTAL GENETIC STRUCTURE OF BOBCATS
journal, April 2012
- Reding, Dawn M.; Bronikowski, Anne M.; Johnson, Warren E.
- Molecular Ecology, Vol. 21, Issue 12
Mapping amphibian contact zones and phylogeographical break hotspots across the United States: U.S. AMPHIBIAN DIVERGENCE HOTSPOT ZONES
journal, November 2010
- Rissler, Leslie J.; Smith, Walter H.
- Molecular Ecology, Vol. 19, Issue 24
Out of the tropics: a phylogeographic history of the long-tailed weasel, Mustela frenata
journal, September 2012
- Harding, Larisa E.; Dragoo, Jerry W.
- Journal of Mammalogy, Vol. 93, Issue 4
Phylogeography of a widespread small carnivore, the western spotted skunk ( Spilogale gracilis ) reveals temporally variable signatures of isolation across western North America
journal, May 2017
- Ferguson, Adam W.; McDonough, Molly M.; Guerra, Gema I.
- Ecology and Evolution, Vol. 7, Issue 12
Genomic ancestry of the American puma (Puma concolor)
journal, May 2000
- Culver, M.
- Journal of Heredity, Vol. 91, Issue 3
Global patterns of connectivity and isolation of populations of forest bird species in the late Pleistocene: Global range connectivity
journal, December 2012
- Peterson, A. Townsend; Ammann, Caspar M.
- Global Ecology and Biogeography, Vol. 22, Issue 5
Effects of Quaternary Climatic Change on Speciation in Mammals
journal, June 2005
- Barnosky, Anthony D.
- Journal of Mammalian Evolution, Vol. 12, Issue 1-2
Molecular Phylogeny of Short-Tailed Shrews, Blarina (Insectivora: Soricidae)
journal, February 2002
- Brant, Sara V.; Ortı́, Guillermo
- Molecular Phylogenetics and Evolution, Vol. 22, Issue 2
New Mitochondrial dna data Affirm the Importance of Pleistocene Speciation in North American Birds
journal, January 2004
- Johnson, Ned K.; Cicero, Carla
- Evolution, Vol. 58, Issue 5
Molecular systematics and Pleistocene biogeography of Mesoamerican flying squirrels
journal, June 2010
- Kerhoulas, Nicholas J.; Arbogast, Brian S.
- Journal of Mammalogy, Vol. 91, Issue 3
MrBayes 3: Bayesian phylogenetic inference under mixed models
journal, August 2003
- Ronquist, Fredrik; Huelsenbeck, John P.
- Bioinformatics, Vol. 19, Issue 12, p. 1572-1574
High gene flow in the American badger overrides habitat preferences and limits broadscale genetic structure
journal, August 2016
- Kierepka, E. M.; Latch, E. K.
- Molecular Ecology, Vol. 25, Issue 24
Gis-based niche models reveal unifying climatic mechanisms that maintain the location of avian hybrid zones in a North American suture zone
journal, May 2006
- Swenson, N. G.
- Journal of Evolutionary Biology, Vol. 19, Issue 3
genalex 6: genetic analysis in Excel. Population genetic software for teaching and research
journal, March 2006
- Peakall, Rod; Smouse, Peter E.
- Molecular Ecology Notes, Vol. 6, Issue 1
Ecological and genetic spatial structuring in the Canadian lynx
journal, September 2003
- Rueness, Eli Knispel; Stenseth, Nils Chr.; O'Donoghue, Mark
- Nature, Vol. 425, Issue 6953
jModelTest 2: more models, new heuristics and parallel computing
journal, July 2012
- Darriba, Diego; Taboada, Guillermo L.; Doallo, Ramón
- Nature Methods, Vol. 9, Issue 8
Ecological Change, Range Fluctuations and Population Dynamics during the Pleistocene
journal, July 2009
- Hofreiter, Michael; Stewart, John
- Current Biology, Vol. 19, Issue 14
Glacial cycles and the tempo of avian speciation
journal, February 2005
- Lovette, I.
- Trends in Ecology & Evolution, Vol. 20, Issue 2