Genetics informs meaningful intraspecific taxonomy: the black-tailed and mule deer complex
Emily K. Latch
A * and James R. Heffelfinger B
+ Author Affiliations
- Author Affiliations
A Department of Biological Sciences, University of Wisconsin-Milwaukee, Milwaukee, WI, USA.
B Terrestrial Wildlife Branch, Arizona Game and Fish Department, Phoenix, AZ, USA.
Animal Production Science 63(16) 1615-1622 https://doi.org/10.1071/AN22191
Submitted: 13 May 2022 Accepted: 12 August 2022 Published: 6 September 2022
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Meaningful intraspecific taxonomy allows for robust classification of within-species diversity and effective conservation and management. Subspecies definitions broadly agree that subspecies are groups of populations that exhibit some degree of geographic separation, phenotypic distinctiveness, and unique evolutionary potential. The most powerful assessments of within-species taxonomy are those that employ multiple lines of evidence, including phenotypic, ecological, geographic and genetic, to delineate evolutionarily definable units.
Aims: Here we describe how genetic data can be integrated into intraspecific taxonomy.
Methods: We use our experiences incorporating genetic data to assess taxonomy within black-tailed and mule deer (Odocoileus hemionus), a widespread and highly mobile species with significant phenotypic variation and a complex evolutionary history.
Key results: High-resolution sampling of individuals across the landscape and loci across the genome yielded accurate estimates of genetic variation in black-tailed and mule deer and better insight into the evolutionary processes that generate and maintain diversity.
Conclusions: Integrating genetic data has informed meaningful intraspecific taxonomy within O. hemionus, showing support for the following five subspecies: two black-tailed deer subspecies (Columbian O. h. columbianus and Sitka O. h. sitkensis) and three mule deer subspecies (mainland O. h. hemionus and the two island subspecies, O. h. cerrosensis on Cedros Island and O. h. sheldoni on Tiburón Island).
Implications: Our integrative approach provides a framework for incorporating genetic data in intraspecific taxonomy in other deer species.
Keywords: adaptation, black-tailed deer, evolutionary divergence, genetic diversity, genomics, hybridisation, integrative taxonomy, island, mule deer, North America, Odocoileus hemionus, phenotypic divergence, subspecies.
References
Alminas OSV, Heffelfinger JR, Statham MJ, Latch EK (2021) Phylogeography of Cedros and Tiburón Island mule deer in North America’s desert southwest. Journal of Heredity 112, 260–275.| Phylogeography of Cedros and Tiburón Island mule deer in North America’s desert southwest.Crossref | GoogleScholarGoogle Scholar |
Avise JC (1989) A role for molecular genetics in the recognition and conservation of endangered species. Trends in Ecology & Evolution 4, 279–281.
| A role for molecular genetics in the recognition and conservation of endangered species.Crossref | GoogleScholarGoogle Scholar |
Ba H, Li Z, Yang Y, Li C (2018) Development of diagnostic SNP markers to monitor hybridization between sika deer (Cervus nippon) and wapiti (Cervus elaphus). G3: Genes, Genomes, Genetics 8, 2173–2179.
| Development of diagnostic SNP markers to monitor hybridization between sika deer (Cervus nippon) and wapiti (Cervus elaphus).Crossref | GoogleScholarGoogle Scholar |
Baier LE (2015) ‘Inside the Equal Access to Justice Act: environmental litigation and the crippling battle over America’s lands, endangered species, and critical habitats.’ (Rowman & Littlefield: Lanham, MD, USA)
Barrowclough GF (1982) Geographic variation, predictiveness, and subspecies. The Auk 99, 601–603.
Barrowclough GF, Cracraft J, Klicka J, Zink RM (2016) How many kinds of birds are there and why does it matter? PLoS One 11, e0166307
| How many kinds of birds are there and why does it matter?Crossref | GoogleScholarGoogle Scholar |
Barton NH, Charlesworth B (1984) Genetic revolutions, founder effects, and speciation. Annual Review of Ecology and Systematics 15, 133–164.
| Genetic revolutions, founder effects, and speciation.Crossref | GoogleScholarGoogle Scholar |
Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 22, 148–155.
| Cryptic species as a window on diversity and conservation.Crossref | GoogleScholarGoogle Scholar |
Burbrink FT, Lawson R, Slowinski JB (2000) Mitochondrial DNA phylogeography of the polytypic North American rat snake (Elaphe obsoleta): a critique of the subspecies concept. Evolution 54, 2107–2118.
| Mitochondrial DNA phylogeography of the polytypic North American rat snake (Elaphe obsoleta): a critique of the subspecies concept.Crossref | GoogleScholarGoogle Scholar |
Carr SM, Hughes GA (1993) Direction of introgressive hybridization between species of North American deer (Odocoileus) as inferred from mitochondrial-cytochrome-b sequences. Journal of Mammalogy 74, 331–342.
| Direction of introgressive hybridization between species of North American deer (Odocoileus) as inferred from mitochondrial-cytochrome-b sequences.Crossref | GoogleScholarGoogle Scholar |
Carr SM, Ballinger SW, Derr JN, Blankenship LH, Bickham JW (1986) Mitochondrial DNA analysis of hybridization between sympatric white-tailed deer and mule deer in west Texas. Proceedings of the National Academy of Sciences of the United States of America 83, 9576–9580.
Cathey JC, Bickham JW, Patton JC (1998) Introgressive hybridization and nonconcordant evolutionary history of maternal and paternal lineages in North American deer. Evolution 52, 1224–1229.
| Introgressive hybridization and nonconcordant evolutionary history of maternal and paternal lineages in North American deer.Crossref | GoogleScholarGoogle Scholar |
Chafin TK, Zbinden ZD, Douglas MR, Martin BT, Middaugh CR, Gray MC, Ballard JR, Douglas ME (2021) Spatial population genetics in heavily managed species: separating patterns of historical translocation from contemporary gene flow in white-tailed deer. Evolutionary Applications 14, 1673–1689.
| Spatial population genetics in heavily managed species: separating patterns of historical translocation from contemporary gene flow in white-tailed deer.Crossref | GoogleScholarGoogle Scholar |
Clegg SM, Degnan SM, Moritz C, Estoup A, Kikkawa J, Owens IPF (2002) Microevolution in island forms: the roles of drift and directional selection in morphological divergence of a passerine bird. Evolution 56, 2090–2099.
| Microevolution in island forms: the roles of drift and directional selection in morphological divergence of a passerine bird.Crossref | GoogleScholarGoogle Scholar |
Coates DJ, Byrne M, Moritz C (2018) Genetic diversity and conservation units: dealing with the species–population continuum in the age of genomics. Frontiers in Ecology and Evolution 6, 165
| Genetic diversity and conservation units: dealing with the species–population continuum in the age of genomics.Crossref | GoogleScholarGoogle Scholar |
Colson KE, Brinkman TJ, Person DK, Hundertmark KJ (2013) Fine-scale social and spatial genetic structure in Sitka black-tailed deer. Conservation Genetics 14, 439–449.
| Fine-scale social and spatial genetic structure in Sitka black-tailed deer.Crossref | GoogleScholarGoogle Scholar |
Cook CN, Sgrò CM (2017) Aligning science and policy to achieve evolutionarily enlightened conservation. Conservation Biology 31, 501–512.
| Aligning science and policy to achieve evolutionarily enlightened conservation.Crossref | GoogleScholarGoogle Scholar |
Cook RM, Suttner B, Giglio RM, Haines ML, Latch EK (2022) Selection and demography drive range-wide patterns of MHC-DRB varaition in mule deer. BMC Ecology and Evolution 22, 42
Cowan IM (1936) Distribution and variation in deer (Genus Odocoileus) of the Pacific Coastal Region of North America. California Fish and Game 22, 155–246.
Cowan IM (1956) What and where are the mule and black-tailed deer? In ‘The deer of North America’. (Ed. WP Taylor) pp. 334–359. (Stackpole Company: Harrisburg, PA, USA)
Crispo E, Moore J-S, Lee-Yaw JA, Gray SM, Haller BC (2011) Broken barriers: human-induced changes to gene flow and introgression in animals: an examination of the ways in which humans increase genetic exchange among populations and species and the consequences for biodiversity. BioEssays 33, 508–518.
| Broken barriers: human-induced changes to gene flow and introgression in animals: an examination of the ways in which humans increase genetic exchange among populations and species and the consequences for biodiversity.Crossref | GoogleScholarGoogle Scholar |
Cronin MA (1991a) Mitochondrial and nuclear genetic relationships of deer (Odocoileus spp.) in western North America. Canadian Journal of Zoology 69, 1270–1279.
| Mitochondrial and nuclear genetic relationships of deer (Odocoileus spp.) in western North America.Crossref | GoogleScholarGoogle Scholar |
Cronin MA (1991b) Mitochondrial-DNA phylogeny of deer (Cervidae). Journal of Mammalogy 72, 553–566.
| Mitochondrial-DNA phylogeny of deer (Cervidae).Crossref | GoogleScholarGoogle Scholar |
Cronin MA, Vyse ER, Cameron DG (1988) Genetic relationships between mule deer and white-tailed deer in Montana. The Journal of Wildlife Management 52, 320–328.
| Genetic relationships between mule deer and white-tailed deer in Montana.Crossref | GoogleScholarGoogle Scholar |
de Jong JF, van Hooft P, Megens H-J, Crooijmans RPMA, de Groot GA, Pemberton JM, Huisman J, Bartoš L, Iacolina L, van Wieren SE, Ydenberg RC, Prins HHT (2020) Fragmentation and translocation distort the genetic landscape of ungulates: red deer in the Netherlands. Frontiers in Ecology and Evolution 8, 535715
| Fragmentation and translocation distort the genetic landscape of ungulates: red deer in the Netherlands.Crossref | GoogleScholarGoogle Scholar |
De Queiroz K (2007) Species concepts and species delimitation. Systematic Biology 56, 879–886.
| Species concepts and species delimitation.Crossref | GoogleScholarGoogle Scholar |
de Queiroz K (2020) An updated concept of subspecies resolves a dispute about the taxonomy of incompletely separated lineages. Herpetological Review 51, 459–461.
Degnan JH, Rosenberg NA (2009) Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends in Ecology & Evolution 24, 332–340.
| Gene tree discordance, phylogenetic inference and the multispecies coalescent.Crossref | GoogleScholarGoogle Scholar |
Fišer C, Robinson CT, Malard F (2018) Cryptic species as a window into the paradigm shift of the species concept. Molecular Ecology 27, 613–635.
| Cryptic species as a window into the paradigm shift of the species concept.Crossref | GoogleScholarGoogle Scholar |
Frankham R, Ballou JD, Dudash MR, Eldridge MDB, Fenster CB, Lacy RC, Mendelson JR, Porton IJ, Ralls K, Ryder OA (2012) Implications of different species concepts for conserving biodiversity. Biological Conservation 153, 25–31.
| Implications of different species concepts for conserving biodiversity.Crossref | GoogleScholarGoogle Scholar |
Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Molecular Ecology 10, 2741–2752.
| Adaptive evolutionary conservation: towards a unified concept for defining conservation units.Crossref | GoogleScholarGoogle Scholar |
Fuller J, Ferchaud A-L, Laporte M, Le Luyer J, Davis TB, Côté SD, Bernatchez L (2020) Absence of founder effect and evidence for adaptive divergence in a recently introduced insular population of white-tailed deer (Odocoileus virginianus). Molecular Ecology 29, 86–104.
| Absence of founder effect and evidence for adaptive divergence in a recently introduced insular population of white-tailed deer (Odocoileus virginianus).Crossref | GoogleScholarGoogle Scholar |
Gavin TA, May B (1988) Taxonomic status and genetic purity of Columbian white-tailed deer. The Journal of Wildlife Management 52, 1–10.
| Taxonomic status and genetic purity of Columbian white-tailed deer.Crossref | GoogleScholarGoogle Scholar |
Geist V (1998) ‘Deer of the world: their evolution, behaviour and ecology.’ (Stackpole Books: Mechanicsburg, PA, USA)
Gilbert MTP, Bandelt H-J, Hofreiter M, Barnes I (2005) Assessing ancient DNA studies. Trends in Ecology & Evolution 20, 541–544.
| Assessing ancient DNA studies.Crossref | GoogleScholarGoogle Scholar |
Haig SM, Beever EA, Chambers SM, Draheim HM, Dugger BD, Dunham S, Elliott-Smith EL, Fontaine JB, Kesler DC, Knaus BJ, Lopes IF, Loschl P, Mullins TD, Sheffield LM (2006) Taxonomic considerations in listing subspecies under the US Endangered Species Act. Conservation Biology 20, 1584–1594.
| Taxonomic considerations in listing subspecies under the US Endangered Species Act.Crossref | GoogleScholarGoogle Scholar |
Haines ML, Luikart G, Amish SJ, Smith S, Latch EK (2019) Evidence for adaptive introgression of exons across a hybrid swarm in deer. BMC Evolutionary Biology 19, 199
| Evidence for adaptive introgression of exons across a hybrid swarm in deer.Crossref | GoogleScholarGoogle Scholar |
Hall ER (1981) ‘The mammals of North America.’ 2nd edn. (John Wiley and Sons: New York, NY, USA)
Haynes GD, Latch EK (2012) Identification of novel single nucleotide polymorphisms (SNPs) in deer (Odocoileus spp.) using the BovineSNP50 BeadChip. PLoS One 7, e36536
| Identification of novel single nucleotide polymorphisms (SNPs) in deer (Odocoileus spp.) using the BovineSNP50 BeadChip.Crossref | GoogleScholarGoogle Scholar |
Heffelfinger JR (2000) Status of the name Odocoileus hemionus crooki (Mammalia: Cervidae). Proceedings of the Biological Society of Washington 113, 319–333.
Heffelfinger JR, Latch EK (2022) Origin, classification, and distribution. In ‘Ecology and Management of black-tailed and mule deer in North America’. (Eds JR Heffelfinger, PR Krausman) pp. 1–26. (CRC Press, Taylor and Francis Group: Boca Raton, FL, USA)
Hoffmann A, Griffin P, Dillon S, Catullo R, Rane R, Byrne M, Jordan R, Oakeshott J, Weeks A, Joseph L, Lockhart P, Borevitz J, Sgrò C (2015) A framework for incorporating evolutionary genomics into biodiversity conservation and management. Climate Change Responses 2, 1
| A framework for incorporating evolutionary genomics into biodiversity conservation and management.Crossref | GoogleScholarGoogle Scholar |
Isaac NJB, Mallet J, Mace GM (2004) Taxonomic inflation: its influence on macroecology and conservation. Trends in Ecology & Evolution 19, 464–469.
| Taxonomic inflation: its influence on macroecology and conservation.Crossref | GoogleScholarGoogle Scholar |
Kolbe JJ, Leal M, Schoener TW, Spiller DA, Losos JB (2012) Founder effects persist despite adaptive differentiation: a field experiment with lizards. Science 335, 1086–1089.
| Founder effects persist despite adaptive differentiation: a field experiment with lizards.Crossref | GoogleScholarGoogle Scholar |
LaCava MEF, Gagne RB, Gustafson KD, Oyler-McCance S, Monteith KL, Sawyer H, Kauffman MJ, Thiele DJ, Ernest HB (2021) Functional connectivity in a continuously distributed, migratory species as revealed by landscape genomics. Ecography 44, 987–999.
| Functional connectivity in a continuously distributed, migratory species as revealed by landscape genomics.Crossref | GoogleScholarGoogle Scholar |
Latch EK, Amann RP, Jacobson JP, Rhodes OE (2008) Competing hypotheses for the etiology of cryptorchidism in Sitka black-tailed deer: an evaluation of evolutionary alternatives. Animal Conservation 11, 234–246.
| Competing hypotheses for the etiology of cryptorchidism in Sitka black-tailed deer: an evaluation of evolutionary alternatives.Crossref | GoogleScholarGoogle Scholar |
Latch EK, Heffelfinger JR, Fike JA, Rhodes OE (2009) Species-wide phylogeography of North American mule deer (Odocoileus hemionus): cryptic glacial refugia and postglacial colonization. Molecular Ecology 18, 1730–1745.
| Species-wide phylogeography of North American mule deer (Odocoileus hemionus): cryptic glacial refugia and postglacial colonization.Crossref | GoogleScholarGoogle Scholar |
Latch EK, Kierepka EM, Heffelfinger JR, Rhodes OE (2011) Hybrid swarm between divergent lineages of mule deer (Odocoileus hemionus). Molecular Ecology 20, 5265–5279.
| Hybrid swarm between divergent lineages of mule deer (Odocoileus hemionus).Crossref | GoogleScholarGoogle Scholar |
Latch EK, Reding DM, Heffelfinger JR, Alcalá-Galván CH, Rhodes OE (2014) Range-wide analysis of genetic structure in a widespread, highly mobile species (Odocoileus hemionus) reveals the importance of historical biogeography. Molecular Ecology 23, 3171–3190.
| Range-wide analysis of genetic structure in a widespread, highly mobile species (Odocoileus hemionus) reveals the importance of historical biogeography.Crossref | GoogleScholarGoogle Scholar |
Martins RF, Fickel J, Le M, van Nguyen T, Nguyen HM, Timmins R, Gan HM, Rovie-Ryan JJ, Lenz D, Förster DW, Wilting A (2017) Phylogeography of red muntjacs reveals three distinct mitochondrial lineages. BMC Evolutionary Biology 17, 34
| Phylogeography of red muntjacs reveals three distinct mitochondrial lineages.Crossref | GoogleScholarGoogle Scholar |
Mayr E (1963) ‘Animal species and evolution.’ (Belknap Press: Cambridge, MA, USA)
Moritz C (1999) A molecular perspective of biodiversity. In ‘The biology of biodiversity’. (Ed. S Kato) pp. 21–34. (Springer: Tokyo, Japan)
Müller-Schwarze D, Müller-Schwarze C (1975) Subspecies specificity of response to a mammalian social odor. Journal of Chemical Ecology 1, 125–131.
| Subspecies specificity of response to a mammalian social odor.Crossref | GoogleScholarGoogle Scholar |
Oliver P, Keogh JS, Moritz C (2015) New approaches to cataloguing and understanding evolutionary diversity: a perspective from Australian herpetology. Australian Journal of Zoology 62, 417–430.
| New approaches to cataloguing and understanding evolutionary diversity: a perspective from Australian herpetology.Crossref | GoogleScholarGoogle Scholar |
Orsini L, Vanoverbeke J, Swillen I, Mergeay J, De Meester L (2013) Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization. Molecular Ecology 22, 5983–5999.
| Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization.Crossref | GoogleScholarGoogle Scholar |
Pääbo S, Poinar H, Serre D, Jaenicke-Després V, Hebler J, Rohland N, Kuch M, Krause J, Vigilant L, Hofreiter M (2004) Genetic analyses from ancient DNA. Annual Review of Genetics 38, 645–679.
| Genetic analyses from ancient DNA.Crossref | GoogleScholarGoogle Scholar |
Padial JM, Miralles A, De la Riva I, Vences M (2010) The integrative future of taxonomy. Frontiers in Zoology 7, 16
| The integrative future of taxonomy.Crossref | GoogleScholarGoogle Scholar |
Patten MA (2015) Subspecies and the philosophy of science. The Auk 132, 481–485.
| Subspecies and the philosophy of science.Crossref | GoogleScholarGoogle Scholar |
Pease KM, Freedman AH, Pollinger JP, McCormack JE, Buermann W, Rodzen J, Banks J, Meredith E, Bleich VC, Schaefer RJ, Jones K, Wayne RK (2009) Landscape genetics of California mule deer (Odocoileus hemionus): the roles of ecological and historical factors in generating differentiation. Molecular Ecology 18, 1848–1862.
| Landscape genetics of California mule deer (Odocoileus hemionus): the roles of ecological and historical factors in generating differentiation.Crossref | GoogleScholarGoogle Scholar |
Powell JH, Amish SJ, Haynes GD, Luikart G, Latch EK (2016) Candidate adaptive genes associated with lineage divergence: identifying SNPs via next-generation targeted resequencing in mule deer (Odocoileus hemionus). Molecular Ecology Resources 16, 1165–1172.
| Candidate adaptive genes associated with lineage divergence: identifying SNPs via next-generation targeted resequencing in mule deer (Odocoileus hemionus).Crossref | GoogleScholarGoogle Scholar |
Reznick DN, Ghalambor CK (2001) The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112, 183–198.
| The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution.Crossref | GoogleScholarGoogle Scholar |
Reznick E, Rodd H, Nunney L (2004) Empirical evidence for rapid evolution. In ‘Evolutionary conservation biology’. (Eds R Ferriere, U Dieckmann, D Couvet) pp. 101–118. (Cambridge University Press: Cambridge)
Russell T, Cullingham C, Ball M, Pybus M, Coltman D (2021) Extent and direction of introgressive hybridization of mule and white-tailed deer in western Canada. Evolutionary Applications 14, 1914–1925.
| Extent and direction of introgressive hybridization of mule and white-tailed deer in western Canada.Crossref | GoogleScholarGoogle Scholar |
Schaefer JA (2006) Towards maturation of the population concept. Oikos 112, 236–240.
| Towards maturation of the population concept.Crossref | GoogleScholarGoogle Scholar |
Shackleton DM (1999) ‘Hoofed mammals of British Columbia.’ (UBC Press: Vancouver, BC, Canada)
Struck TH, Feder JL, Bendiksby M, Birkeland S, Cerca J, Gusarov VI, Kistenich S, Larsson K-H, Liow LH, Nowak MD, Stedje B, Bachmann L, Dimitrov D (2018) Finding evolutionary processes hidden in cryptic species. Trends in Ecology & Evolution 33, 153–163.
| Finding evolutionary processes hidden in cryptic species.Crossref | GoogleScholarGoogle Scholar |
Świsłocka M, Matosiuk M, Ratkiewicz M, Borkowska A, Czajkowska M, Mackiewicz P (2020) Phylogeny and diversity of moose (Alces alces, Cervidae, Mammalia) revealed by complete mitochondrial genomes. Hystrix, the Italian Journal of Mammalogy 31, 1–9.
| Phylogeny and diversity of moose (Alces alces, Cervidae, Mammalia) revealed by complete mitochondrial genomes.Crossref | GoogleScholarGoogle Scholar |
Taylor WP (1956) ‘The deer of North America.’ (Stackpole Books: Harrisburg, PA, USA)
Vogler AP, Desalle R (1994) Diagnosing units of conservation management. Conservation Biology 8, 354–363.
| Diagnosing units of conservation management.Crossref | GoogleScholarGoogle Scholar |
Wallmo OC (1981) Distribution and habits. In ‘Mule and black-tailed deer of North America’. (Ed. OC Wallmo) pp. 1–26. (Wildlife Management Institute and University of Nebraska Press: Lincoln, NE, USA)
Wandeler P, Hoeck PEA, Keller LF (2007) Back to the future: museum specimens in population genetics. Trends in Ecology & Evolution 22, 634–642.
| Back to the future: museum specimens in population genetics.Crossref | GoogleScholarGoogle Scholar |
Waples RS (1995) Evolutionarily significant units and the conservation of biological diversity under the Endangered Species Act. In ‘Evolution and the aquatic ecosystem: defining unique units in population conservation’. (Eds JL Nielsen, GA Powers) pp. 8–27. (American Fisheries Society: Bethesda, MD, USA)
Waples RS, Gustafson RG, Weitkamp LA, Myers JM, Johnson OW, Busby PJ, Hard JJ, Bryant GJ, Waknitz FW, Nelly K, Teel D, Grant WS, Winans GA, Phelps S, Marshall A, Baker BM (2001) Characterizing diversity in salmon from the Pacific Northwest. Journal of Fish Biology 59, 1–41.
| Characterizing diversity in salmon from the Pacific Northwest.Crossref | GoogleScholarGoogle Scholar |
Willerslev E, Cooper A (2005) Ancient DNA. Proceedings of the Royal Society B: Biological Sciences 272, 3–16.
| Ancient DNA.Crossref | GoogleScholarGoogle Scholar |
Wilson EO, Brown WL (1953) The subspecies concept and its taxonomic application. Systematic Zoology 2, 97–111.
| The subspecies concept and its taxonomic application.Crossref | GoogleScholarGoogle Scholar |
Yeates DK, Seago A, Nelson L, Cameron SL, Joseph L, Trueman JWH (2011) Integrative taxonomy, or iterative taxonomy? Systematic Entomology 36, 209–217.
| Integrative taxonomy, or iterative taxonomy?Crossref | GoogleScholarGoogle Scholar |
Zamudio KR, Bell RC, Mason NA (2016) Phenotypes in phylogeography: species’ traits, environmental variation, and vertebrate diversification. Proceedings of the National Academy of Sciences of the United States of America 113, 8041–8048.
| Phenotypes in phylogeography: species’ traits, environmental variation, and vertebrate diversification.Crossref | GoogleScholarGoogle Scholar |
Zhu L, Deng C, Zhao X, Ding J, Huang H, Zhu S, Wang Z, Qin S, Ding Y, Lu G, Yang Z (2018) Endangered Père David’s deer genome provides insights into population recovering. Evolutionary Applications 11, 2040–2053.
| Endangered Père David’s deer genome provides insights into population recovering.Crossref | GoogleScholarGoogle Scholar |
Zink RM (2004) The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proceedings of the Royal Society of London B: Biological Sciences 271, 561–564.
| The role of subspecies in obscuring avian biological diversity and misleading conservation policy.Crossref | GoogleScholarGoogle Scholar |
