Abstract
The divergence between the Andean fox (Lycalopex culpaeus) and the South American gray fox (L. griseus) represents a recent speciation event in South America. These taxa are partially sympatric and share biological, morphological, and ecological traits. Previous studies failed to recover reciprocal monophyly, suggesting the occurrence of introgression or incomplete lineage sorting (ILS). Here, we obtained mitochondrial and nuclear markers for 140 L. culpaeus and 134 L. griseus from the Southern Cone of South America to assess their inter and intraspecific divergence. We recovered reciprocal monophyly of L. culpaeus and L. griseus, with mild signatures of introgression or ILS. Therefore, taxonomic misidentification and the use of a limited number of markers may be the main reason behind the past debate about the delimitation of both species. Two main divergent clades were found in L. culpaeus with a phylogeographical boundary in the High Plateau of northeastern Chile. The southern clade along with three northern sub-clades corresponded to four morphological subspecies. Less genetic differentiation was found in L. griseus with a spatial population structure that does not support the occurrence of distinct subspecies. The results found in this study suggest the extant evolutionary significant units that need to be considered for biological conservation management of these species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All haplotypes found in this study were deposited in GenBank under accession numbers OM169041-OM169067, OM677763 (L. culpaeus CR), OM169012-OM169040 (L. griseus CR), OM169082-OM169102 (L. culpaeus MT-CYB), OM169068-OM169081 (L. griseus MT-CYB), OM169113 (L. culpaeus FES), and OM169103-OM169112 (L. griseus FES).
References
Aljanabi SM, Martinez I (1997) Universal and rapid salt−extraction of high quality genomic DNA for PCR−based techniques. Nucl Acids Res 25:4692–4693. https://doi.org/10.1093/nar/25.22.4692
Álvarez-Varas R, González-Acuña D, Vianna JA (2015) Comparative phylogeography of co−distributed Phrygilus species (Aves, Thraupidae) from the Central Andes. Mol Phylogenet Evol 90:150–163. https://doi.org/10.1016/j.ympev.2015.04.009
Atalah GA, Sieldfeld KW, Venegas Canelo C (1980) Antecedentes sobre el nicho trófico de Canis g. griseus Gray 1836 en Tierra del Fuego. An Inst Patagon 11:259–271
Bandelt HJ, Forster P, Röhl A (1999) Median−joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Berta A (1987) Origin, diversification, and zoogeography of the South American Canidae. In: Patterson BD, Timm RM (eds) Studies in neotropical mammalogy: essays in honor of Philip Hershkovitz, 39. Zoology, United States of America, Fieldiana, Chicago, Ill, Field Museum of Natural History, pp 455–471. Available at: https://archive.org/details/cbarchive_34134_origindiversificationandzoogeo1987
Bininda-Emonds ORP, Gittleman JL, Purvis A (1999) Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biol Rev 74:143–175. https://doi.org/10.1111/j.1469−185X.1999.tb00184.x
Boutin-Ganache I, Raposo M, Raymond M, Deschepper CF (2001) M13−tailed primers improve the readability and usability of microsatellite analyses performed with two different allele− sizing methods. BioTechniques 31:25–28. https://doi.org/10.2144/01311bm02
Cabello JE, Dávila JA (2014) Isolation and characterization of microsatellite loci in Darwin’s fox (Lycalopex fulvipes) and cross−amplification in other canid species. Conserv Genet Resour 6:759–761. https://doi.org/10.1007/s12686−014−0208−6
Cabrera A (1931) On some South American Canine Genera. J Mammal 12:54–67. https://doi.org/10.2307/1373806
Chavez DE, Gronau I, Hains T, Dikow RB, Frandsen PB, Figueiró HV et al (2022) Comparative genomics uncovers the evolutionary history, demography, and molecular adaptations of South American canids. PNAS 119:e2205986119. https://doi.org/10.1073/pnas.2205986119
de Moura Bubadué J, Cáceres N, dos Santos Carvalho R, Meloro C (2016a) Ecogeographical variation in skull shape of South−American canids: abiotic or biotic processes? Evol Biol 43:145–159. https://doi.org/10.1007/s11692−015−9362−3
de Moura Bubadué J, Cáceres N, dos Santos Carvalho R, Sponchiado J, Passaro F, Saggese F et al (2016b) Character displacement under influence of Bergmann’s rule in Cerdocyon thous (Mammalia: Canidae). Hystrix 27:1–8. https://doi.org/10.4404/hystrix−27.2−11433
Di Cataldo S, Cevidanes A, Ulloa-Contreras C, Sacristán I, Peñaloza-Madrid D, Vianna J, González-Acuña D, Sallaberry-Pincheira N, Cabello J, Napolitano C, Hidalgo-Hermoso E, Acosta-Jamett G, Millán J (2021) Widespread infection with hemotropic mycoplasmas in free-ranging dogs and wild foxes across six bioclimatic regions of Chile. Microorganisms 9:919. https://doi.org/10.3390/microorganisms9050919
Díaz-Ruiz F, Rodríguez A, Procopio D, Zapata S, Zanón-Martínez JI, Travaini A (2020) Inferring species interactions from long-term monitoring programs: carnivores in a protected area from Southern Patagonia. Diversity 12:319. https://doi.org/10.3390/d12090319
Donadio E, Buskirk SW (2006) Diet, Morphology, and interspecific killing in Carnivora. Am Nat 167:524–536. https://doi.org/10.1086/501033
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686−011−9548−7
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365−294X.2005.02553.x
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. https://doi.org/10.1111/j.1755−0998.2010.02847.x
Favarini MO, Simão TL, Macedo GS, Garcez FS, Oliveira LR, Cárdenas-Alayza S et al (2022) Complex evolutionary history of the South American fox genus Lycalopex (Mammalia, Carnivora, Canidae) inferred from multiple mitochondrial and nuclear markers. Diversity 14:642. https://doi.org/10.3390/d14080642
Francisco LV, Langsten AA, Mellersh CS, Neal CL, Ostrander EA (1996) A class of highly polymorphic tetranucleotide repeats for canine genetic mapping. Mamm Genome 7:359–362. https://doi.org/10.1007/s003359900104
Fuentes ER, Jaksic FM (1979) Latitudinal size variation of chilean foxes: tests of alternative hypotheses. Ecology 60:43–47. https://doi.org/10.2307/1936466
Galende GI, Raffaele E (2016) Predator feeding ecology on Patagonian rocky outcrops: implications for colonies of mountain vizcacha (Lagidium viscacia). Stud Neotrop Fauna Environ 51:104–111. https://doi.org/10.1080/01650521.2016.1185270
González del Solar R, Rau J (2004) Chilla. Pseudalopex griseus (Gray, 1837). In: Sillero-Zubiri C, Hoffmann M, Macdonald DW (eds) Canids: foxes, wolves, jackals and dogs: status survey and conservation action plan. IUCN/SSC Canid Specialist Group Gland, Switzerland and Cambridge, pp 56–63. Available at: https://portals.iucn.org/library/node/8500. Accessed 9 April 2021
Gopalakrishnan S, Sinding MHS, Ramos-Madrigal J, Niemann J, Castruita JAS, Vieira FG et al (2018) Interspecific gene flow shaped the evolution of the genus Canis. Curr Biol 28:3441–3449. https://doi.org/10.1016/j.cub.2018.08.041
Guerrero PC, Rosas M, Arroyo MTK, Wiens JJ (2013) Evolutionary lag times in an ancient desert. PNAS 110:11469–11474. https://doi.org/10.1073/pnas.1308721110
Guillot G, Mortier F, Estoup A (2005) Geneland: a computer package for landscape genetics. Mol Ecol Notes 5:712–715. https://doi.org/10.1111/j.1471−8286.2005.01031.x
Guzmán JA, D’Elía G, Ortiz JC (2009) Variación geográfica del zorro Lycalopex culpaeus (Mammalia, Canidae) en Chile: implicaciones taxonómicas. RBT 57:421–432. https://doi.org/10.15517/rbt.v57i1−2.11358
Guzmán-Sandoval J, Sielfeld W, Ferrú M (2007) Diet of Lycalopex culpaeus (Mammalia: Canidae) in Northernmost Chile (Tarapaca Region). Gayana 71:1–7. https://doi.org/10.4067/S0717-65382007000100001
Hindrikson M, Männil P, Ozolins J, Krzywinski A, Saarma U (2012) Bucking the trend in wolf−dog hybridization: first evidence from Europe of hybridization between female dogs and male wolves. PLoS ONE 7:e46465. https://doi.org/10.1371/journal.pone.0046465
Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332. https://doi.org/10.1111/j.1755−0998.2009.02591.x
Iriarte A (2008) Lycalopex culpaeus. In: Mamíferos de Chile, Primera Edición. Lynx Ediciones, Barcelona, pp 237–239
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. https://doi.org/10.1093/bioinformatics/btm233
Jayat JP, Barquez RM, Díaz MM (1999) Aportes al conocimiento de la distribución de los carnívoros del noroeste de Argentina. Mastozool Neotrop 6:15–30
Jiménez JE, Yáñez JL, Tabilo EL, Jaksić FM (1995) Body size of Chilean foxes: a new pattern in light of new data. Acta Theriol 40:321–326. https://doi.org/10.4098/AT.arch.95−31
Jiménez J, Yañez JL, Tabilo EL, Jaksic FM (1996) Niche−complementarity of South American foxes: reanalysis and test of a hypothesis. Rev Chil De Hist Nat 63:113–123
Jiménez JE, Novaro AJ (2004) Culpeo. Pseudalopex culpaeus (Molina, 1782). In: Sillero-Zubiri C, Hoffmann M, Macdonald DW (eds) Canids: foxes, wolves, jackals and dogs: status survey and conservation action plan. IUCN/SSC Canid Specialist Group, Gland, pp 44–49. Available at: https://portals.iucn.org/library/node/8500. Accessed 9 April 2021
Johnson WE, Franklin WL (1994) Spatial resource partitioning by sympatric grey fox (Dusicyon griseus) and culpeo fox (Dusicyon culpaeus) in southern Chile. Can J Zool 72:1788–1793. https://doi.org/10.1139/z94−242
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. https://doi.org/10.1186/1471−2156−11−94
Lagos N, Villalobos R, Vianna JA, Espinosa-Miranda C, Rau JR, Iriarte A (2021) The spatial and trophic ecology of culpeo foxes (Lycalopex culpaeus) in the high Andes of northern Chile. Stud Neotrop Fauna Environ https://doi.org/10.1080/01650521.2021.2005393
Lancaster ML, Gemmell NJ, Negro S, Goldsworthy S, Sunnucks P (2006) Ménage à trois on Macquarie Island: hybridization among three species of fur seal (Arctocephalus spp.) following historical population extinction. Mol Ecol 15:3681–3692. https://doi.org/10.1111/j.1365−294X.2006.03041.x
Lehman N, Eisenhawer A, Hansen K, Mech LD, Peterson RO, Gogan PJP et al (1991) Introgression of coyote mitochondrial Dna into sympatric North American gray wolf populations. Evolution 45:104–119. https://doi.org/10.1111/j.1558−5646.1991.tb05270.x
Lucherini M (2016a) Lycalopex culpaeus. IUCN Red List of Threatened Species. https://doi.org/10.2305/IUCN.UK.2016−1.RLTS.T6929A85324366.en
Lucherini M (2016b) Lycalopex griseus (errata version published in 2017). IUCN Red List of Threatened Species. https://doi.org/10.2305/IUCN.UK.2016−1.RLTS.T6927A86440397.en
Machado FA (2020) Selection and constraints in the ecomorphological adaptive evolution of the skull of living Canidae (Carnivora, Mammalia). Am Nat 196:197–215. https://doi.org/10.1086/709610
Marín JC, Casey CS, Kadwell M, Yaya K, Hoces D, Olazabal J et al (2007) Mitochondrial phylogeography and demographic history of the Vicuña: implications for conservation. Heredity 99:70–80. https://doi.org/10.1038/sj.hdy.6800966
Marín JC, González BA, Poulin E, Casey CS, Johnson WE (2013) The influence of the arid Andean high plateau on the phylogeography and population genetics of guanaco (Lama guanicoe) in South America. Mol Ecol 22:463–482. https://doi.org/10.1111/mec.12111
Martinez PA, Pia MV, Bahechar IA, Molina WF, Bidau CJ, Montoya-Burgos JI (2018) The contribution of neutral evolution and adaptive processes in driving phenotypic divergence in a model mammalian species, the Andean fox Lycalopex culpaeus. J Biogeogr 45:1114–1125. https://doi.org/10.1111/jbi.13189
Matschiner M, Salzburger W (2009) TANDEM: integrating automated allele binning into genetics and genomics workflows. Bioinformatics 25:1982–1983. https://doi.org/10.1093/bioinformatics/btp303
Medel RG, Jaksic F (1988) Ecología de los cánidos sudamericanos: Una revisión. Rev Chil De Hist Nat 61:67–79
Medel RG, Jiménez JE, Jaksić FM, Yáñez J, Armesto JJ (1990) Discovery of a continental population of the rare Darwin’s fox, Dusicyon fulvipes (Martin, 1837) in Chile. Biol Conserv 51:71–77. https://doi.org/10.1016/0006−3207(90)90033−L
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In: 2010 Gateway Computing Environments Workshop (GCE). IEEE, New Orleans, pp 1–8. https://doi.org/10.1109/GCE.2010.5676129
Moritz C (1999) Conservation units and translocations: strategies for conserving evolutionary processes. Hereditas 130:217–228. https://doi.org/10.1111/j.1601−5223.1999.00217.x
Nester PL, Gayó E, Latorre C, Jordan TE, Blanco N (2007) Perennial stream discharge in the hyperarid Atacama Desert of northern Chile during the latest Pleistocene. PNAS 104:19724–19729. https://doi.org/10.1073/pnas.0705373104
Novaro AJ, Funes MC, Jiménez JE (2004) Patagonian foxes. Selection for introduced prey and conservation of culpeo and chilla foxes in Patagonia. In: Macdonald DW, Sillero-Zubiri C (eds) The biology and conservation of wild Canids. Oxford University Press, New York, pp 243–254. https://doi.org/10.1093/acprof:oso/9780198515562.001.0001
Novaro, A. J. (1997) Pseudalopex culpaeus. Mamm Species. pp 1–8. https://doi.org/10.2307/3504483
Núñez MB, Bozzolo L (2006) Diet analysis of gray fox, Pseudalopex griseus (Canidae) (Gray, 1869), in Sierra de las Quijadas National Park, San Luis, Argentina. Gayana 70:163–167. https://doi.org/10.4067/S0717−65382006000200002
O’Brien SJ, Mayr E (1991) Bureaucratic mischief: recognizing endangered species and subspecies. Science 251:1187–1188. https://doi.org/10.1126/SCIENCE.251.4998.1187
Osgood WH (1943) Order Carnivora. In: The mammals of Chile. Field Museum of Natural History, Zoological Series 30:1-268. pp 63–105. Available at: https://www.biodiversitylibrary.org/bibliography/3842
Pacheco V, Cadenillas R, Salas E, Tello C, Zeballos H (2009) Diversidad y endemismo de los mamíferos del Perú. Rev Peru Biol 16:5–32
Palma RE, Marquet PA, Boric-Bargetto D (2005) Inter− and intraspecific phylogeography of small mammals in the Atacama Desert and adjacent areas of northern Chile. J Biogeogr 32:1931–1941. https://doi.org/10.1111/j.1365−2699.2005.01349.x
Palma RE, Boric-Bargetto D, Jayat JP, Flores DA, Zeballos H, Pacheco V, Cancino RA, Alfaro FD, Rodríguez-Serrano E, Pardiñas UFJ (2014) Molecular phylogenetics of mouse opossums: new findings on the phylogeny of Thylamys (Didelphimorphia, Didelphidae). Zool Scr 43:217–234. https://doi.org/10.1111/zsc.12051
Park SDE (2002) Trypanotolerace in West African cattle and the population genetic effects of selection. Available at: http://www.tara.tcd.ie/handle/2262/89035. Accessed 10 April 2021
Perini FA, Russo CAM, Schrago CG (2010) The evolution of South American endemic canids: a history of rapid diversification and morphological parallelism. J Evol Biol 23:311–322. https://doi.org/10.1111/j.1420−9101.2009.01901.x
Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first−generation migrant detection. J Hered 95:536–539. https://doi.org/10.1093/jhered/esh074
Placzek C, Quade J, Betancourt JL, Patchett PJ, Rech JA, Latorre C et al (2009) Climate in the dry central andes over geologic, millennial, and interannual timescales. Ann Mo Bot Gard 96:386–397. https://doi.org/10.3417/2008019
Porras-Hurtado L, Ruiz Y, Santos C, Phillips C, Carracedo Á, Lareu MV (2013) An overview of STRUCTURE: applications, parameter settings, and supporting software. Front Genet 4:1–13. https://doi.org/10.3389/fgene.2013.00098
Prevosti FJ (2010) Phylogeny of the large extinct South American Canids (Mammalia, Carnivora, Canidae) using a “total evidence” approach. Cladistics 26:456–481. https://doi.org/10.1111/j.1096−0031.2009.00298.x
Prevosti FJ, Forasiepi AM (2018) South American Fossil Carnivorans (Order Carnivora). In: Prevosti FJ, Forasiepi AM (eds) Evolution of South American mammalian predators during the Cenozoic: paleobiogeographic and paleoenvironmental contingencies. Springer International Publishing, Cham, pp 85–136
Prevosti FJ, Segura V, Cassini G, Martin GM (2013) Revision of the systematic status of Patagonian and Pampean Gray foxes (Canidae: Lycalopex griseus and L. gymnocercus) using 3D geometric morphometrics. Mastozool Neotrop 20:289–300
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. https://doi.org/10.1093/genetics/155.2.945
R Core Team (2021) R: A language and environment for statistical computing. In: R Foundation for Statistical Computing. Vienna, Austria. Available at: https://www.R-project.org/
Rambaut A (2009) FigTree v1. 3.1. Tree figure drawing tool. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh. http://tree.bio.ed.ac.uk/software/figtree/
Rivera DS, Vianna JA, Ebensperger LA, Palma RE (2016) Phylogeography and demographic history of the Andean degu, Octodontomys gliroides (Rodentia: Octodontidae). Zool J Linn Soc 178:410–430. https://doi.org/10.1111/zoj.12412
Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138. https://doi.org/10.1046/j.1471−8286.2003.00566.x
Rosenzweig ML (1966) Community structure in sympatric Carnivora. J Mammal 47:602–612. https://doi.org/10.2307/1377891
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE et al (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248
Rubio AV, Alvarado R, Bonacic C (2013) Introduced European rabbit as main prey of the native carnivore culpeo fox (Lycalopex culpaeus) in disturbed ecosystems of central Chile. Stud Neotrop Fauna Environ 48:89–94. https://doi.org/10.1080/01650521.2013.831521
Ruiz-Garcia M, Rivas-Sánchez D, Lichilín-Ortiz N (2013) Phylogenetics relationships among four putative taxa of foxes of the Pseudoalopex Genus. In: Ruiz-Garcia M, Shostell JM (eds) Molecular population genetics, evolutionary biology, and biological conservation of neotropical carnivores. Nova Science Publishers Inc, New York, pp 97–128
Schwartz MK, Pilgrim KL, McKelvey KS, Lindquist EL, Claar JJ, Loch S et al (2004) Hybridization between Canada lynx and bobcats: genetic results and management implications. Conserv Genet 5:349–355. https://doi.org/10.1023/B:COGE.0000031141.47148.8b
Sikes RS, Gannon WL, the Animal Care and Use Committee of the American Society of Mammalogists (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92:235–253. https://doi.org/10.1644/10−MAMM−F−355.1
Silva-Rodríguez EA, Soto-Gamboa M, Ortega-Solís GR, Jiménez JE (2009) Foxes, people and hens: human dimensions of a conflict in a rural area of southern Chile. Rev Chil Hist Nat 82:375–386. https://doi.org/10.4067/S0716−078X2009000300005
Stamatakis A (2006) RAxML−VI−HPC: maximum likelihood−based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. https://doi.org/10.1093/bioinformatics/btl446
Tchaicka L, Eizirik E, Oliveira TGD, Cândido JF, Freitas TRO (2007) Phylogeography and population history of the crab−eating fox (Cerdocyon thous). Mol Ecol 16:819–838. https://doi.org/10.1111/j.1365−294X.2006.03185.x
Tchaicka L, de Freitas TRO, Bager A, Vidal SL, Lucherini M, Iriarte A et al (2016) Molecular assessment of the phylogeny and biogeography of a recently diversified endemic group of South American canids (Mammalia: Carnivora: Canidae). Genet Mol Biol 39:442–451. https://doi.org/10.1590/1678−4685−GMB−2015−0189
Thomas O (1914a) LXVI.—Three new S.−American mammals. Ann Mag Nat Hist 13:573–575. https://doi.org/10.1080/00222931408693526
Thomas O (1914b) XLI.—On various South−American mammals. Ann Mag Nat Hist 13:345–363. https://doi.org/10.1080/00222931408693492
Trigo TC, Freitas TRO, Kunzler G, Cardoso L, Silva JCR, Johnson WE et al (2008) Inter−species hybridization among Neotropical cats of the genus Leopardus, and evidence for an introgressive hybrid zone between L. geoffroyi and L. tigrinus in southern Brazil. Mol Ecol 17:4317–4333. https://doi.org/10.1111/j.1365−294X.2008.03919.x
Venta PJ, Brouillette JA, Yuzbasiyan-Gurkan V, Brewer GJ (1996) Gene−specific universal mammalian sequence−tagged sites: application to the canine genome. Biochem Genet 34:321–341. https://doi.org/10.1007/BF02399951
Vianna JA, Noll D, Dantas GPM, Petry MV, Barbosa A, González-Acuña D et al (2017) Marked phylogeographic structure of Gentoo penguin reveals an ongoing diversification process along the Southern Ocean. Mol Phylogenet Evol 107:486–498. https://doi.org/10.1016/j.ympev.2016.12.003
Vilà C, Leonard JA, Iriarte A, O’Brien SJ, Johnson WE, Wayne RK (2004) Detecting the vanishing populations of the highly endangered Darwin’s fox, Pseudalopex fulvipes. Anim Conserv 7:147–153. https://doi.org/10.1017/S1367943004001271
Vivar E, Pacheco V (2014) Status of gray fox Lycalopex griseus (Gray, 1837) (Mammalia: Canidae) from Peru. Rev Peru Biol 21:071–078. https://doi.org/10.15381/rpb.v21i1.8249
Wayne RK, Van Valkenburgh B, Kat PW, Fuller TK, Johnson WE, O’Brien SJ (1989) Genetic and morphological divergence among sympatric canids. J Hered 80:447–454. https://doi.org/10.1093/oxfordjournals.jhered.a110896
Wozencraft WC (2005) Order carnivora. In: Wilson DW, Reeder DM (eds) Mammal species of the world: a taxonomic and geographic reference. The Johns Hopkins University Press, Baltimore, pp 532–628
Yahnke CJ (1995) Metachromism and the insight of Wilfred Osgood: evidence of common ancestory for Darwin’s fox and the Sechura fox. Rev Chil De Hist Nat 68:459–461
Yahnke CJ, Johnson WE, Geffen E, Smith D, Hertel F, Roy MS et al (1996) Darwin’s fox: a distinct endangered species in a vanishing habitat. Conserv Biol 10:366–375. https://doi.org/10.1046/j.1523−1739.1996.10020366.x
Zapata SC, Travaini A, Delibes M, Martínez-Peck R (2005) Food habits and resource partitioning between grey and culpeo foxes in southeastern Argentine Patagonia. Stud Neotrop Fauna Environ 40(97):103. https://doi.org/10.1080/01650520500129836
Zapata SC, Procopio DE, Martínez-Peck R, Zanón JI, Travaini A (2008) Morfometría externa y reparto de recursos en zorros simpátricos (Pseudalopex culpaeus y P. griseus) en el sureste de la Patagonia Argentina. Mastozool Neotrop 15(103):111
Zapata SC, Delibes M, Travaini A, Procopio D (2014) Co−occurrence patterns in carnivorans: correspondence between morphological and ecological characteristics of an assemblage of Carnivorans in Patagonia. J Mamm Evol 21:417–426. https://doi.org/10.1007/s10914−013−9237−2
Zúñiga A, Muñoz-Pedreros A, Fierro A (2008) Diet of Lycalopex griseus (Gray, 1837) (Mammalia: Canidae) in the intermediate depression of Southern Chile. Gayana (Concepc) 72(113):116. https://doi.org/10.4067/S0717−65382008000100013
Zunino G, Vaccaro O, Caevari M, Gardner A (1995) Taxonomy of the genus Lycalopex (Carnivora: Canidae) in Argentina. Proc Biol Soc Wash 108:729–747
Zurano JP, Martinez PA, Canto-Hernandez J, Montoya-Burgos JI, Costa GC (2017) Morphological and ecological divergence in South American canids. J Biogeogr 44:821–833. https://doi.org/10.1111/jbi.12984
Zurita C, Soto N, Jaksic FM (2023) Historical ecology and current abundance of the translocated Chilla or Grey fox Lycalopex griseus on the large Tierra del Fuego Island shared by Argentina and Chile. Austral Ecol 48:481–497. https://doi.org/10.1111/aec.13285
Acknowledgements
We would like to dedicate this study to one of the co−authors, Daniel González−Acuña, a great scientist and conservationist that passed away last December 2020. Credits for the fox illustrations and the figures to Toni Llobet in Wilson, D.E. and Mittermeier, R.A. eds. (2009). Handbook of the Mammals of the World. Vol. 1. Carnivores. Lynx Edicions, Barcelona.
Funding
This work has been supported by the Millennium Institute Center for Genome Regulation–CRG (ANID-MILENIO-ICN2021_044), the Millennium Institute Biodiversity of Antarctic and Subantarctic Ecosystems ICN2021_002 (BASE), NCN2021-050 (LiLi), DID-UBB (grant N°2020416 IF/R), and Fondo Nacional de Desarrollo Científico y Tecnologico (Fondecyt 1181677 and 1161593). During the collection of samples in Santa Cruz (Argentina), A.R. and A.T. were supported by the Spanish Ministry of Science and Innovation (grant CGL2011-27469) and the European Regional Development Fund.
Author information
Authors and Affiliations
Contributions
E.J.P., B.J-K., J.C.M., and J.A.V. obtained the samples from foxes, undertook molecular laboratory and analyses, interpreted the results, wrote the manuscript and prepared the figures. V. M. undertook molecular laboratory. J.A.V. and J.C.M. secured funding support. J.C., G.A.J., N.S-P., D.G-A., C.B., A.I., A.R., A.T., A.C., J.L.B., J.M., and J.C.M. collected and provided samples for the study. All authors reviewed the full manuscript.
Corresponding author
Ethics declarations
Ethics approval
Capture and sampling methods was carried out in strict accordance with the guidelines of the American Society of Mammalogists. The research protocols were approved by all the institutions involved in sample collection in accordance with local regulations from Chile and Argentina as well as and the ARRIVE (Animal Research: Reporting of In Vivo Experiments) guidelines.
Competing interests
The authors declare no competing interests.
Additional information
Communicated by Rafał Kowalczyk
This work is dedicated to Daniel González-Acuña who passed away during the preparation of this study.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Pizarro, E.J., Julio-Kalajžić, B., Sallaberry-Pincheira, N. et al. Species delimitation and intraspecific diversification in recently diverged South American foxes. Mamm Res 69, 71–87 (2024). https://doi.org/10.1007/s13364-023-00717-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13364-023-00717-y