Abstract
South American Canids are endemic and form a monophyletic clade supported by molecular and morphological data, with the exception of Urocyon cinereoargenteus, which is a typical North American form. South American canids occur in almost all environments in continent, and exhibit diet diversity and large size variation. Here we analyzed the skull ontogeny by applying 3D geometric morphometric techniques, in a well-represented sample of South American canids, with the aim of exploring variation in cranial size and shape as well as evolutionary patterns of such variation. The sample consisted of 1227 crania of the 11 living species of South American canids and 92 crania of Canis lupus and Vulpes vulpes, which were considered as out-groups. South American canids exhibited similar shape and diet (they are mostly omnivorous), which implies similar mechanical commitments, which are reflected in their almost uniform skulls. However, it is possible that cranial similarity is related to a shared evolutionary history with a short time of divergence. Speothos venaticus differed in its ontogenetic trajectory, with the difference being stronger between adults of this species and the remaining canids. The skull configuration is consistent with the hyper-carnivorous diet. In the case of Chrysocyon brachyurus, size plays an important role in the structure of a skull, giving rise to remarkable morphological differences from other species, although in terminal stages of its ontogeny.
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Data supporting this manuscript is available on digital repository of Universidad Nacional de La Plata http://sedici.unlp.edu.ar/handle/10915/41
References
Antón, M., Salesa, M. J., Pastor, J. F., Sánchez, I. M., Fraile, S., & Morales, J. (2004). Implications of the mastoid anatomy of larger extant felids for the evolution and predatory behaviour of sabretoothed cats (Mammalia, Carnivora, Felidae). Zoological Journal of the Linnean Society, 140, 207–221. https://doi.org/10.1111/j.1096-3642.2003.00093.x.
Aragona, M., & Setz, E. Z. F. (2001). Diet of the maned wolf, Chrysocyon brachyurus (Mammalia: Canidae), during wet and dry seasons at Ibitipoca State Park, Brazil. Journal of Zoology, 254, 131–136. https://doi.org/10.1017/S0952836901000620.
Austin, J. J., Soubrier, J., Prevosti, F. J., Prates, L., Trejo, V., Mena, F., & Cooper, A. (2013). The origins of the enigmatic Falkland Islands wolf. Nature Communications, 4, 1552. https://doi.org/10.1038/ncomms2570.
Beisiegel, B. M., & Zuercher, G. L. (2005). Speothos venaticus. Mammalian Species, 783, 1–6. https://doi.org/10.1644/783.1.
Bekoff, M., & Jamieson, R. (1975). Physical development in coyotes (Canis latrans), with a comparison to other canids. Journal of Mammalogy, 56, 685–692. https://doi.org/10.2307/1379485.
Berta, A. (1987). Origin, diversification, and zoogeography of the South American Canidae. Fieldiana Zoology, 39, 455–471.
Biben, M. (1982). Ontogeny of social behaviour related to feeding in the crab-eating fox (Cerdocyon thous) and the bush dog (Speothos venaticus). Journal of Zoology, 196, 207–216. https://doi.org/10.1111/j.1469-7998.1982.tb03501.x.
Biben, M. (1983). Comparative ontogeny of social behaviour in three South American canids, the maned wolf, crab-eating fox and bush dog: Implications for sociality. Animal Behaviour, 31, 814–826. https://doi.org/10.1016/S0003-3472(83)80238-3.
Biknevicius, A. R., & Leigh, S. R. (1997). Patterns of growth of the mandibular corpus in spotted hyenas (Crocuta crocuta) and cougars (Puma concolor). Zoological Journal of the Linnean Society, 120, 139–161. https://doi.org/10.1111/j.1096-3642.1997.tb01276.x.
Biknevicius, A. R., & Van Valkenburgh, B. (1996). Design for killing: Craniodental adaptations of predators. In J. L. Gittleman (Ed.), Carnivore behavior, ecology, and evolution (pp. 393–428). New York: Cornell University Press.
Bingham, J., & Purchase, G. K. (2003). Age determination in jackals (Canis adustus Sundevall, 1846, and Canis mesomelas Schreber, 1778; Carnivora: Canidae) with reference to the age structure and breeding patterns of jackal populations in Zimbabwe. African Zoology, 38, 153–160. https://doi.org/10.1080/15627020.2003.11657203.
Black, K. H., Archer, M., Hand, S. J., & Godthelp, H. (2010). First comprehensive analysis of cranial ontogeny in a fossil marsupial—From a 15-million-year-old cave deposit in northern Australia. Journal of Vertebrate Paleontology, 30, 993–1011. https://doi.org/10.1080/02724634.2010.483567.
Blomberg, S. P., Garland, T., & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution, 57, 717–745. https://doi.org/10.1111/j.0014-3820.2003.tb00285.x.
Bookstein, F. L. (1991). Morphometric tools for landmark data: Geometry and biology. Cambridge: Cambridge University Press.
Brady, C. A. (1978). Reproduction, growth and parental care in crab-eating foxes (Cerdocyon thous) at the National Zoological Park, Washington. International Zoo Yearbook, 18, 130–134. https://doi.org/10.1111/j.1748-1090.1978.tb00243.x.
Brady, C. A., & Ditton, M. K. (1979). Management and breeding of maned wolves. International Zoo Yearbook, 19, 171–176. https://doi.org/10.1111/j.1748-1090.1979.tb00557.x.
Bubadué, J., Cáceres, N., dos Santos Carvalho, R., & Meloro, C. (2016a). Ecogeographical variation in skull shape of South-American Canids: Abiotic or biotic processes? Evolutionary Biology, 43, 145–159. https://doi.org/10.1007/s11692-015-9362-3.
Bubadué, J., Cáceres, N., Carvalho, R., Sponchiado, J., Passaro, F., Saggese, F., Mondanaro, A., Raia, P., & Carotenuto, F. (2016b). Character displacement under influence of Bergmann’s rule in Cerdocyon thous (Mammalia: Canidae). Hystrix, 27, 83–90. https://doi.org/10.4404/hystrix-27.2-11433.
Byron, C. D. (2006). Role of the osteoclast in cranial suture waveform patterning. Anatomical Record, 288A, 552–563. https://doi.org/10.1002/ar.a.20322.
Cardini, A., & Polly, P. D. (2013). Larger mammals have longer faces because of size-related constraints on skull form. Nature Communications, 4, 2458. https://doi.org/10.1038/ncomms3458.
Cassini, G. H., & Vizcaíno, S. F. (2012). An approach to the biomechanics of the masticatory apparatus of early Miocene (Santacrucian age) south American ungulates (Astrapotheria, Litopterna, and Notoungulata): Moment arm estimation based on 3D landmarks. Journal of Mammalian Evolution, 19, 9–25. https://doi.org/10.1007/s10914-011-9179-5.
Cassini, G. H., Flores, D. A., & Vizcaíno, S. F. (2015). Postnatal ontogenetic scaling of pampas deer (Ozotoceros bezoarticus celer: Cervidae) cranial morphology. Mammalia, 79(1), 69–79. https://doi.org/10.1515/mammalia-2013-0051.
Catalano, S. A., & Goloboff, P. A. (2012). Simultaneously mapping and superimposing landmark configurations with parsimony as optimality criterion. Systematic Biology, 61, 392. https://doi.org/10.1093/sysbio/syr119.
Catalano, S. A., Goloboff, P. A., & Giannini, N. P. (2010). Phylogenetic morphometrics (I): The use of landmark data in a phylogenetic framework. Cladistics, 26, 539–549. https://doi.org/10.1111/j.1096-0031.2010.00302.x.
Christiansen, P., & Adolfssen, J. S. (2005). Bite forces, canine strength and skull allometry in carnivores (Mammalia, Carnivora). Journal of Zoology, 266, 133–151. https://doi.org/10.1017/S0952836905006643.
Courtenay, O., & Maffei, L. (2004). Crab-eating fox Cerdocyon thous. In C. Sillero-Zubiri, M. Hoffmann, & D. W. Macdonald (Eds.), Canids: Foxes, wolves, jackals and dogs. Status survey and conservation action plan (pp. 32–38). IUCN Species Programme: Gland.
Cox, P. G. (2007). A quantitative analysis of the eutherian orbit: Correlations with masticatory apparatus. Biological Reviews, 83(1), 35–69. https://doi.org/10.1111/j.1469-185X.2007.00031.x.
Crespo, J. A. (1971). Ecología del zorro gris Dusicyon gymnocercus antiquus (Ameghino) en la provincia de La Pampa. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, 5, 1–205.
Crespo, J. A., & De Carlo, J. M. (1963). Estudio ecológico de una población de zorros colorados Dusicyon culpaeus. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, 1, 1–55.
Dalponte, J. C. (2009). Lycalopex vetulus (Carnivora: Canidae). Mammalian Species, 847, 1–7. https://doi.org/10.1644/847.1.
Dalponte, J., & Courtenay, O. (2004). Hoary fox Pseudalopex vetulus. In C. Sillero-Zubiri, M. Hoffmann, & D. W. Macdonald (Eds.), Canids: Foxes, wolves, jackals and dogs. Status survey and conservation action plan (pp. 72–76). IUCN Species Programme: Gland.
Damasceno, E. M., Hingst-Zaher, E., & Astúa, D. (2013). Bite force and encephalization in the Canidae (Mammalia: Carnivora). Journal of Zoology, 290, 246–254. https://doi.org/10.1111/jzo.12030.
Drake, A. G. (2011). Dispelling dog dogma: An investigation of heterochrony in dogs using 3D geometric morphometric analysis of skull shape: Investigation of heterochrony in dogs. Evolution & Development, 13, 204–213. https://doi.org/10.1111/j.1525-142X.2011.00470.x.
Dryden, I. L., & Mardia, K. V. (1998). Statistical shape analysis. Chichester: Wiley.
Duckler, G. L. (1998). An unusual osteological formation in the posterior skulls of captive tigers (Panthera tigris). Zoo Biology, 17, 135–142. https://doi.org/10.1002/(SICI)1098-2361(1998)17:2<135::AID-ZOO8>3.0.CO;2-A.
Eizirik, E. (2012). A molecular view on the evolutionary history and biogeography of Neotropical carnivores (Mammalia, Carnivora). In B. D. Patterson & L. P. Costa (Eds.), Bones, clones, and biomes: The history and geography of recent Neotropical mammals (pp. 123–142). Chicago: The University of Chicago Press.
Emerson, S. B., & Bramble, D. M. (1993). Scaling, allometry and skull design. In J. Hanken & B. K. Hall (Eds.), The skull (pp. 384–416). Chicago: The University of Chicago Press.
Evans, H. E. (1993). Miller’s anatomy of the dog (3rd ed.). Philadelphia: W. B. Saunders Company.
Ewer, R. F. (1973). The carnivores. Ithaca: Cornell University Press.
Figueirido, B., MacLeod, N., Krieger, J., De Renzi, M., Pérez-Claros, J. A., & Palmqvist, P. (2011). Constraint and adaptation in the evolution of carnivoran skull shape. Paleobiology, 37, 490–518. https://doi.org/10.1666/09062.1.
Flores, D. A., Giannini, N., & Abdala, F. (2018). Evolution of post-weaning skull ontogeny in New World opossums (Didelphidae). Organisms Diversity & Evolution, 18, 367–382. https://doi.org/10.1007/s13127-018-0369-3.
Forbes-Harper, J. L., Crawford, H. M., Dundas, S. J., Warburton, N. M., Adams, P. J., Bateman, P. W., et al. (2017). Diet and bite force in red foxes: Ontogenetic and sex differences in an invasive carnivore. Journal of Zoology, 303, 54–63. https://doi.org/10.1111/jzo.12463.
Fuentes-González, J. A., & Muñoz-Durán, J. (2017). Comportamiento social y preferencias alimentarias en la evolución de los cánidos actuales. Revista Mexicana de Biodiversidad, 88, 192–206. https://doi.org/10.1016/j.rmb.2017.01.022.
Fuller, T. K., & Cypher, B. L. (2004). Gray fox Urocyon cinereoargenteus. In C. Sillero-Zubiri, M. Hoffmann, & D. W. Macdonald (Eds.), Canids: Foxes, wolves, jackals and dogs. Status survey and conservation action plan (pp. 92–97). IUCN Species Programme: Gland.
Galatius, A., Berta, A., Frandsen, M. S., & Goodall, R. N. P. (2011). Interspecific variation of ontogeny and skull shape among porpoises (Phocoenidae). Journal of Morphology, 272, 136–148. https://doi.org/10.1002/jmor.10900.
García-Perea, R. (1996). Patterns of postnatal development in skull of lynxes, Genus Lynx (Mammalia: Carnivora). Journal of Morphology, 229, 241–254. https://doi.org/10.1002/(SICI)1097-4687(199609)229:3<241::AID-JMOR1>3.0.CO;2-1.
German, R. Z., & Crompton, A. W. (1996). Ontogeny of suckling mechanisms in opossums (Didelphis virginiana). Brain, Behavior and Evolution, 48, 157–164. https://doi.org/10.1159/000113194.
German, R. Z., Crompton, A. W., Levitch, L. C., & Thexton, A. J. (1992). The mechanism of suckling in two species of infant mammal: Miniature pigs and long-tailed macaques. Journal of Experimental Zoology, 261, 322–330. https://doi.org/10.1002/jez.1402610311.
Giannini, N. P., Segura, V., Giannini, M. I., & Flores, D. (2010). A quantitative approach to the cranial ontogeny of the puma. Mammalian Biology, 75, 547–554. https://doi.org/10.1016/j.mambio.2009.08.001.
Gipson, P. S., Ballard, W. B., Nowak, R. M., & Mech, L. D. (2000). Accuracy and precision of estimating age of gray wolves by tooth wear. Journal of Wildlife Management, 64, 752–758 http://digitalcommons.unl.edu/usgsnpwrc/400.
Gittleman, J. L. (1985). Carnivore body size: Ecological and taxonomic correlates. Oecologia, 67, 540–554. https://doi.org/10.1007/BF00790026.
Goloboff, P. A., & Catalano, S. A. (2016). TNT version 1.5, including a full implementation of phylogenetic morphometrics. Cladistics, 32, 221–238. https://doi.org/10.1111/cla.12160.
Goloboff, P. A., Mattoni, C. I., & Quinteros, A. S. (2006). Continuous characters analyzed as such. Cladistics, 22, 589–601. https://doi.org/10.1111/j.1096-0031.2006.00122.x.
González del Solar, R., & Rau, J. (2004). Chilla Pseudalopex griseus. In C. Sillero-Zubiri, M. Hoffmann, & D. W. Macdonald (Eds.), Canids: Foxes, wolves, jackals and dogs. Status survey and conservation action plan (pp. 56–63). IUCN Species Programme: Gland.
Goodall, C. (1991). Procrustes methods in the statistical analysis of shape. Journal of the Royal Statistical Society: Series B (Methodological), 53, 285–321. https://doi.org/10.1111/j.2517-6161.1991.tb01825.x.
Goodwin, E. A., & Ballard, W. B. (1985). Use of tooth cementum for age determination of gray wolves. The Journal of Wildlife Management, 49, 313. https://doi.org/10.2307/3801522.
Goswami, A. (2006). Morphological integration in the carnivoran skull. Evolution, 60, 169–183. https://doi.org/10.1111/j.0014-3820.2006.tb01091.x.
Goswami, A., Milne, N., & Wroe, S. (2010). Biting through constraints: cranial morphology, disparity and convergence across living and fossil carnivorous mammals. Proceedings of the Royal Society B: Biological Sciences, 278, 1831–1839. https://doi.org/10.1098/rspb.2010.2031.
Grue, H., & Jensen, B. (1973). Annular structures in canine tooth cementum in red foxes. Vulpes vulpes. Danish Review of Game Biology, 8, 1–16.
Guzmán, J. A., & Ortiz, J. C. (2009). Variación geográfica del zorro Lycalopex culpaeus (Mammalia, Canidae) en Chile: implicaciones taxonómicas. Revista de Biología Tropical, 57, 421–432.
Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4, 1–9 http://palaeo-electronica.org/2001_1/past/past.pdf.
Harris, S. (1978). Age determination in the red fox (Vulpes vulpes)-an evaluation of technique efficiency as applied to a sample of suburban foxes. Journal of Zoology, 184, 91–117. https://doi.org/10.1111/j.1469-7998.1978.tb03268.x.
Helm, J. W., & German, R. Z. (1996). The epigenetic impact of weaning on craniofacial morphology during growth. The Journal of Experimental Zoology, 276, 243–253. https://doi.org/10.1002/(SICI)1097-010X(19961101)276:4<243::AID-JEZ1>3.0.CO;2-O.
Hildebrand, M. (1995). Analysis of vertebrate structure. Hoboken: Wiley.
Holliday, J. A., & Steppan, S. J. (2004). Evolution of hypercarnivory: The effect of specialization on morphological and taxonomic diversity. Paleobiology, 30, 108–128. https://doi.org/10.1666/0094-8373(2004)030<0108:EOHTEO>2.0.CO;2.
Jantschke, F. (1973). On the breeding and rearing of bush dogs Speothos venaticus at Frankfurt Zoo. International Zoo Yearbook, 13, 141–143. https://doi.org/10.1111/j.1748-1090.1973.tb02130.x.
Jiménez, J. E., & McMahon, E. (2004). Darwin’s fox Pseudalopex fulvipes. In C. Sillero-Zubiri, M. Hoffmann, & D. W. Macdonald (Eds.), Canids: Foxes, wolves, jackals and dogs. Status survey and conservation action plan (pp. 50–55). IUCN Species Programme: Gland.
Jiménez, J. E., & Novaro, A. J. (2004). Culpeo Pseudalopex culpaeus. In C. Sillero-Zubiri, M. Hoffmann, & D. W. Macdonald (Eds.), Canids: Foxes, wolves, jackals and dogs. Status survey and conservation action plan (pp. 44–49). IUCN Species Programme: Gland.
Juarez, K. M., & Marinho-Filho, J. (2002). Diet, habitat use, and home ranges of sympatric canids in Central Brazil. Journal of Mammalogy, 83, 925–933. https://doi.org/10.1644/1545-1542(2002)083<0925:DHUAHR>2.0.CO;2.
Klingenberg, C. P. (1998). Heterochrony and allometry: The analysis of evolutionary change in ontogeny. Biological Reviews, 73, 79–123. https://doi.org/10.1017/S000632319800512X.
Klingenberg, C. P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11, 353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x.
Knowlton, F. F., & Whittemore, S. L. (2001). Pulp cavity-tooth width ratios from known-age and wild-caught coyotes determined by radiography. Wildlife Society Bulletin, 239, 244 www.jstor.org/stable/3784003.
Kremenak, C. R. (1969). Dental eruption chronology in dogs: Deciduous tooth gingival emergence. Journal of Dental Research, 48, 1177–1184. https://doi.org/10.1177/00220345690480061501.
Kremenak, C. R., Russell, L. S., & Christensen, R. D. (1969). Tooth-eruption ages in suckling dogs as affected by local heating. Journal of Dental Research, 48, 427–430. https://doi.org/10.1177/00220345690480061501.
La Croix, S., Holekamp, K. E., Shivik, J. A., Lundrigan, B. L., & Zelditch, M. L. (2011a). Ontogenetic relationships between cranium and mandible in coyotes and hyenas. Journal of Morphology, 272, 662–674. https://doi.org/10.1002/jmor.10934.
La Croix, S., Zelditch, M. L., Shivik, J. A., Lundrigan, B. L., & Holekamp, K. E. (2011b). Ontogeny of feeding performance and biomechanics in coyotes. Journal of Zoology, 285, 301–315. https://doi.org/10.1111/j.1469-7998.2011.00847.x.
Landon, D. B., Waite, C. A., Peterson, R. O., & Mech, L. D. (1998). Evaluation of age determination techniques for gray wolves. The Journal of Wildlife Management, 62, 674. https://doi.org/10.2307/3802343.
Leite Pitman, M. R. P., & Williams, R. S. R. (2004). Short-eared dog Atelocynus microtis. In C. Sillero-Zubiri, M. Hoffmann, & D. W. Macdonald (Eds.), Canids: Foxes, wolves, jackals and dogs. Status survey and conservation action plan (pp. 26–31). IUCN Species Programme: Gland.
Linhart, S. B. (1968). Dentition and pelage in the juvenile red fox (Vulpes vulpes). Journal of Mammalogy, 49, 526. https://doi.org/10.2307/1378217.
Linhart, S. B., & Knowlton, F. F. (1967). Determining age of coyotes by tooth cementum layers. The Journal of Wildlife Management, 31, 362. https://doi.org/10.2307/3798334.
Lombaard, L. J. (1971). Age determination and growth curves in the black-backed jackal, Canis mesomelas Schreber, 1775 (Carnivora: Canidae). Annals of the Transvaal Museum, 27, 135–169.
Losos, J. B., & Miles, D. B. (2002). Testing the hypothesis that a clade has adaptively radiated: Iguanid lizard clades as a case study. The American Naturalist, 160, 147–157. https://doi.org/10.1086/341557.
Lucherini, M., Pessino, M., & Farias, A. A. (2004). Pampas fox Pseudalopex gymnocercus. In C. Sillero-Zubiri, M. Hoffmann, & D. W. Macdonald (Eds.), Canids: Foxes, wolves, jackals and dogs. Status survey and conservation action plan (pp. 63–68). IUCN Species Programme: Gland.
Machado, F. D. A., & Hingst-Zaher, E. (2009). Investigating south American biogeographic history using patterns of skull shape variation on Cerdocyon thous (Mammalia: Canidae). Biological Journal of the Linnean Society, 98, 77–84. https://doi.org/10.1111/j.1095-8312.2009.01274.x.
Machado, F. A., Zahn, T. M. G., & Marroig, G. (2018). Evolution of morphological integration in the skull of Carnivora (Mammalia): Changes in Canidae lead to increased evolutionary potential of facial traits. Evolution, 72, 1399–1419. https://doi.org/10.1111/evo.13495.
Martinez, P. A., Marti, D. A., Molina, W. F., & Bidau, C. J. (2013). Bergmann’s rule across the equator: A case study in Cerdocyon thous (Canidae). Journal of Animal Ecology, 82, 997–1008. https://doi.org/10.1111/1365-2656.12076.
McNamara, K. J. (2012). Heterochrony: The evolution of development. Evolution: Education and Outreach, 5, 203–218. https://doi.org/10.1007/s12052-012-0420-3.
Meloro, C., & O’Higgins, P. (2011). Ecological adaptations of mandibular form in fissiped Carnivora. Journal of Mammalian Evolution, 18, 185–200. https://doi.org/10.1007/s10914-011-9156-z.
Mitteroecker, P., Gunz, P., Bernhard, M., Schaefer, K., & Bookstein, F. L. (2004). Comparison of cranial ontogenetic trajectories among great apes and humans. Journal of Human Evolution, 46, 679–698. https://doi.org/10.1016/j.jhevol.2004.03.006.
Moore, W. J. (1981). The mammalian skull. Cambridge: Cambridge University Press.
Morales, M. M., & Giannini, N. P. (2010). Morphofunctional patterns in Neotropical felids: Species co-existence and historical assembly. Biological Journal of the Linnean Society, 100, 711–724. https://doi.org/10.1111/j.1095-8312.2010.01461.x.
Muñoz, N. A., Cassini, G. H., Candela, A. M., & Vizcaíno, S. F. (2017). Ulnar articular surface 3-D landmarks and ecomorphology of small mammals: A case study of two early Miocene typotheres (Notoungulata) from Patagonia. Earth and Environmental Science Transactions of the Royal Society of Edinburgh, 106, 315–323. https://doi.org/10.1017/S1755691016000141.
Nowak, R. M. (2005). Walker’s carnivores of the world. Baltimore: Johns Hopkins University Press.
Perez, S. I., Klaczko, J., Rocatti, G., & Dos Reis, S. F. (2011). Patterns of cranial shape diversification during the phylogenetic branching process of New World monkeys (Primates: Platyrrhini): Cranial shape diversification of Platyrrhini. Journal of Evolutionary Biology, 24, 1826–1835. https://doi.org/10.1111/j.1420-9101.2011.02309.x.
Perini, F. A., Russo, C. A. M., & Schrago, C. G. (2010). The evolution of south American endemic canids: A history of rapid diversification and morphological parallelism. Journal of Evolutionary Biology, 23, 311–322. https://doi.org/10.1111/j.1420-9101.2009.01901.x.
Prestrud, P., & Nilssen, K. (1995). Growth, size, and sexual dimorphism in Arctic foxes. Journal of Mammalogy, 76, 522–530. https://doi.org/10.2307/1382360.
Prevosti, F. J. (2006). Grandes cánidos (Carnivora, Canidae) del Cuaternario de la República Argentina: Sistemática, Filogenia, Bioestratigrafía y Paleoecología. Doctoral thesis, Universidad Nacional de La Plata, Facultad de Ciencias Naturales y Museo.
Prevosti, F. J. (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, F. J., & Forasiepi, A. M. (2018). Evolution of South American mammalian predators during the Cenozoic: Paleobiogeographic and paleoenvironmental contingencies. Cham: Springer Nature.
Prevosti, F. J., & Lamas, L. (2006). Variation of cranial and dental measurements and dental correlations in the pampean fox (Dusicyon gymnocercus). Journal of Zoology, 270, 636–649. https://doi.org/10.1111/j.1469-7998.2006.00187.x.
Prevosti, F. J., & Rincón, A. D. (2007). A new fossil canid assemblage from the late Pleistocene of Northern South America: The canids of the Inciarte asphalt pit (Zulia, Venezuela), fossil record and biogeography. Journal of Paleontology, 81, 1053–1065. https://doi.org/10.1666/pleo05-143.1.
Prevosti, F., & Soibelzon, L. H. (2012). Evolution of the south American carnivores (Mammalia, Carnivora): A paleontological perspective. In B. D. Patterson & L. P. Costa (Eds.), Bones, clones, and biomes: The history and geography of recent Neotropical mammals (pp. 102–122). Chicago: Oxford University Press.
Prevosti, F. J., Segura, V., Cassini, G. H., & Martin, G. M. (2013). Revision of the systematic status of Patagonian and Pampean gray foxes (Canidae: Lycalopex griseus and Lycalopex gymnocercus) using 3 D Geometric Morphometrics. Mastozoología Neotropical, 20, 289–300.
R Development Core Team (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available in: https://www.r-project.org/
Radinsky, L. B. (1981). Evolution of skull shape in carnivores: 1. Representative modern carnivores. Biological Journal of the Linnean Society, 15, 369–388. https://doi.org/10.1111/j.1095-8312.1981.tb00770.x.
Reilly, S. M., Wiley, E. O., & Meinhardt, D. J. (1997). An integrative approach to heterochrony: The distinction between interspecific and intraspecific phenomena. Biological Journal of the Linnean Society, 60, 119–143. https://doi.org/10.1111/j.1095-8312.1997.tb01487.x.
Rice, D. P. (2008). Craniofacial sutures development, disease and treatment (Frontiers of Oral Biology Vol. 12). Basel: Karger.
Richmond, F. J. R., Thomson, D. B., & Loeb, G. E. (1992). Electromyographic studies of neck muscles in the intact cat: I. Patterns of recruitment underlying posture and movement during natural behaviors. Experimental Brain Research, 88, 41–58. https://doi.org/10.1007/BF02259127.
Rodden, M., Rodrigues, F., & Bestelmeyer, S. (2004). Maned wolf Chrysocyon brachyurus. In C. Sillero-Zubiri, M. Hoffmann, & D. W. Macdonald (Eds.), Canids: Foxes, wolves, jackals and dogs. Status survey and conservation action plan (pp. 38–43). IUCN Species Programme: Gland.
Rohlf, F. J. (1999). Shape statistics: Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39, 40–59. https://doi.org/10.1007/s003579900054.
Root, D. A., & Payne, N. F. (1984). Evaluation of techniques for aging gray fox. The Journal of Wildlife Management, 48, 926–933. https://doi.org/10.2307/3801440.
Sánchez-Villagra, M. R., Segura, V., Geiger, M., Heck, L., Veitschegger, K., & Flores, D. (2017). On the lack of a universal pattern associated with mammalian domestication: Differences in skull growth trajectories across phylogeny. Royal Society Open Science, 4, 170876. https://doi.org/10.1098/rsos.170876.
Schlager, S. (2017). Morpho and Rvcg – Shape analysis in R: R-packages for geometric Morphometrics, shape analysis and surface manipulations. In G. Zheng, S. Li, & G. Székely (Eds.), Statistical shape and deformation analysis (pp. 217–256). Elsevier: Academic Press.
Segura, V. (2013). Skull ontogeny of Lycalopex culpaeus (Carnivora: Canidae): Description of cranial traits and craniofacial sutures. Mammalia, 77(2), 205–214. https://doi.org/10.1515/mammalia-2012-0028.
Segura, V. (2015). A three-dimensional skull ontogeny in the bobcat (Lynx rufus) (Carnivora: Felidae): A comparison with other carnivores. Canadian Journal of Zoology, 93, 225–237. https://doi.org/10.1139/cjz-2014-0148.
Segura, V., & Flores, D. (2009). Aproximación cualitativa y aspectos funcionales en la ontogenia craneana de Puma concolor (Felidae). Mastozoología Neotropical, 16, 169–182.
Segura, V., & Prevosti, F. (2012). A quantitative approach to the cranial ontogeny of Lycalopex culpaeus (Carnivora: Canidae). Zoomorphology, 131, 79–92. https://doi.org/10.1007/s00435-012-0145-4.
Segura, V., Prevosti, F., & Cassini, G. (2013). Cranial ontogeny in the Puma lineage, Puma concolor, Herpailurus yagouaroundi, and Acinonyx jubatus (Carnivora: Felidae): A three-dimensional geometric morphometric approach. Zoological Journal of the Linnean Society, 169, 235–250. https://doi.org/10.1111/zoj.12047.
Segura, V., Cassini, G. H., & Prevosti, F. J. (2017). Three-dimensional cranial ontogeny in pantherines (Panthera leo, P. onca, P. pardus, P. tigris, Carnivora: Felidae). Biological Journal of the Linnean Society, 120, 210–227. https://doi.org/10.1111/bij.12888.
Sicuro, F. L. (2011). Evolutionary trends on extant cat skull morphology (Carnivora: Felidae): A three-dimensional geometrical approach. Biological Journal of the Linnean Society, 103, 176–190. https://doi.org/10.1111/j.1095-8312.2011.01636.x.
Sicuro, F. L., & Oliveira, L. F. B. (2011). Skull morphology and functionality of extant Felidae (Mammalia: Carnivora): A phylogenetic and evolutionary perspective. Zoological Journal of the Linnean Society, 161, 414–462. https://doi.org/10.1111/j.1096-3642.2010.00636.x.
Sillero-Zubiri, C. (2009). Family Canidae. In D. E. Wilson & R. A. Mittermeier (Eds.), Handbook of the mammals of the world (pp. 352–447). Barcelona: Lynx Editions.
Slater, G. J., & Van Valkenburgh, B. (2009). Allometry and performance: The evolution of skull form and function in felids. Journal of Evolutionary Biology, 22, 2278–2287. https://doi.org/10.1111/j.1420-9101.2009.01845.x.
Slater, G. J., Dumont, E. R., & Van Valkenburgh, B. (2009). Implications of predatory specialization for cranial form and function in canids. Journal of Zoology, 278, 181–188. https://doi.org/10.1111/j.1469-7998.2009.00567.x.
Smith, K. K. (1997). Comparative patterns of craniofacial development in eutherian and metatherian mammals. Evolution, 51, 1663–1678. https://doi.org/10.1111/j.1558-5646.1997.tb01489.x.
Soibelzon, L. H., & Prevosti, F. J. (2007). Los carnívoros (Carnivora, Mammalia) terrestres del Cuaternario de América del Sur. In G. X. Pons & D. Vicens (Eds.), Geomorfología litoral i Quaternari. Homenatge a Joan Cuerda Barceló (pp. 49–68). Societat d’Història Natural de les Balears: Palmas de Mallorca.
Tanner, J. B., Zelditch, M. L., Lundrigan, B. L., & Holekamp, K. E. (2009). Ontogenetic change in skull morphology and mechanical advantage in the spotted hyena (Crocuta crocuta). Journal of Morphology, 271(3), 353–365. https://doi.org/10.1002/jmor.10802.
Tchaicka, L., Freitas, T. R. O., Bager, A., Vidal, S. L., Lucherini, M., Iriarte, A., & Eizirik, E. (2016). Molecular assessment of the phylogeny and biogeography of a recently diversified endemic group of South American canids (Mammalia: Carnivora: Canidae). Genetics and Molecular Biology, 39, 442–451. https://doi.org/10.1590/1678-4685-GMB-2015-0189.
Tedford, R. H., Taylor, B. E., & Wang, X. (1995). Phylogeny of the Caninae (Carnivora, Canidae): The living taxa. American Museum Novitates, 3146.
Thexton, A. J., Crompton, A. W., Owerkowicz, T., & German, R. Z. (2004). Correlation between intraoral pressures and tongue movements in the suckling pig. Archives of Oral Biology, 49, 567–575. https://doi.org/10.1016/j.archoralbio.2004.02.002.
Thomason, J. J. (1991). Cranial strength in relation to estimated biting forces in some mammals. Canadian Journal of Zoology, 69, 2326–2333. https://doi.org/10.1139/z91-327.
Travaini, A., Juste, J., Novaro, A. J., & Capurro, A. F. (2000). Sexual dimorphism and sex identification in the South American culpeo fox, Pseudalopex culpaeus (Carnivora : Canidae). Wildlife Research, 27, 669. https://doi.org/10.1071/WR99064.
Tseng, Z. J., & Flynn, J. J. (2018). Structure-function covariation with nonfeeding ecological variables influences evolution of feeding specialization in Carnivora. Science Advances, 4, eaao5441. https://doi.org/10.1126/sciadv.aao5441.
Van Valkenburgh, B. (1989). Carnivore dental adaptations and diet: A study of trophic diversity within guilds. In J. L. Gittleman (Ed.), Carnivore behavior, ecology, and evolution (pp. 410–436). Boston: Springer.
Van Valkenburgh, B. (1991). Iterative evolution of hypercarnivory in canids (Mammalia: Carnivora): Evolutionary interactions among sympatric predators. Paleobiology, 17, 340–362. https://doi.org/10.1017/S0094837300010691.
Van Valkenburgh, B. (2007). Deja vu: The evolution of feeding morphologies in the Carnivora. Integrative and Comparative Biology, 47, 147–163. https://doi.org/10.1093/icb/icm016.
Van Valkenburgh, B., & Koepfli, K. P. (1993). Cranial and dental adaptations to predation in canids. In N. Dunstone & M. L. Gorman (Eds.), Mammals as predators (pp. 15–37). London: Symposia of the Zoological Society of London, Oxford University Press.
Van Valkenburgh, B., Theodor, J., Friscia, A., Pollack, A., & Rowe, T. (2004). Respiratory turbinates of canids and felids: A quantitative comparison. Journal of Zoology, 264, 281–293. https://doi.org/10.1017/S0952836904005771.
Wainwright, P. C., & Reilly, S. M. (1994). Ecological morphology. Chicago: University of Chicago Press.
Wall, C. E., & Smith, K. K. (2001). Ingestion in Mammals. In J. Wiley & Sons (Ed.), Encyclopedia of life sciences (p. a0001837). Chichester: Wiley.
Wang, X., & Tedford, R. H. (2007). Evolutionary history of canids. In P. Jensen (Ed.), The behavioural biology of dogs (pp. 3–20). London: CAB International.
Wang, X., Tedford, R. H., & Antón, M. (2008). Dogs: Their fossil relatives and evolutionary history. New York: Columbia University Press.
Wayne, R. K. (1986). Cranial morphology of domestic and wild canids: The influence of development on morphological change. Evolution, 40, 243–261. https://doi.org/10.1111/j.1558-5646.1986.tb00467.x.
Wayne, R. K., Van Valkenburgh, B., Kat, P. W., Fuller, T. K., Johnson, W. E., & O’Brien, S. J. (1989). Genetic and morphological divergence among sympatric canids. Journal of Heredity, 80, 447–454. https://doi.org/10.1093/oxfordjournals.jhered.a110896.
Wayne, R. K., Geffen, E., Girman, D. J., Koepfli, K. P., Lau, L. M., & Marshall, C. R. (1997). Molecular systematics of the Canidae. Systematic Biology, 46, 622–653. https://doi.org/10.1093/sysbio/46.4.622.
Werdelin, L. (1983). Morphological patterns in the skulls of cats. Biological Journal of the Linnean Society, 19, 375–391. https://doi.org/10.1111/j.1095-8312.1983.tb00793.x.
Werneburg, I., & Geiger, M. (2017). Ontogeny of domestic dogs and the developmental foundations of carnivoran domestication. Journal of Mammalian Evolution, 24, 323–343. https://doi.org/10.1007/s10914-016-9346-9.
Westneat, M. W. (2003). A biomechanical model for analysis of muscle force, power output and lower jaw motion in fishes. Journal of Theoretical Biology, 223, 269–281. https://doi.org/10.1016/S0022-5193(03)00058-4.
Wickland, C. R., Baker, J. F., & Paterson, B. W. (1991). Torque vectors of neck muscles in the cat. Experimental Brain Research, 84, 64–659. https://doi.org/10.1007/BF00230978.
Wiens, J. J., & Graham, C. H. (2005). Niche conservatism: Integrating evolution, ecology, and conservation biology. Annual Review of Ecology, Evolution, and Systematics, 36, 519–539. https://doi.org/10.1146/annurev.ecolsys.36.102803.095431.
Wilson, D. E., & Mittermeier, R. A. (2009). Handbook of the mammals of the world (Vol. 1. Carnivores). Barcelona: Lynx Editions.
Wood, J. E. (1958). Age structure and productivity of a gray fox population. Journal of Mammalogy, 39, 74–86. https://doi.org/10.2307/1376612.
Wozencraft, W. C. (2005). Order Carnivora. In D. E. Wilson & D. M. Reeder (Eds.), Mammal species of the world. A taxonomic and geographic reference (pp. 532–628). Baltimore: The Johns Hopkins University Press.
Wroe, S., & Milne, N. (2007). Convergence and remarkably consistent constraint in the evolution of carnivore skull shape: Convergence in carnivore skull shape. Evolution, 61, 1251–1260. https://doi.org/10.1111/j.1558-5646.2007.00101.x.
Zapata, S. C., Funes, M., & Novaro, A. (1997). Estimación de la edad en el zorro colorado patagónico (Pseudalopex culpaeus). Mastozoología Neotropical, 4, 145–150.
Zar, J. H. (2009). Biostatistical analysis. New Jersey: Prentice Hall.
Zelditch, M. L., & Carmichael, A. C. (1989). Growth and intensity of integration through postnatal growth in the skull of Sigmodon fulviventer. Journal of Mammalogy, 70, 477–484. https://doi.org/10.2307/1381419.
Zelditch, M. L., Lundrigan, B. L., & Garland, T. (2004). Developmental regulation of skull morphology. I. Ontogenetic dynamics of variance. Evolution and Development, 6, 194–206. https://doi.org/10.1111/j.1525-142X.2004.04025.x.
Zrzavý, J., Duda, P., Robovský, J., Okřinová, I., & Řičánková, V. P. (2018). Phylogeny of the Caninae (Carnivora): Combining morphology, behaviour, genes and fossils. Zoologica Scripta, 47, 373–389. https://doi.org/10.1111/zsc.12293.
Zuercher, G. L., Swarner, M., Silveira, L., & Carrillo, O. (2004). Bush dog Speothos venaticus. In C. Sillero-Zubiri, M. Hoffmann, & D. W. Macdonald (Eds.), Canids: Foxes, wolves, jackals and dogs. Status survey and conservation action plan (pp. 76–80). IUCN Species Programme: Gland.
Zunino, G. E., Vaccaro, O. B., Canevari, M., & Gardner, A. L. (1995). Taxonomy of the genus Lycalopex (Carnivora: Canidae) in Argentina. Proceedings of the Biological Society of Washington, 108, 729–747.
Zurano, J. P., Martinez, P. A., Canto-Hernandez, J., Montoya-Burgos, J. I., & Costa, G. C. (2017). Morphological and ecological divergence in south American canids. Journal of Biogeography, 44, 821–833. https://doi.org/10.1111/jbi.12984.
Acknowledgments
For access to collections under their care, we thank all the curators. This is a contribution to PICT 2015-2389, 2015-0966 and 2016-3151. We thank the anonymous reviewer who provided precise comments that considerably improved this article.
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Préstamo BID PICT 2015-0966, and 2016-3151.
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Appendix 1 List of specimens used in this study
Appendix 1 List of specimens used in this study
Atelocynus microtis (N=23). AMNH: 76031; 76579; 95284; 95285; 98639; 100095. FMNH: 52491; 57836; 60674; 60675; 60676; 93955; 98080; 98081; 110949; 121286. MZUSP: 4320; 19750; 19751; 19752; 19753; 19754. NMNH: 361013.
Cerdocyon thous (N=163). AMNH: 14628; 14850; 17555; 21349; 23572; 61797; 63799; 132787; 133931; 135462; 205796; 205797; 205798; 205800; 205803; 205813; 205814; 205826. CFA: 3556; 3763; 3875; 3913; 4265; 4402; 4419; 4496; 4511; 4512; 4661; 4663; 5048; 5197; 5198; 5263; 5278; 5282; 5284; 5285; 5313; 5414; 6000; 6071; 6346. CML: 588; 3715; 3716; 3717; 3718; 3719; 3756; 3827; 4083; 4083; 4692; 5964; 5966; 5967; 5968; 6213; 6214; 6339; 6340; 6341. GECM: 154. MACN: 4.213; 17.122; 20.32; 20.34; 23.45; 24.127; 25.119; 25.159; 29.839; 30.344; 30.345; 32.261; 32.262; 32.75; 32.93; 33.6; 34.676; 36.191; 36.481; 43.26; 44.11; 45.34; 45.40; 47.116; 47.189; 47.190; 47.191; 47.192; 47.193; 47.402; 48.3; 48.5; 48.6; 48.7; 48.10; 49.367; 50.40; 50.43; 50.45; 50.57; 50.59; 50.60; 50.61; 50.62; 50.63; 50.64; 50.65; 50.66; 52.54; 52.63; 52.64; 13051; 14322; 14681; 15741; 16189; 19071; 20316; 20454; 20455; 20456; 20815; 20816; 20817; 21228; 23180; 23669; 23670; 23726; 23727; 24045; 24202; 24264; 24267. MFA-ZV: 228; 1204; 1205. MLP: 16.X.01.7; 20.IX.49.13; 1322. MZUSP: 19755; 2922; 32617; 3486; 4289; 856; 9687. NMNH: 123342; 137512; 143813; 238670; 239965; 241404; 253824; 270367; 281496; 372840; 372844; 372847.
Chrysocyon brachyurus (N=85). AMNH: 120999; 133940; 133941; 135274. CFA: 12826; 12827. CML: 1376; 6352; 6353. FMNH: 28311; 28312; 28313; 44534; 46003; 96003; 99213; 101848; 104088; 125401; 127434; 134483; 137425; 150739. MACN: 3.71; 3.73; 4.32; 4.303; 4.385; 24.4; 30.198; 30.29; 53.49; 13466; 19146; 20646; 23456; 23983; 23984; 24043; 24201. MFA-ZV: 185; 273; 517; 524; 553; 568; 581; 651; 652; 919; 1166. MLP: 2.IV.02.4; 5.X.99.1; 6; 92; 564; 695; 1684; 1686. MZUSP: 525; 3025; 3090; 3338; 3700; 9420; 19733; 19736; 19745; 28870; 31981; 32039; 32042; 32043; 32056; 32199; 32505; 32629. NMNH: 196975; 261022; 261023; 270371; 271567; 314863; 534807; 588223.
Lycalopex culpaeus (N=143). CFA: 4229; 6451. CML: 5067; 5068; 5069; 5070; 5071; 5970; 5974; 6343; 6344. LIEB: 791; 792. MACN: 3.68; 4.41; 4.211; 7.42; 25.128; 27.131; 30.69; 31.58; 31.59; 33.67; 33.68; 36.231; 38.39; 41.55; 15022; 15024; 15025; 15028; 15033; 15037; 15040; 15044; 15045; 15049; 15049; 15050; 15055; 15062; 15063; 15064; 15073; 15078; 15081; 15082; 15083; 15089; 15093; 15096; 15101; 15106; 15112; 15119; 15121; 15122; 15123; 15124; 15127; 15129; 15130; 15131; 15132; 15133; 15138; 15140; 15149; 15151; 15154; 15158; 15163; 15168; 15172; 15173; 15177; 15181; 15182; 15190; 15194; 15196; 15197; 15199; 15200; 15201; 15202; 15203; 15208; 15212; 15220; 15223; 15224; 15226; 15227; 15228; 15229; 15232; 15233; 15240; 15243; 15246; 15248; 15258; 15259; 15260; 15261; 15266; 15267; 15268; 19221; 19222; 20813; 21899; 23072; 23076; 23077; 23093; 23095; 23098; 23099; 23100; 23101; 23102; 23103; 23104; 23108; 23119; 23123; 23125; 23143; 23148; 23720; 23721; 23841; 23915; 23916; 24.119; 24047; 24210; 24270; 24271. MLP: 15.V.96.2; 1264; 1266.
Lycalopex fulvipes (N=2). FMNH: 23814; 23815.
Lycalopex griseus (N=137). AMNH: 14081; 17440a; 17440b; 17441a. CFA: 2175; 2197; 4197; 5291; 5649; 5777; 5782; 10243. CML: 837; 838; 1177; 1178; 1489; 3714; 4967; 6189; 6190; 6191. FMNH: 154639; 154640. LIEB: 794; 809. MACN: 2.38; 2.39; 3.63; 4.253; 7.40; 7.41; 23.19; 23.20; 24.50; 24.51; 24.52; 24.53; 24.54; 24.55; 24.63; 24.66; 24.76; 24.78; 24.79; 24.80; 24.81; 32.263; 50.419; 50.420; 50.432; 50.490; 51.170; 53.42; 223; 224; 225; 226; 319; 13781; 14540; 14902; 15020; 15185; 15186; 15189; 15262; 15263; 15264; 15265; 15269; 16321; 16322; 16325; 20205; 20206; 20207; 20208; 20276; 20277; 20278; 20814; 20829; 23150; 23662; 23663; 23664; 23668; 23718; 23728; 23729; 23730; 23919; 24206; 24251; 24256; 24257; 24258; 24262; 24263. MLP: 2.IV.60.1; 4.VIII.98.4; 5.III.36.27; 27.XII.01.27; 240; 441; 559; 696; 701; 712. NMNH: 482163; 482164; 92139; 92140; 92141; 92142; 92143; 92144; 92145; 92146; 92147; 92149; 92150; 92151; 92152; 92158; 92159; 92160; 92161; 92162; 92169; 92170; 92173; 92175; 92176; 92177; 92178; 92179.
Lycalopex gymnocercus (N=374). AMNH: 41502; 41503; 41504; 41505; 41506; 41507; 41508; 41509; 41510. CFA: 3255; 3698; 3962; 4256; 4416; 4417; 4659; 5219; 5280; 8588; 8589; 11062. CML: 192; 236; 495; 545; 645; 834; 836; 895; 908; 909; 959; 1179; 1526; 1526; 1529; 1558; 3072; 4081; 4082; 5143; 5473; 5474; 5479; 5480; 5772; 6342. GECM: 24; 34; 40; 57; 65; 67; 75; 76; 85; 100; 108; 112; 119; 121; 129; 139; 149; 152; 153; 179; 217Bis; 227Bis; 220Bis. MACN: 2.32; 3.10; 4.5; 4.54; 4.271; 4.290; 4.299; 20.33; 20.35; 23.33; 23.37; 23.38; 24.47; 24.48; 24.49; 24.133; 24.134; 24.140; 24.141; 24.143; 24.144; 24.148; 24.156; 24.162; 24.169; 24.171; 25.27; 26.6; 26.28; 26.87; 26.129; 26.162; 26.163; 27.53; 28.182; 29.35; 30.144; 30.150; 30.210; 30.211; 32.252; 32.263; 33.177; 33.266; 33.268; 34.317; 35.241; 35.407; 36.479; 36.480; 37.82; 38.243; 39.191; 39.194; 41.221; 44.17; 48.266; 49.134; 49.139; 49.148; 49.149; 49.159; 49.160; 49.167; 50.56; 50.443; 50.491; 50.492; 50.494; 50.495; 50.497; 50.498; 50.500; 50.501; 50.502; 50.503; 50.504; 50.505; 53.2; 53.6; 54.133; 246; 285; 293; 13299; 13313; 13327; 13331; 13337; 14319; 14323; 14386; 14409; 15363; 15364; 15387; 15388; 15389; 15390; 15601; 15692; 15742; 15748; 15749; 15750; 15751; 15752; 15754; 15757; 15758; 15760; 15761; 15762; 15764; 15765; 15766; 15769; 15771; 15783; 15784; 15785; 15787; 15788; 15789; 15791; 15792; 15794; 15795; 15796; 15797; 15800; 15818; 15820; 15831; 15833; 15834; 15838; 15854; 15856; 15858; 15859; 15860; 15861; 15862; 15863; 15864; 15865; 15866; 15867; 15868; 15869; 15870; 15871; 15873; 15875; 15879; 15882; 15888; 15892; 15894; 15895; 15896; 15898; 15901; 15902; 15906; 15908; 15909; 15917; 15932; 15933; 15934; 15938; 15941; 15954; 15958; 15963; 15964; 15966; 15970; 15973; 15979; 15981; 15982; 15986; 15987; 15992; 15998; 15999; 16000; 16001; 16002; 16003; 16004; 16005; 16006; 16007; 16009; 16010; 16013; 16014; 16015; 16024; 16025; 16026; 16027; 16030; 16031; 16032; 16035; 16036; 16037; 16038; 16039; 16040; 16041; 16046; 16047; 16048; 16049; 16050; 16053; 16055; 16059; 16062; 16063; 16066; 16068; 16074; 16077; 16079; 16080; 16083; 16085; 16088; 16094; 16096; 16097; 16099; 16100; 16101; 16102; 16103; 16104; 16105; 16106; 16107; 16108; 16110; 16111; 16115; 16117; 16118; 16120; 16122; 16123; 16130; 16131; 16139; 16143; 16145; 16149; 16151; 22936; 23153; 23154; 23155; 23156; 23157; 23158; 23290; 23910; 23913; 23920; 24203; 24204; 24205; 24208; 24209; 24259; 24265; 24266; 24282. MLP: 16.III.99.16; 20.IV.95.3; 30.III.99.13; 13.IV.99.3; 13.IV.99.13; 13.IV.99.14; 13.IV.99.19; 13.IV.99.20; 13.IV.99.31; 13.IV.99.35; 13.IV.99.36; 13.IV.99.44; 26.V.95.9; 4.VIII.98.9; 30.XII.02.65; 442; 710. NMNH: 172789; 172790; 236362; 236366; 331065.
Lycalopex sechurae (N=39). AMNH: 46525; 46527; 46528; 46529; 46530; 46531; 46532; 46533; 63709. FMNH: 19541; 19971; 19972; 21129; 41237; 53911; 53912; 53913; 80953; 80954; 80955; 80956; 80957; 80958; 80959; 80960; 80961; 80962; 80963; 80964; 80965; 80966; 80967; 80968; 80969. NMNH: 121171; 121172; 181150; 545109; 545110.
Lycalopex vetulus (N=34). AMNH: 349; 391; 70091; 100091; 100100; 133926; 133927; 133928; 133929; 133937; 245699. FMNH: 20747. MACN: 3.17. MLP: 1258. MZUSP: 825; 1011; 1012; 1014; 1015; 1016; 1018; 1075; 1076; 1084; 2170; 2479; 3046; 3047; 3047; 3048; 3049; 3050; 12040; 13611.
Speothos venaticus (N=43). AMNH: 37472; 76035; 76805; 76806; 98558; 98559; 98560; 98640; 136284; 136285; 167846; 175306; 184688; 202839. FMNH: 60290; 60579; 87861; 121544; 125402. MACN 33.154; 50.67; 16510. MZUSP: 19743; 19744. NMNH: 179047; 179048; 253504; 269135; 270165; 270171; 270368; 270369; 270370; 307650; 314048; 395841; 398030; 521045; 538307; 544414; 546298; 582465; 583255.
Urocyon cinereoargenteus (N=92). AMNH: 6405; 8197; 19207; 26012; 26013; 100301; 120989; 121664; 127561; 127573; 127575; 127576; 183939; 183942; 183943; 183953; 183954; 183956; 183960; 183973; 183979; 183991; 183995; 184002; 184007; 184009; 184012; 184013; 184014; 184064; 184065; 184068; 184077; 184080; 184083; 184087; 184091; 184092; 184094; 184097; 184098; 184105; 184117; 184121; 184122; 184126; 184132; 185512; 203066; 243095; 243449; 254470; 255645; 255646; 255648; 255649. NMNH: 14552; 14553; 21391; 29287; 34860; 35531; 54991; 55501; 61207; 68193; 73466; 76424; 91173; 91174; 98305; 107209; 117637; 117640; 130065; 133191; 151224; 151237; 180262; 180740; 188094; 203121; 215376; 215377; 215378; 265932; 265933; 271091; 287505; 507119; 529675; 569080.
Canis lupus (N=11). AMNH: 16848; 18215; 18218; 18238; 19124; 34468. MACN: 3.76; 23.12; 23.15; 35.210. MLP: 1031.
Vulpes vulpes (N=81). AMNH: 3796; 6412; 6413; 6414; 6415; 6416; 19024; 19841; 59311; 60131; 60132; 70165; 80061; 85032; 85033; 90799; 146724; 147569; 150299; 150300; 242479. FMNH: 74469; 74472; 74987; 74988; 74989; 75644; 75645; 75646; 77130; 77136; 78650; 78651; 80827; 80829; 80836; 80837; 80839; 80840; 84697; 84698; 85216; 85217; 85218; 86820; 89369; 89370; 89371; 89372; 89587; 89595; 89710; 89712; 89963; 90361; 90473; 90474; 91605; 91725; 91726; 91731; 91741; 92264; 92265; 92267; 92636; 92727; 95863; 95865; 95867; 95870; 95872; 95873; 98733; 98734; 98735; 98736; 106726; 107271; 140172; 140176.
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Segura, V., Cassini, G.H. & Prevosti, F.J. Evolution of Cranial Ontogeny in South American Canids (Carnivora: Canidae). Evol Biol 48, 170–189 (2021). https://doi.org/10.1007/s11692-020-09529-3
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DOI: https://doi.org/10.1007/s11692-020-09529-3