Skip to main content

Advertisement

SpringerLink
Log in

Comparative craniometric analysis between two species of South American canids and domestic dogs

  • Research
  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

Abstract

A comparative craniometric analysis among maned wolves (Chrysocyon brachyurus, n = 9), crab-eating foxes (Cerdocyon thous, n = 8) and domestic dogs (Canis lupus familiaris, n = 124) was performed. A total of 18 craniometric measurements were taken from these specimens, and eight craniometric indices were further computed from those measurements. Using correlation analysis, we found that the 26 variables could be clustered into four groups, namely: (1) indicators of rostro-caudal length; (2) ventro-dorsal height and latero-lateral width; (3) cranial indices; and (4) dimensions of the foramen magnum. Consequently, multivariate techniques were applied to the data in order to reduce dimensionality and thus facilitate the comparisons among domestic and wild species. The projection of the data into the lower-dimensional space created by a principal component analysis showed that skulls of crab-eating foxes resembled small mesaticephalic skulls of domestic dogs, whereas the skulls of maned wolves were closer to those of larger dolichocephalic dogs. However, both species shared similarities with the mesaticephalic and dolichocephalic morphotypes of domestic dogs when variables were considered individually. Importantly, the variation in skull morphology found in the wild specimens was significantly smaller than that found in domestic dogs. These findings suggest an evolutionary constraint to skull shape diversity in maned wolves and crab-eating foxes, which seems consistent with adaptation to a generalist omnivorous diet.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Availability of data and materials

The craniometric measurements of each specimen are provided in Online Resource 3.

References

  • American Kennel Club (2023) Breed Weight Chart. Available at: https://www.akc.org/expert-advice/nutrition/breed-weight-chart/. Accessed on 19 Jan 2023.

  • Boyko AR, Quignon P, Li L, Schoenebeck JJ, Degenhardt JD, Lohmueller KE, Zhao K, Brisbin A, Parker HG, vonHoldt BM, Cargill M, Auton A, Reynolds A, Elkahloun AG, Castelhano M, Mosher DS, Sutter NB, Johnson GS, Novembre J, Hubisz MJ, Siepel A, Wayne RK, Bustamante CD, Ostrander EA (2010) A simple genetic architecture underlies morphological variation in dogs. PLoS Biol 8(8):e1000451. https://doi.org/10.1371/journal.pbio.1000451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boyle EA, Li YI, Pritchard JK (2017) An expanded view of complex traits: From polygenic to omnigenic. Cell 169(7):1177-1186. https://doi.org/10.1016/j.cell.2017.05.038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calaway M (2001) Possible index to distinguish between Canis latrans and Canis familiaris. Lambda Alpha J 31:24–27. http://hdl.handle.net/10057/1882

  • Chavez DE, Gronau I, Hains T, Dikow RB, Frandsen PB, Figueiró HV, Garcez FS, Tchaicka L, de Paula RC, Rodrigues FHG, Jorge RSP, Lima ES, Songsasen N, Johnson WE, Eizirik E, Koepfli KP, Wayne RK (2022) Comparative genomics uncovers the evolutionary history, demography, and molecular adaptations of South American canids. Proc Natl Acad Sci U S A 119(34):e2205986119. https://doi.org/10.1073/pnas.2205986119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Courtenay O, Maffei L (2004) Crab-eating fox Cerdocyon thous. In: Sillero-Zubiri C, Hoffmann M and Macdonald DW (2004) Canids: foxes, wolves, jackals and dogs - status survey and conservation action plan. IUCN, Gland, Switzerland and Cambridge, UK, pp 32-38.

    Google Scholar 

  • de Moura Bubadué J, Cáceres N, Dos Santos Carvalho R, Meloro C. (2016) 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

    Article  Google Scholar 

  • Drake AG, Klingenberg CP (2010) Large-scale diversification of skull shape in domestic dogs: Disparity and modularity. Am Nat 175(3):289-301. https://doi.org/10.1086/650372

    Article  PubMed  Google Scholar 

  • Dutra-Vieira FM, Silva MS, Vieira GS, Carvalho AS, Schmming BC (2021) Diet of crab-eating fox (Cerdocyon thous) in two conservation units of the Amazon rainforest, Brazil. Braz J Biol 84:e252093. https://doi.org/10.1590/1519-6984.252093

    Article  CAS  PubMed  Google Scholar 

  • Geiger M, Haussman S (2016) Cranial suture closure in domestic dog breeds and its relationships to skull morphology Anat Rec 299(4):412-420. https://doi.org/10.1002/ar.23313

    Article  PubMed  Google Scholar 

  • IUCN (2022). The IUCN Red List of Threatened Species. Version 2022–2. https://www.iucnredlist.org. Accessed on 15 Jun 2023.

  • Kassambara A, Mundt F (2020) factoextra: Extract and Visualize the Results of Multivariate Data Analyses. https://cran.r-project.org/web/packages/factoextra/index.html.

  • Kyllar M, Paral V, Pyszko M, Doskarova B (2016) Facial pillars in dogs: an anatomical study. Anat Sci Int 92(3):343-351. https://doi.org/10.1007/s12565-016-0338-x

    Article  PubMed  Google Scholar 

  • Lindblad-Toh K, Wade CM, Mikkelsen TS, Karlsson EK, Jaffe DB, Kamal M, Clamp M, Chang JL, Kulbokas EJ 3rd, Zody MC, Mauceli E, Xie X, Breen M, Wayne RK, Ostrander EA, Ponting CP, Galibert F, Smith DR, DeJong PJ, Kirkness E, Alvarez P, Biagi T, Brockman W, Butler J, Chin CW, Cook A, Cuff J, Daly MJ, DeCaprio D, Gnerre S, Grabherr M, Kellis M, Kleber M, Bardeleben C, Goodstadt L, Heger A, Hitte C, Kim L, Koepfli KP, Parker HG, Pollinger JP, Searle SM, Sutter NB, Thomas R, Webber C, Baldwin J, Abebe A, Abouelleil A, Aftuck L, Ait-Zahra M, Aldredge T, Allen N, An P, Anderson S, Antoine C, Arachchi H, Aslam A, Ayotte L, Bachantsang P, Barry A, Bayul T, Benamara M, Berlin A, Bessette D, Blitshteyn B, Bloom T, Blye J, Boguslavskiy L, Bonnet C, Boukhgalter B, Brown A, Cahill P, Calixte N, Camarata J, Cheshatsang Y, Chu J, Citroen M, Collymore A, Cooke P, Dawoe T, Daza R, Decktor K, DeGray S, Dhargay N, Dooley K, Dooley K, Dorje P, Dorjee K, Dorris L, Duffey N, Dupes A, Egbiremolen O, Elong R, Falk J, Farina A, Faro S, Ferguson D, Ferreira P, Fisher S, FitzGerald M, Foley K, Foley C, Franke A, Friedrich D, Gage D, Garber M, Gearin G, Giannoukos G, Goode T, Goyette A, Graham J, Grandbois E, Gyaltsen K, Hafez N, Hagopian D, Hagos B, Hall J, Healy C, Hegarty R, Honan T, Horn A, Houde N, Hughes L, Hunnicutt L, Husby M, Jester B, Jones C, Kamat A, Kanga B, Kells C, Khazanovich D, Kieu AC, Kisner P, Kumar M, Lance K, Landers T, Lara M, Lee W, Leger JP, Lennon N, Leuper L, LeVine S, Liu J, Liu X, Lokyitsang Y, Lokyitsang T, Lui A, Macdonald J, Major J, Marabella R, Maru K, Matthews C, McDonough S, Mehta T, Meldrim J, Melnikov A, Meneus L, Mihalev A, Mihova T, Miller K, Mittelman R, Mlenga V, Mulrain L, Munson G, Navidi A, Naylor J, Nguyen T, Nguyen N, Nguyen C, Nguyen T, Nicol R, Norbu N, Norbu C, Novod N, Nyima T, Olandt P, O'Neill B, O'Neill K, Osman S, Oyono L, Patti C, Perrin D, Phunkhang P, Pierre F, Priest M, Rachupka A, Raghuraman S, Rameau R, Ray V, Raymond C, Rege F, Rise C, Rogers J, Rogov P, Sahalie J, Settipalli S, Sharpe T, Shea T, Sheehan M, Sherpa N, Shi J, Shih D, Sloan J, Smith C, Sparrow T, Stalker J, Stange-Thomann N, Stavropoulos S, Stone C, Stone S, Sykes S, Tchuinga P, Tenzing P, Tesfaye S, Thoulutsang D, Thoulutsang Y, Topham K, Topping I, Tsamla T, Vassiliev H, Venkataraman V, Vo A, Wangchuk T, Wangdi T, Weiand M, Wilkinson J, Wilson A, Yadav S, Yang S, Yang X, Young G, Yu Q, Zainoun J, Zembek L, Zimmer A, Lander ES (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438(7069):803-19. https://doi.org/10.1038/nature04338

    Article  CAS  PubMed  Google Scholar 

  • Marchant TW, Johnson EJ, McTeir L, Johnson CI, Gow A, Liuti T, Kuehn D, Svenson K, Bermingham ML, Drögemüller M, Nussbaumer M, Davey MG, Argyle DJ, Powell RM, Guilherme S, Lang J, Haar GT, Leeb T, Schwarz T, Mellanby RJ, Clements DN, Schoenebeck JJ (2017) Canine brachycephaly is associated with a retrotransposon-mediated missplicing of SMOC2. Curr Biol 27(11):1573-1584.e6. https://doi.org/10.1016/j.cub.2017.04.057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marsden CD, Ortega-Del Vecchyo D, O'Brien DP, Taylor JF, Ramirez O, Vilà C, Marques-Bonet T, Schnabel RD, Wayne RK, Lohmueller KE (2016) Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs. Proc Natl Acad Sci U S A 113(1):152-7. https://doi.org/10.1073/pnas.1512501113

    Article  CAS  PubMed  Google Scholar 

  • Mathieson I (2021) The omnigenic model and polygenic prediction of complex traits. Am J Hum Genet 108(9):1558-1563. https://doi.org/10.1016/j.ajhg.2021.07.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Motta-Junior JC, Talamoni SA, Lombardi JA, Simokomaki K (1996) Diet of the maned wolf, Chrysocyon brachyurus, in central Brazil. J Zool 240:277-284. https://doi.org/10.1111/j.1469-7998.1996.tb05284.x

    Article  Google Scholar 

  • Neto AM, Viotto de Souza W, Fromme L, Domingues MG, Guimarães LP, Silva TA, Santos ALQ (2020) Craniometry in Cerdocyon thous (Carnivora, Canidae). Int J Morphol 38(3):640-644. https://doi.org/10.4067/S0717-95022020000300640

    Article  Google Scholar 

  • Parker HG, VonHoldt BM, Quignon P, Margulies EH, Shao S, Mosher DS, Spady TC, Elkahloun A, Cargill M, Jones PG, Maslen CL, Acland GM, Sutter NB, Kuroki K, Bustamante CD, Wayne RK, Ostrander EA (2009) An expressed fgf4 retrogene is associated with breed-defining chondrodysplasia in domestic dogs. Science 325(5943):995-8. https://doi.org/10.1126/science.1173275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perini FA, Russo CA, Schrago CG. The evolution of South American endemic canids: a history of rapid diversification and morphological parallelism. J Evol Biol 23(2):311–22. https://doi.org/10.1111/j.1420-9101.2009.01901.x

  • Plassais J, Kim J, Davis BW, Karyadi DM, Hogan AN, Harris AC, Decker B, Parker HG, Ostrander EA (2019) Whole genome sequencing of canids reveals genomic regions under selection and variants influencing morphology. Nat Commun 10(1):1489. https://doi.org/10.1038/s41467-019-09373-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2023) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Raymond PW, Velie BD, Wade CM (2022) Forensic DNA phenotyping: Canis familiaris breed classification and skeletal phenotype prediction using functionally significant skeletal SNPs and indels. Anim Genet 53(3):247-263. https://doi.org/10.1111/age.13165

    Article  CAS  PubMed  Google Scholar 

  • Rodden M, Rodrigues F, Bestelmeye S (2004) Maned wolf Chrysocyon brachyurus. In: Sillero-Zubiri C, Hoffmann M and Macdonald DW (2004) Canids: Foxes, Wolves, Jackals and Dogs - status survey and conservation action plan. IUCN, Gland, Switzerland and Cambridge, UK, pp 32–38.

  • Santos LQS, Paz BF, Barros RF, Nalla SF, Pereira TS (2017) Craniometric measurements in maned wolves Chrysocyon brachyurus Illiger, 1815 (Carnivora, Canidae). Cienc Anim Bras 18:e-37693. https://doi.org/10.1590/1089-6891v18e-37693

  • Schimming BC, Pinto e Silva JRC. (2013) Craniometric measurements in dogs (Canis familiaris). Features in the mesaticephalic skulls. Braz J Vet Res Anim Sci 50(1):5–11. https://doi.org/10.11606/issn.2318-3659.v50i1p5-11

  • Schoenebeck JJ, Ostrander EA (2013) The genetics of canine skull shape variation. Genetics 193(2):317-325. https://doi.org/10.1534/genetics.112.145284

    Article  PubMed  PubMed Central  Google Scholar 

  • Slater GJ, Dumont ER, Valkenburgh BV (2009) Implications of predatory specialization for cranial form and function in canids. J Zool 278:181-188. https://doi.org/10.1111/j.1469-7998.2009.00567.x

    Article  Google Scholar 

  • Tseng ZJ, Flynn JJ (2018) Structure-function covariation with nonfeeding ecological variables influences evolution of feeding specialization in Carnivora. Sci Adv 4(2):eaao5441. https://doi.org/10.1126/sciadv.aao5441

  • Warnes GR (2011) gplots: Various R Programming Tools for Plotting Data. http://cran.r-project.org/web/packages/gplots/index.html

  • Wayne RK, Geffen E, Girman DJ, Koepfli KP, Lau LM, Marshall CR (1997) Molecular systematics of the Canidae. Syst Biol 46(4):622-53. https://doi.org/10.1093/sysbio/46.4.622

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to Pedro Luis Florindo for his support on handling the canid specimens. We also thank the Editor and two anonymous reviewers for their suggestions to improve the manuscript.

Funding

This research was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.

Author information

Authors and Affiliations

  1. Department of Production and Animal Health, School of Veterinary Medicine of Araçatuba (FMVA), São Paulo State University (Unesp), Araçatuba, SP, Brazil

    Rodrigo Antonio Fernandes, Isabelle Leite Miam, Guilherme da Silva Rogério, Luciana Del Rio Pinoti, Fabiano Antonio Cadioli & Yuri Tani Utsunomiya

  2. Department of Preventive Veterinary Medicine and Animal Reproduction, School of Agricultural and Veterinarian Sciences (FCAV), São Paulo State University (Unesp), Jaboticabal, SP, Brazil

    Fabiano Antonio Cadioli

Authors
  1. Rodrigo Antonio Fernandes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Isabelle Leite Miam
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guilherme da Silva Rogério
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luciana Del Rio Pinoti
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fabiano Antonio Cadioli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yuri Tani Utsunomiya
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

R.A.F., F.A.C. and Y.T.U. conceived and designed the study; R.A.F., I.L.M. and G.S.R. performed traditional craniometric analyses; R.A.F., I.L.M. and L.D.R.P. performed radiographic craniometric analyses; R.A.F. and Y.T.U. performed statistical analyses; R.A.F. and Y.T.U. wrote the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Rodrigo Antonio Fernandes.

Ethics declarations

Competing interests

The authors declare no competing interests.

Supplementary Information

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fernandes, R.A., Miam, I.L., da Silva Rogério, G. et al. Comparative craniometric analysis between two species of South American canids and domestic dogs. J Mammal Evol 31, 1 (2024). https://doi.org/10.1007/s10914-023-09697-x

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10914-023-09697-x

Keywords

Search

Navigation