Integration or Modularity in the Mandible of Canids (Carnivora: Canidae): a Geometric Morphometric Approach

Abstract

Understanding the interplay between morphological integration and modularity is considered an important topic in the study of the evolution of the form of complex structures. The mandible is a complex structure that can be shaped by diverse factors such as ontogeny, ecology, and evolutionary history. In canids, this is particularly interesting because they have a large diversity in feeding behavior and hunting strategy. Here, we employed geometric morphometric techniques to evaluate the balance between integration and modularity in 1011 mandibles of a sample of extinct and extant canids. The results show that allometric scaling seems to have little influence in determining the mandibular shape of canids. Some divergence associated with ecology was observed, especially for highly specialized taxa (hypercarnivores and insectivores). Finally, macroevolutionary patterns were more integrated than intraspecific patterns, suggesting that correlational selection might play a strong role in the evolution of mandibular form and function. We found no evidence of an evolutionary line of least resistance in shaping mandible disparity.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Adams DC (2014) A generalized K statistic for estimating phylogenetic signal from shape and other high-dimensional multivariate data. Syst Biol 63:685–697

  2. Adams DC (2016) Evaluating modularity in morphometric data: challenges with the RV coefficient and a new test measure. Methods Ecol Evol 7:565–572. https://doi.org/10.1111/2041-210X.12511

    Article  Google Scholar 

  3. Adams DC, Felice RN (2014) Assessing trait covariation and morphological integration on phylogenies using evolutionary covariance matrices. PLoS One 9:e94335–e94338

    Article  Google Scholar 

  4. Adams DC, Otárola-Castillo E (2013) Geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol Evol 4:393–399

  5. Biknevicius AR, Ruff CB (1992) Use of biplanar radiographs for estimating cross-sectional geometric properties of mandibles. Anat Rec 232:157–163

    CAS  Article  Google Scholar 

  6. Bookstein FL (1991) Morphometric Tools for Landmark Data. Geometry and Biology. Cambridge University Press, New York

  7. Bubadué J de M, Cáceres N, Santos Carvalho R dos, Meloro C (2016) Ecogeographical variation in skull shape of South-American canids: abiotic or biotic processes? Evol Biol 43: 145–159

  8. Cerny R, Lwigale P, Ericsson R, Meulemans D, Epperlein H. H, Bronner-Fraser M (2004) Developmental origins and evolution of jaws: new interpretation of “maxillary” and “mandibular.” Dev Biol 276:225–236

  9. Cheverud JM (1996) Developmental integration and the evolution of pleiotropy. Am Zool 36:44–50

    Article  Google Scholar 

  10. Christiansen P (2008) Evolution of skull and mandible shape in cats (Carnivora: Felidae). PLoS One 3:e2807

    Article  Google Scholar 

  11. Clark HO (2005) Otocyon megalotis. Mammal Species 766:1–5

    Article  Google Scholar 

  12. Conith AJ, Meagher MA, Dumont ER (2018) The influence of climatic variability on morphological integration, evolutionary rates, and disparity in the Carnivora. Am Nat 191:704–715

    Article  Google Scholar 

  13. Curth S, Fischer MS, Kupczik K (2017) Patterns of integration in the canine skull: an inside view into the relationship of the skull modules of domestic dogs and wolves. Zoology 125:1–9

    Article  Google Scholar 

  14. Echarri S, Prevosti FJ (2015) Differences in mandibular disparity between extant and extinct species of metatherian and placental carnivore clades. Lethaia 48:196–204

    Article  Google Scholar 

  15. Emerson SB, Radinsky LB (1980) Functional analysis of sabretooth cranial morphology. Paleobiology 6:295–312

    Article  Google Scholar 

  16. Esteve-Altava B (2017) In search of morphological modules: a systematic review. Biol Rev 92:1332–1347

    Article  Google Scholar 

  17. Ewer RF (1998) The Carnivores. Cornell University Press, Ithaca

    Google Scholar 

  18. Figueirido B, Serrano-Alarcón FJ, Slater GJ, Palmqvist P (2010) Shape at the cross-roads: homoplasy and history in the evolution of the carnivoran skull towards herbivory. J Evol Biol 23:2579–2594

  19. Garcia GRG, Hingst-Zaher E, Cerqueira R, Marroig G (2014) Quantitative genetics and modularity in cranial and mandibular morphology of Calomys expulsus. Evol Biol 41:619–636. doi: https://doi.org/10.1007/s11692-014-9293-4

    Article  Google Scholar 

  20. Goodall CR (1991) Procrustes methods in the statistical analysis of shape. J Roy Stat Soc Ser B (Methodological) 53:285–339

    Google Scholar 

  21. Greaves WS (1982) A mechanical limitation on the position of the jaw muscles of mammals: the one-third rule. J Mammal 63:261–266

    Article  Google Scholar 

  22. Greaves WS (1983) A functional analysis of carnassial biting. Biol J Linnean Soc 20:353–363

    Article  Google Scholar 

  23. Hallgrímsson B, Jamniczky H, Young NM, Rolian C, Parsons TE, Boughner JC, Marcucio RS (2009) Deciphering the palimpsest: studying the relationship between morphological integration and phenotypic covariation. Evol Biol 36:355–376

  24. Hansen T (1997) Stabilizing selection and the comparative analysis of adaptation. Evolution 51:1341–1351

    Article  Google Scholar 

  25. Hansen T, Houle D (2008) Measuring and comparing evolvability and constraint in multivariate characters. J Evol Biol 21:1201–1219

    CAS  Article  Google Scholar 

  26. Harmon LJ, Schulte JA, Larson A, Losos JB (2003) Tempo and mode of evolutionary radiation in iguanian lizards. Science 301:961–964

    CAS  Article  Google Scholar 

  27. Holliday JA, Steppan SJ (2004) Evolution of hypercarnivory: the effect of specialization on morphological and taxonomic diversity. Paleobiology 30:108–128

  28. Klingenberg CP (2008) Morphological integration and developmental modularity. Annu Rev Ecol Evol Syst 39:115–132

    Article  Google Scholar 

  29. Klingenberg CP (2009) Morphometric integration and modularity in configurations of landmarks: tools for evaluating a priori hypotheses. Evol Dev 11:405–421

  30. Klingenberg CP, Leamy LJ, Cheverud JM (2004) Integration and modularity of quantitative trait locus effects on geometric shape in the mouse mandible. Genetics 166:1909–1921

    CAS  Article  Google Scholar 

  31. La Croix S, Holekamp KE, Shivik JA, Lundrigan BL, Zelditch ML (2011a) Ontogenetic relationships between cranium and mandible in coyotes and hyenas. J Morphol 272:662–674

    Article  Google Scholar 

  32. La Croix S, Zelditch ML, Shivik JA, Lundrigan BL, Holekamp KE (2011b) Ontogeny of feeding performance and biomechanics in coyotes. J Zool 285:301–315

    Article  Google Scholar 

  33. Larouche O, Zelditch ML, Cloutier R (2018) Modularity promotes morphological divergence in ray-finned fishes. Sci Rep 8:7278

    Article  Google Scholar 

  34. Machado FA, Hingst-Zaher E (2009) Investigating South American biogeographic history using patterns of skull shape variation on Cerdocyon thous (Mammalia: Canidae). Biol J Linnean Soc 98:77–84

  35. Machado FA, Teta P (2020) Morphometric analysis of skull shape reveals unprecedented diversity of African Canidae. J Mammal

  36. Machado FA, Zahn TMG, 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

  37. Marroig G, Cheverud JM (2010) Size as a line of least resistance II: direct selection on size or correlated response due to constraints? Evolution 64:1470–1488

  38. 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 3:595–512

    Google Scholar 

  39. Meloro C, Hudson A, Rook L (2014) Feeding habits of extant and fossil canids as determined by their skull geometry. J Zool 295:178–188

    Article  Google Scholar 

  40. Meloro C, O’Higgins P (2011) Ecological adaptations of mandibular form in fissiped Carnivora. J Mammal Evol 18:185–200

    Article  Google Scholar 

  41. Meloro C, Raia P, Carotenuto F, Cobb SN (2011) Phylogenetic signal, function and integration in the subunits of the carnivoran mandible. Evol Biol 38:465–475

    Article  Google Scholar 

  42. Meloro C, Raia P, Piras P, Barbera C, O’Higgins P (2008) The shape of the mandibular corpus in large fissiped carnivores: allometry, function and phylogeny. Zool J Linn Soc 154:832–845

  43. Mitteroecker P, Bookstein FL (2007) The conceptual and statistical relationship between modularity and morphological integration. Syst Zool 56:818

    Google Scholar 

  44. Mitteroecker P, Bookstein F (2008) The evolutionary role of modularity and integration in the hominoid cranium. Evolution 62:943–958

    Article  Google Scholar 

  45. Muñoz NA, Cassini GH, Candela AM, Vizcaíno SF (2017) Ulnar articular surface 3-D landmarks and ecomorphology of small mammals: a case study of two early Miocene typotheres (Notoungulata) from Patagonia. Earth Env Sci Trans R Soc 106:315–323

  46. Murrell DJ (2018) A global envelope test to detect non-random bursts of trait evolution. Methods Ecol Evol 9:1739–1748

    Article  Google Scholar 

  47. Nowak RM (2005) Walker’s Carnivores of the World. John Hopkins University Press, London

    Google Scholar 

  48. Olson EC, Miller RL (1958) Morphological Integration. University of Chicago Press, Chicago

  49. Oudot M, Neige P, Laffont R, Navarro N, Khaldi AY, Crônier C (2019) Functional integration for enrolment constrains evolutionary variation of phacopid trilobites despite developmental modularity. Palaeontology 4:393–317. https://doi.org/10.1111/pala.12428

    Article  Google Scholar 

  50. Parr WC, Wilson LA, Wroe S, Colman NJ, Crowther MS, Letnic M (2016) Cranial shape and the modularity of hybridization in dingoes and dogs; hybridization does not spell the end for native morphology. Evol Biol 43:171–187.

    Article  Google Scholar 

  51. Penrose F, Kemp GJ, Jeffery N (2016) Scaling and accommodation of jaw adductor muscles in Canidae. Anat Rec 299:951–966

  52. Polly PD, Lawing AM, Fabre AC, Goswami A (2013) Phylogenetic principal components analysis and geometric morphometrics. Hystrix 24:33–41

    Google Scholar 

  53. Porto A, Shirai LT, Oliveira FB, Marroig G (2013) Size variation, growth strategies, and the evolution of modularity in the mammalian skull. Evolution 67:3305–3322. https://doi.org/10.1111/evo.12177

    Article  PubMed  Google Scholar 

  54. Prevosti FJ, Turazzini GF, Ercoli MD, Hingst-Zaher E (2011) Mandible shape in marsupial and placental carnivorous mammals: a morphological comparative study using geometric morphometrics. Zool J Linn Soc 164:836–855

  55. Prevosti FJ, Segura V, Cassini GH (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

  56. R Core Team (2018) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna

  57. Radinsky LB (1981a) Evolution of skull shape in carnivores 1. Representative modern carnivores. Biol J Linnean Soc 15:369–388

    Article  Google Scholar 

  58. Radinsky LB (1981b) Evolution of skull shape in carnivores 2. Additional modern carnivores. Biol J Linnean Soc 16:337–355

    Article  Google Scholar 

  59. Radinsky LB (1982) Evolution of skull shape in carnivores. 3. The origin and early radiation of the modern carnivore families. Paleobiology 8:177–195

    Article  Google Scholar 

  60. Rayner JM (1985) Linear relations in biomechanics: the statistics of scaling functions. J Zool 206:415–439

  61. Revell LJ (2009) Size-correction and principal components for interspecific comparative studies. Evolution 63:3258–3268

  62. Rohlf FJ (1999) Shape statistics: Procrustes superimpositions and tangent spaces. J Classif 16:197–223

  63. Rohlf FJ, Corti M (2000) Use of two-block partial least-squares to study covariation in shape. Syst Zool 49:740

  64. Schiaffini MI, Segura V, Prevosti FJ (2019) Geographic variation in skull shape and size of the pampas fox Lycalopex gymnocercus (Carnivora: Canidae) in Argentina. Mammal Biol 97:50–58

  65. Schlager S (2017) Morpho and Rvcg - shape analysis in R. In: Zheng G, Li S, Szekely G (eds) Statistical Shape and Deformation Analysis. Academic Press, London, pp 217–256

  66. Schluter D (1996) Adaptive radiation along genetic lines of least resistance. Evolution 50:1766–1774

  67. Segura V (2014) Ontogenia craneana postnatal en canidos y felidos neotropicales: funcionalidad y patrones evolutivos. Ph.D. Thesis, Universidad Nacional de La Plata, Argentina

  68. Segura V, Cassini GH, Prevosti FJ (2017) Three-dimensional cranial ontogeny in pantherines (Panthera leo, P. onca, P. pardus, P. tigris; Carnivora: Felidae). Biol J Linnean Soc 120:210–227

    Google Scholar 

  69. Segura V, Prevosti FJ (2012) A quantitative approach to the cranial ontogeny of Lycalopex culpaeus (Carnivora: Canidae). Zoomorphology 131:79–92

  70. Sidlauskas B (2008) Continuous and arrested morphological diversification in sister clades of characiform fishes: a phylomorphospace approach. Evolution 62:3135–3156

  71. Silva FM, Prudente ALDC, Machado FA, Santos MM, Zaher H, Hingst-Zaher E (2017) Aquatic adaptations in a Neotropical coral snake: a study of morphological convergence. J Zool Syst Evol Res 4:393–313. https://doi.org/10.1111/jzs.12202

  72. Slater GJ, Dumont ER, Van Valkenburgh B (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

  73. Slater GJ, Price SA, Santini F, Alfaro ME (2010) Diversity versus disparity and the radiation of modern cetaceans. Proc R Soc B-Biol Sci 277:3097–3104

    Article  Google Scholar 

  74. Sydney NV, Machado FA, Hingst-Zaher E. (2012) Timing of ontogenetic changes of two cranial regions in Sotalia guianensis (Delphinidae). Mammal Biol 77:397–403

    Article  Google Scholar 

  75. Therrien F (2005) Mandibular force profiles of extant carnivorans and implications for the feeding behaviour of extinct predators. J Zool 267:249–270

    Article  Google Scholar 

  76. Tseng ZJ, Binder WJ (2009) Mandibular biomechanics of Crocuta crocuta, Canis lupus, and the late Miocene Dinocrocuta gigantea (Carnivora, Mammalia). Zool J Linnean Soc 158:683–696

    Article  Google Scholar 

  77. Van Valkenburgh B (1991) Iterative evolution of hypercarnivory in canids (Mammalia: Carnivora): evolutionary interactions among sympatric predators. Paleobiology 17:340–362

  78. Van Valkenburgh B, Wayne RK (1994) Shape divergence associated with size convergence in sympatric East African jackals. Ecology 75:1567–1581

  79. Wainwright PC, Reilly SM (1994) Ecological Morphology. University of Chicago Press, Chicago

  80. Wayne RK (1986) Cranial morphology of domestic and wild canids: the influence of development on morphological change. Evolution 40 (2):243–261

  81. Zrzavý J, Duda P, Robovský J, Okřinová I, Řičánková VP (2018) Phylogeny of the Caninae (Carnivora): combining morphology, behaviour, genes and fossils. Zool Scr 47:373–389

  82. 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

Download references

Acknowledgments

We thank to N. Toledo and S. Vizcaíno for inviting us to participate in this tribute to L.B. Radinsky within the framework of the Symposium: El paradigma de correlación forma-función en mastozoología: un tributo a Leonard Radinsky (1937–1985), which took place during the XXXI Jornadas Argentinas de Mastozoología, in La Rioja, Argentina, 25 October, 2018. For permission to access material under their care and the attention in mammal collections we thank Robert Voss, Eileen Westwig (AMNH), Sergio Bogan, Yolanda Davies (CFA), Rubén Barquez, Mónica Díaz (CML), Bruce Patterson (FMNH), Mauro Lucherini, Estela Luengos (GECM), Mauro Schiaffini, Gabriel Martin (LIEB), Andrés Pautasso (MFAZV), Pablo Teta, David Flores, Sergio Lucero (MACN), Diego Verzi, Itatí Olivares (MLP), Mario de Vivo, Juliana Gualda (MZUSP), and Kristofer Helgen, Darrin Lunde (NMNH). This is a contribution to PICT 2014-1930, 2015-2389, 2015-0966, 2016-3151, 2016-3682, PUE 0125 and DEB 1350474 (NSF grant to Liam Revell).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Valentina Segura.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Comment on Ethics

This article does not contain any studies with human participants or animals performed by any of the authors.

Electronic supplementary material

ESM 1

(PDF 417 kb)

ESM 2

(PDF 677 kb)

ESM 3

(PDF 1065 kb)

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: 5249; 57836; 60674; 60675; 60676; 93955; 98080; 98081; 110949; 121286. MZUSP: 4320; 19750; 19751; 19752; 19753; 19754. NMNH: 361013.

Canis aureus (N = 1). MLP: 1035–1031.

Canis latrans (N = 1). MACN: 25.123.

Canis lupus (N = 5). AMNH: 18215. MACN 3.76; 23.15; 35.210. MLP: 1031.

Canis nehringi (N = 1). MACN-PV: 500.

Cerdocyon thous (N = 109). CFA: 3697; 3875; 4265; 4419; 4496; 4511; 4512; 4661; 4663; 4664; 4717; 5048; 5197; 5278; 5283; 5313; 5375; 6000; 6071; 6128; 6129. CML: 588; 3719; 3756; 3827; 4083; 4083; 4692; 5964; 5966; 5967; 6213; 6214; 6340. MACN: 4.213; 20.32; 24.85; 24.127; 25.119; 25.159; 29.839; 30.344; 30.345; 32.261; 32.262; 32.75; 33.6; 34.676; 36.191; 36.481; 39.460; 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; 49.221; 49.367; 50.40; 50.43; 50.45; 50.57; 50.59; 50.60; 50.61; 50.62; 50.63; 50.64; 52.54; 52.63; 52.64; 13051; 14,322; 14681; 15741; 16189; 20316; 20454; 20456; 20815; 20816; 20817; 21228; 23180; 23669; 23670; 23726; 23727; 24045; 24046; 24207; 24208. MFA-ZV: 228; 1204. MLP: 20.IX.49.13; 16.X.01.7; 31.XII.02.77; 1322. MZUSP: 9687.

Chrysocyon brachyurus (N = 82). AMNH: 36962; 71179; 120999; 133940; 133941; 135274. CFA: 12826; 12827. CML: 1376; 6133; 6352. FMNH: 28311; 28312; 28313; 44534; 46003; 54406; 96003; 101848; 125401; 127434; 134483; 137425; 150739. MACN: 3.71; 3.73; 4.32; 4.303; 24.4; 30.29; 30.231; 53.49; 13466; 19146; 20646; 23456; 23984; 24043; 24201. MFA-ZV 517; 524; 581; 651; 652; 919; 1166. MLP: 2.IV.02.4; 5.X.99.1; 31.XII.02.88; 6; 92; 564; 695; 1684; 1686. MZUSP: 525; 3025; 3338; 9420; 19733; 19736; 29870; 31981; 32039; 32042; 32043; 32056; 32199; 32505; 32629. NMNH: 196975; 258614; 261022; 261023; 270371; 271567; 314863; 521007; 534807; 534970; 588,223; 588425.

Lycalopex culpaeus (N = 107). CFA: 2129; 6451. CML: 5067; 5068; 5069; 5070; 5071; 5970; 5974; 6343; 6344. LIEB: 791; 793. MACN: 3.68; 4.41; 7.42; 24.119; 25.128; 27.131; 30.69; 31.58; 31.59; 33.67; 33.68; 33.69; 38.39; 41.55; 15024; 15033; 15037; 15040; 15044; 15045; 15049; 15050; 15055; 15062; 15063; 15064; 15073; 15078; 15081; 15082; 15083; 15089; 15093; 15096; 15101; 15106; 15112; 15119; 15121; 15124; 15127; 15138; 15140; 15149; 15151; 15154; 15158; 15163; 15168; 15172; 15173; 15177; 15181; 15882; 15190; 15194; 15196; 15208; 15212; 15220; 15223; 15224; 15226; 15227; 15228; 15229; 15232; 15233; 15240; 15243; 15246; 15248; 19221; 19222; 20813; 21899; 23072; 23076; 23077; 23093; 23095; 23103; 23108; 23119; 23123; 23125; 23148; 23719; 23720; 23721; 23,915; 24210. MLP: 1264; 1266.

Lycalopex fulvipes (N = 2). FMNH: 23814; 23815.

Lycalopex griseus (N = 127). AMNH: 17440a; 17440b; 17441a. CFA: 2175; 4197; 5291; 5649; 5650; 5777; 5782; 10243. CML: 837; 838; 1177; 1178; 1427; 1489; 3714; 4967; 6189; 6190; 6192. FMNH: 154639; 154640. LIEB: 794; 809. MACN: 4.253; 23.20; 24.50; 24.52; 24.53; 24.54; 24.56; 24.57; 24.59; 24.62; 24.63; 24.64; 24.66; 24.68; 24.69; 24.71; 24.74; 24.75; 24.76; 24.79; 24.80; 24.81; 223; 225; 226; 13781; 14540; 14902; 15020; 15185; 15186; 15187; 15189; 15262; 15263; 15264; 15265; 15269; 16321; 16322; 16325; 20205; 20206; 20207; 20208; 20276; 20277; 20278; 20814; 20829; 23150; 23468; 23662; 23,663; 2664; 23668; 23718; 23728; 23729; 23730; 23910; 24206; 29.895; 50.419; 50.420; 50.432; 50.490; 51.170. MLP: 5.III.36.12; 5.III.36.27; 2.IV.60.1; 4.VIII.98.4; 240; 441; 559; 696; 701; 712. NMNH: 92139; 92140; 92141; 92142; 92143; 92144; 92145; 92146; 92147; 92149; 92150; 92151; 92152; 92169; 92173; 92174; 92175; 92176; 92177; 92178; 92179; 482163; 482164.

Lycalopex gymnocercus (N = 355). AMNH: 41502; 41503; 41504; 41505; 41506; 41507; 41508; 41509; 41510. CFA: 3255; 3698; 3962; 4256; 4406; 4416; 4417; 4659; 8312; 8313; 8588; 8589; 8590; 8591; 10887; 11062; 11063. CML: 192; 495; 545; 645; 834; 836; 895; 908; 909; 959; 1179; 1526; 1526; 3072; 4081; 4082; 5143; 5473; 5474; 5479; 5480; 5772; 6342. GECM: 24; 34; 40; 51; 57; 65; 67; 75; 76; 85; 100; 108; 112; 119; 121; 129; 139; 149; 152; 153; 179; 217Bis; 220Bis; 227Bis. MACN: 4.271; 20.33; 26.28; 20.35; 23.33; 23.34; 23.36; 23.37; 23.38; 24.48; 24.49; 24.133; 24.134; 24.140; 24.141; 24.142; 24.143; 24.144; 24.145; 24.146; 24.147; 24.148; 24.149; 24.151; 24.152; 24.154; 24.156; 24.162; 24.169; 24.170; 26.129; 26.162; 26.163; 27.53; 28.182; 29.35; 30.150; 30.210; 30.211; 30.212; 32.252; 32.263; 33.177; 33.266; 33.268; 34.317; 35.241; 36.178; 36.479; 36.480; 37.82; 38.243; 39.191; 39.194; 41.220; 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; 51.81; 53.2; 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; 1766; 157769; 15771; 15783; 15784; 15785; 15787; 15788; 15791; 15792; 15794; 15795; 15796; 15797; 15800; 15818; 15820; 15831; 15833; 15834; 15838; 15854; 15859; 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; 15958; 15963; 15964; 15966; 15970; 15973; 15979; 15981; 15982; 15986; 15987; 15992; 15998; 15999; 16000; 16001; 16006; 16009; 16010; 16013; 16014; 16015; 16024; 16025; 16026; 16027; 16030; 16031; 16032; 16035; 16036; 16037; 16038; 16039; 16040; 16041; 16046; 16047; 16048; 16049; 16050; 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; 23920; 24203; 24204; 24205; 24208; 24209; 24259; 24265; 24282. MLP: 16.III.99.16; 13.IV.99.3; 13.IV.99.13; 13.IV.99.14; 13.IV.99.36; 26.V.95.9; 4.VIII.98.9; 30.XII.02.65; 710. NMNH: 172789; 172790; 236366; 331065.

Lycalopex sechurae (N = 35). AMNH: 100091; 100100; 133926; 133927; 133928; 133929; 133937; 2091; 349; 36457; 391; 46525; 46526; 46527; 46528; 46529; 46530; 46531; 46532; 46533; 63709; 70091. FMNH: 19971; 19972; 20747; 53911; 80953; 80954; 80955; 80956; 80957; 80958; 80959; 80960; 80961; 80962; 80963; 80964; 80965; 80966; 80967; 80968; 80969.

Lycalopex vetulus (N = 31). MLP: 1258. MZUSP: 1011; 1012; 1014; 1015; 1016; 1018; 1075; 1076; 1084; 12040; 13611; 3046; 3047; 3047; 3048; 3049; 3050; 825. NMNH 121171; 121172; 181150; 545109.

Speothos venaticus (N = 34). AMNH: 136285; 167846; 175306; 184688; 37472; 76035; 76805; 76806; 98558; 98559; 98560; 98640. FMNH: 121544; 125402; 60290; 87861. MACN: 50.67; 16510. MZUSP:19743; 19744. NMNH: 253504; 270165; 270171; 270368; 270369; 270370; 307650; 314048; 395841; 398030; 521045; 538307; 544414; 582465.

Urocyon cinereoargenteus (N = 37). AMNH: 255645; 255648; 254470; 8197; 243449; 100301; 243095; 120989; 184105; 184122; 184012; 183939; 184002; 184065; 183979; 184098; 184094; 184077; 184091; 184126; 184083; 184121; 184014; 184087; 184013; 184009; 183991; 183956; 183942; 183943; 183960; 183953; 183995; 183954; 185512; 184064; 184007.

Vulpes lagopus (N = 1). MACN: 4.1.

Vulpes vulpes (N = 54). FMNH: 106726; 107271; 140172; 140176; 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; 89710; 89712; 89963; 90361; 90473; 90474; 91605; 91725; 91726; 91731; 91741; 92727; 95863; 95865; 95867; 95870; 95872; 95873; 98733; 98734; 98735; 98736.

Vulpes zerda (N = 2). CML: 3731. MACN: 3.14.

Theriodictis platensis (N = 1). MLP-PV: 96-IX-1-1.

Otocyon megalotis (N = 1). MACN: 26.115.

Lycaon pictus (N = 1). MACN: 38.249.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Segura, V., Cassini, G.H., Prevosti, F.J. et al. Integration or Modularity in the Mandible of Canids (Carnivora: Canidae): a Geometric Morphometric Approach. J Mammal Evol 28, 145–157 (2021). https://doi.org/10.1007/s10914-020-09502-z

Download citation

Keywords

  • Carnivora
  • Canidae
  • Mandible
  • Integration
  • Modularity