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Stabbing Slinkers: Tusk Evolution Among Artiodactyls

  • Doreen Cabrera
  • Theodore Stankowich
Original Paper

Abstract

Combat weaponry, including elaborate horns and antlers and complex dentition, evolved independently several times among mammals. While it is evident that tusk and tusk-like dentition have emerged primarily among males for intrasexual combat, it is unclear what ecological factors favor the retention or re-evolution of tusks. We investigated patterns of tusk evolution in artiodactyls while exploring specific ecological factors that might favor their use over other cranial weapons (e.g., antlers, horns). We show that among males, small (<15 kg), solitary species tend to retain well-developed canines, and more solitary species live in more closed habitats. These results suggest that tusks are a better weapon option for smaller, slinking artiodactyls in forested environments with low visibility, whereas larger taxa living in more open environment can bear the cost of elaborate headgear and are better served by communicating across distances an honest signal of fighting ability. Small species in dense habitats may also be more likely to be ambushed by predators and have a need to defend themselves; small, slicing daggers may be a better defensive weapon and allow more maneuverability and faster escape than cumbersome headgear in densely vegetated habitats.

Keywords

Tusks Canines Weapons Defense Deer 

Notes

Acknowledgments

We thank James Dines and David Janiger at the Los Angeles County Museum of Natural History, and curators at the American Museum of Natural History and the National Museum of Natural History at the Smithsonian Institution for access to their collections and support. We thank members of the Stankowich Lab at California State University Long Beach and two anonymous reviewers for comments on previous versions of this manuscript.

Compliance with Ethical Standards

This research was supported by funds from California State University Long Beach, College of Natural Sciences and Mathematics. For this type of study formal consent is not required. This article does not contain any studies with human participants or animals performed by any of the authors; all subjects were previously collected specimens deposited in museum collections.

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

10914_2018_9453_MOESM1_ESM.xlsx (495 kb)
ESM 1 (XLSX 494 kb)

References

  1. Aitchison J (1946) Hinged teeth in mammals: a study of the tusks of muntjacs (Muntiacus) and Chinese water deer (Hydropotes inermis). Proc Zool Soc Lond 116:329–338Google Scholar
  2. Arnold C, Matthews LJ, Nunn CL (2010) The 10kTrees website: a new online resource for primate phylogeny. Evol Anthropol 19:114–118Google Scholar
  3. Barrette C (1977) Fighting behavior of muntjac and the evolution of antlers. Evolution 31:169–176Google Scholar
  4. Brashares JS, Garland T, Arcese P (2000) Phylogenetic analysis of coadaptation in behavior, diet, and body size in the African antelope. Behav Ecol 11(4): 452–63.Google Scholar
  5. Bro-Jørgensen J (2007) The intensity of sexual selection predicts weapon size in male bovids. Evolution 61:1316–1326Google Scholar
  6. Bro-Jørgensen J (2008) Dense habitats selecting for small body size: a comparative study on bovids. Oikos 117:729–737Google Scholar
  7. Caro TM (2005) Antipredator Defenses in Birds and Mammals. University of Chicago Press, ChicagoGoogle Scholar
  8. Caro TM, Graham CM, Stoner CJ, Flores MM (2003) Correlates of horn and antler shape in bovids and cervids. Behav Ecol Sociobiol 55:32–41Google Scholar
  9. Clutton-Brock TH, Albon SD, Harvey PH (1980) Antlers, body size and breeding group size in the Cervidae. Nature 285:565–567Google Scholar
  10. Dubost G (1975) Le comportement du Chevrotain africain, Hyemoschus aquaticus Ogilby (Artiodactyla, Ruminantia). Z Tierpsychol 37(4):403–448.  https://doi.org/10.1111/j.1439-0310.1975.tb00889.x
  11. Dubost G, Terrade R (1970) La transformation de la peau des Tragulidae en bouclier protecteur. Mammalia 34:505–513Google Scholar
  12. Emlen DJ (2008) The evolution of animal weapons. Annu Rev Ecol Evol Syst 39:387–413Google Scholar
  13. Erfurt J, Métais G (2007) Endemic European Paleogene artiodactyls: Cebochoeridae, Choeropotamidae, Mixtotheriidae, Cainotheriidae, Anoplotheriidae, Xiphodontidae, and Amphimerycidae. In: Prothero DR, Foss SE (eds) The Evolution of Artiodactyls. Johns Hopkins University Press, Baltimore, pp 59–94Google Scholar
  14. Estes RD (1974) Social organization of the African Bovidae. In: Geist V, Walther F (eds) The Behaviour of Ungulates and Its Relation to Management. IUCN Morges, Switzerland, pp 166–205Google Scholar
  15. Estes RD (1991a) The Behavior Guide to African Mammals Vol 64. University of California Press, BerkeleyGoogle Scholar
  16. Estes RD (1991b) The significance of horns and other male secondary sexual characters in female bovids. Appl Anim Behav Sci 29:403–451Google Scholar
  17. Geist V (1966) The evolution of horn-like organs. Behaviour 27:175–214Google Scholar
  18. Geist V (1971) The relation of social evolution and dispersal in ungulates during the Pleistocene, with emphasis on the Old World deer and the genus Bison. Quaternary Res 1(3): 285–315Google Scholar
  19. Geist V (1974) On the relationship of social evolution and ecology in ungulates. Am Zool 14:205–220Google Scholar
  20. Geist V (1998) Deer of the World: Their Evolution, Behavior, and Ecology. Stackpole Books, MechanicsburgGoogle Scholar
  21. Gentry AW (1994) The Miocene differentiation of Old World Pecora (Mammalia). Hist Biol 7:2 115–158Google Scholar
  22. Gittleman JL, Van Valkenburgh B (1997) Sexual dimorphism in the canines and skulls of carnivores: effects of size, phylogency, and behavioural ecology. J Zool 242:97–117Google Scholar
  23. Goss RJ (2012) Deer Antlers: Regeneration, Function and Evolution. Academic Press, New YorkGoogle Scholar
  24. Gosling LM (1986) The evolution of mating strategies in male antelopes. In: Rubenstein DI, Wrangham RW (eds) Ecological Aspects of Social Evolution. Princeton University Press, Princeton, pp 244–281Google Scholar
  25. Harris JM, Li-Ping L (2007) Superfamily Suoidea. In: Prothero DR, Foss SE (eds) The Evolution of Artiodactyls. Johns Hopkins University Press, Baltimore, pp 130–150Google Scholar
  26. Herring SW (1972) The role of canine morphology in the evolutionary divergence of pigs and peccaries. J Mammal 53:500–512Google Scholar
  27. IUCN (2017) The IUCN Red List of Threatened Species. IUCN Global Species Programme Red List Unit. http://www.iucnredlist.org. Accessed 6 April 2017
  28. Janis CM (1982) Evolution of horns in ungulates: ecology and paleoecology. Biol Rev 57:261–318Google Scholar
  29. Janis CM (1990) The correlation between diet and dental wear in herbivorous mammals, and its relationship to the determination of diets of extinct species. In: Boucot AJ (ed) Evolutionary Paleobiology of Behaviour and Coevolution. Elsevier, Amsterdam, Toronto, pp 241–259Google Scholar
  30. Janis CM, Scott KM (1987) The interrelationships of higher ruminant families with special emphasis on the members of the Cervoidea. Am Mus Novitates 2893:1–85Google Scholar
  31. Jarman PJ (1974) The social organization of antelope in relation to their ecology. Behaviour 48: 215–67Google Scholar
  32. Jarman PJ (1989) On being thick-skinned: dermal shields in large mammalian herbivores. Biol J Linn Soc 36(1–2):169–191.  https://doi.org/10.1111/j.1095-8312.1989.tb00489.x
  33. Lundrigan B (1996) Morphology of horns and fighting behavior in the family Bovidae. J Mammal 77:462–475Google Scholar
  34. MacKinnon J (1981) The structure and function to the tusks of babirusa. Mammal Rev 11:37–40Google Scholar
  35. McCullough EL, Miller CW, Emlen DJ (2016) Why sexually selected weapons are not ornaments. Trends Ecol Evol 31:742–751Google Scholar
  36. Métais G, Vislobokova I (2007) Basal ruminants. In: Prothero DR, Foss SE (eds) The Evolution of Artiodactyls. Johns Hopkins University Press, Baltimore, pp 189–212Google Scholar
  37. Nowak RM (1999) Walker’s Mammals of the World. Johns Hopkins University Press, BaltimoreGoogle Scholar
  38. Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W (2012) caper: comparative analysis of phylogenetics and evolution in R. R package version 0.5. http://CRAN.R-project.org/package=caper
  39. Packer C (1983) Sexual dimorphism: the horns of African antelopes. Science 221:1191–1193Google Scholar
  40. Prothero DR (2007) Family Moschidae. In: Prothero DR, Foss SE (eds) The Evolution of Artiodactyls. Johns Hopkins University Press, Baltimore, pp 221–226Google Scholar
  41. Prothero DR (2017) The Princeton Field Guide to Prehistoric Mammals. Princeton University Press, PrincetonGoogle Scholar
  42. R Core Team (2012) R: A language and environment for statistical computing (Ver. 2.14.12). R Foundation for Statistical Computing, Vienna.Google Scholar
  43. Raia P, Passaro F, Carotenuto F, Maiorino L, Piras P, Teresi L, Meiri S, Itescu Y, Novosolov M, Baiano MA, Martínez R, Fortelius M (2015) Cope's rule and the universal scaling law of ornament complexity. Am Nat 186:165–175Google Scholar
  44. Ralls K, Barasch C, Minkowski K (1975) Behavior of captive mouse deer, Tragulus napu. Z Tierpsychol 37:356–378Google Scholar
  45. Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223Google Scholar
  46. Rico-Guevara A, Hurme KJ (2018) Intrasexually selected weapons. Biol Rev.  https://doi.org/10.1111/brv.12436
  47. Rössner GE (2007) Family Tragulidae. In: Prothero DR, Foss SE (eds) The Evolution of Artiodactyls. Johns Hopkins University Press, Baltimore, pp 213–220Google Scholar
  48. Sánchez IM, Domingo MS, Morales J (2010) The genus Hispanomeryx (Mammalia, Ruminantia, Moschidae) and its bearing on musk deer phylogeny and systematics. Palaeontology 53:1023–1047Google Scholar
  49. Sathyakumar S (1992) The musk deer. Sanctuary Asia 12:52–57Google Scholar
  50. Smith FA, Lyons SK, Ernest SKM, Jones KE, Kaufman DM, Dayan T, Marquet PA, Brown JH, Haskell JP (2003) Body mass of late Quaternary mammals. Ecology 84: 3403Google Scholar
  51. Stankowich T (2012) Armed and dangerous: predicting the presence and function of defensive weaponry in mammals. Adaptive Behavior 20:32–43Google Scholar
  52. Stankowich T, Caro T (2009) Evolution of weaponry in female bovids. Proc R Soc B 276:4329–4334Google Scholar
  53. Stankowich T, Haverkamp PJ, Caro T (2014) Ecological drivers of antipredator defense in carnivores. Evolution 68:1415–1425Google Scholar
  54. UMMZ (2015) Animal Diversity Web. University of Michigan Museum of Zoology. http://animaldiversity.ummz.umich.edu/site/index.html. Accessed 6 April 2017
  55. Theodor JM, Erfurt J, Métais G (2007) The earliest artiodactyls: Diacodexeidae, Dichobunidae, Homacodontidae, Leptochoeridae, and Raoellidae. In: Prothero DR, Foss SE (eds) The Evolution of Artiodactyls. Johns Hopkins University Press, Baltimore, pp 32–58Google Scholar
  56. Ungar PS (2010) Mammal Teeth: Origin, Evolution, and Diversity. Johns Hopkins University Presss, BaltimoreGoogle Scholar
  57. Wilson DE, Mittermeier RA (2011) Handbook of the Mammals of the World. Vol. 2. Hoofed Mammals. Lynx Edicions, BarcelonaGoogle Scholar
  58. Yahner RH (1980) Barking in a primitive ungulate, Muntiacus reevesi: function and adaptiveness. Am Nat 114:157–177Google Scholar
  59. Zhang BL, Dang FM, Li BS (1970) The Farming of Musk Deer. Agricultural Publishing Company, PekingGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesCalifornia State UniversityLong BeachUSA

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