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Stabbing Slinkers: Tusk Evolution Among Artiodactyls

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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.

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References

  • 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 116:329–338

    Google Scholar 

  • Arnold C, Matthews LJ, Nunn CL (2010) The 10kTrees website: a new online resource for primate phylogeny. Evol Anthropol 19:114–118

    Google Scholar 

  • Barrette C (1977) Fighting behavior of muntjac and the evolution of antlers. Evolution 31:169–176

    PubMed  Google Scholar 

  • 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 

  • Bro-Jørgensen J (2007) The intensity of sexual selection predicts weapon size in male bovids. Evolution 61:1316–1326

    PubMed  Google Scholar 

  • Bro-Jørgensen J (2008) Dense habitats selecting for small body size: a comparative study on bovids. Oikos 117:729–737

    Google Scholar 

  • Caro TM (2005) Antipredator Defenses in Birds and Mammals. University of Chicago Press, Chicago

  • Caro TM, Graham CM, Stoner CJ, Flores MM (2003) Correlates of horn and antler shape in bovids and cervids. Behav Ecol Sociobiol 55:32–41

    Google Scholar 

  • Clutton-Brock TH, Albon SD, Harvey PH (1980) Antlers, body size and breeding group size in the Cervidae. Nature 285:565–567

    Google Scholar 

  • 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

    Google Scholar 

  • Dubost G, Terrade R (1970) La transformation de la peau des Tragulidae en bouclier protecteur. Mammalia 34:505–513

  • Emlen DJ (2008) The evolution of animal weapons. Annu Rev Ecol Evol Syst 39:387–413

    Google Scholar 

  • 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 59–94

  • 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 166–205

  • Estes RD (1991a) The Behavior Guide to African Mammals Vol 64. University of California Press, Berkeley

  • Estes RD (1991b) The significance of horns and other male secondary sexual characters in female bovids. Appl Anim Behav Sci 29:403–451

    Google Scholar 

  • Geist V (1966) The evolution of horn-like organs. Behaviour 27:175–214

    Google Scholar 

  • 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): 285–315

    Google Scholar 

  • Geist V (1974) On the relationship of social evolution and ecology in ungulates. Am Zool 14:205–220

    Google Scholar 

  • Geist V (1998) Deer of the World: Their Evolution, Behavior, and Ecology. Stackpole Books, Mechanicsburg

  • Gentry AW (1994) The Miocene differentiation of Old World Pecora (Mammalia). Hist Biol 7:2 115–158

    Google Scholar 

  • Gittleman JL, Van Valkenburgh B (1997) Sexual dimorphism in the canines and skulls of carnivores: effects of size, phylogency, and behavioural ecology. J Zool 242:97–117

    Google Scholar 

  • Goss RJ (2012) Deer Antlers: Regeneration, Function and Evolution. Academic Press, New York

  • 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 244–281

  • Harris JM, Li-Ping L (2007) Superfamily Suoidea. In: Prothero DR, Foss SE (eds) The Evolution of Artiodactyls. Johns Hopkins University Press, Baltimore, pp 130–150

  • Herring SW (1972) The role of canine morphology in the evolutionary divergence of pigs and peccaries. J Mammal 53:500–512

    Google Scholar 

  • IUCN (2017) The IUCN Red List of Threatened Species. IUCN Global Species Programme Red List Unit. http://www.iucnredlist.org. Accessed 6 April 2017

  • Janis CM (1982) Evolution of horns in ungulates: ecology and paleoecology. Biol Rev 57:261–318

    Google Scholar 

  • 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 241–259

  • Janis CM, Scott KM (1987) The interrelationships of higher ruminant families with special emphasis on the members of the Cervoidea. Am Mus Novitates 2893:1–85

  • Jarman PJ (1974) The social organization of antelope in relation to their ecology. Behaviour 48: 215–67

    Google Scholar 

  • 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

    Google Scholar 

  • Lundrigan B (1996) Morphology of horns and fighting behavior in the family Bovidae. J Mammal 77:462–475

    Google Scholar 

  • MacKinnon J (1981) The structure and function to the tusks of babirusa. Mammal Rev 11:37–40

    Google Scholar 

  • McCullough EL, Miller CW, Emlen DJ (2016) Why sexually selected weapons are not ornaments. Trends Ecol Evol 31:742–751

    Google Scholar 

  • Métais G, Vislobokova I (2007) Basal ruminants. In: Prothero DR, Foss SE (eds) The Evolution of Artiodactyls. Johns Hopkins University Press, Baltimore, pp 189–212

  • Nowak RM (1999) Walker’s Mammals of the World. Johns Hopkins University Press, Baltimore

  • 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

  • Packer C (1983) Sexual dimorphism: the horns of African antelopes. Science 221:1191–1193

    CAS  PubMed  Google Scholar 

  • Prothero DR (2007) Family Moschidae. In: Prothero DR, Foss SE (eds) The Evolution of Artiodactyls. Johns Hopkins University Press, Baltimore, pp 221–226

  • Prothero DR (2017) The Princeton Field Guide to Prehistoric Mammals. Princeton University Press, Princeton

  • R Core Team (2012) R: A language and environment for statistical computing (Ver. 2.14.12). R Foundation for Statistical Computing, Vienna.

  • 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 186:165–175

    PubMed  Google Scholar 

  • Ralls K, Barasch C, Minkowski K (1975) Behavior of captive mouse deer, Tragulus napu. Z Tierpsychol 37:356–378

    Google Scholar 

  • Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223

    Google Scholar 

  • Rico-Guevara A, Hurme KJ (2018) Intrasexually selected weapons. Biol Rev. https://doi.org/10.1111/brv.12436

    Google Scholar 

  • Rössner GE (2007) Family Tragulidae. In: Prothero DR, Foss SE (eds) The Evolution of Artiodactyls. Johns Hopkins University Press, Baltimore, pp 213–220

  • Sánchez IM, Domingo MS, Morales J (2010) The genus Hispanomeryx (Mammalia, Ruminantia, Moschidae) and its bearing on musk deer phylogeny and systematics. Palaeontology 53:1023–1047

    Google Scholar 

  • Sathyakumar S (1992) The musk deer. Sanctuary Asia 12:52–57

  • 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: 3403

    Google Scholar 

  • Stankowich T (2012) Armed and dangerous: predicting the presence and function of defensive weaponry in mammals. Adaptive Behavior 20:32–43

    Google Scholar 

  • Stankowich T, Caro T (2009) Evolution of weaponry in female bovids. Proc R Soc B 276:4329–4334

    PubMed  Google Scholar 

  • Stankowich T, Haverkamp PJ, Caro T (2014) Ecological drivers of antipredator defense in carnivores. Evolution 68:1415–1425

    PubMed  Google Scholar 

  • UMMZ (2015) Animal Diversity Web. University of Michigan Museum of Zoology. http://animaldiversity.ummz.umich.edu/site/index.html. Accessed 6 April 2017

  • 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 32–58

  • Ungar PS (2010) Mammal Teeth: Origin, Evolution, and Diversity. Johns Hopkins University Presss, Baltimore

  • Wilson DE, Mittermeier RA (2011) Handbook of the Mammals of the World. Vol. 2. Hoofed Mammals. Lynx Edicions, Barcelona

  • Yahner RH (1980) Barking in a primitive ungulate, Muntiacus reevesi: function and adaptiveness. Am Nat 114:157–177

    Google Scholar 

  • Zhang BL, Dang FM, Li BS (1970) The Farming of Musk Deer. Agricultural Publishing Company, Peking

Download references

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.

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Correspondence to Theodore Stankowich.

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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.

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The authors declare that they have no conflict of interest.

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Significance Statement

While the function and evolution of tusks in elephants, walruses, and even narwhals have received a great deal of scientific and public attention, we know little about what drives the evolution and maintenance of tusks in several groups of artiodactyls (e.g., pigs, muntjac, musk deer). Most male artiodactyls have some sort of sexual weapon (e.g., antlers, horns, tusks), but we don’t know what ecological factors promote the evolution of tusks in some and cranial weapons in others. Using a comparative approach, we show that living a slinking, solitary lifestyle in dense, closed habitats where long range communication during sexual combat is not possible favors the evolution of sharp, dagger-like tusks for combat during territorial disputes. We discuss the sexual benefits of tusks over antlers considering species ecology.

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Cabrera, D., Stankowich, T. Stabbing Slinkers: Tusk Evolution Among Artiodactyls. J Mammal Evol 27, 265–272 (2020). https://doi.org/10.1007/s10914-018-9453-x

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