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Sexual Dimorphism and Inter-Generic Variation in Proboscidean Tusks: Multivariate Assessment of American Mastodons (Mammut americanum) and Extant African Elephants

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Abstract

Characteristics of social structure, mating strategies, and parental investment can be inferred for mammalian species based on degree of sexual dimorphism, especially when males are substantially larger than females. American mastodons (Mammut americanum) and extant African elephants (Loxodonta africana, Loxodonta cyclotis) both exhibit marked dimorphism in tusk size. To evaluate the hypothesis that this dimorphism might be indicative of similar, and possibly conserved, behavioral patterns in each lineage, we undertook a detailed evaluation of the pattern of tusk growth in these two genera. Separate discriminant function analyses (DFA) of 21 adult mastodon tusks of inferred sex and 48 adult elephant tusks of known sex show that patterns of ontogenetic change in tusk circumference, regardless of genus, effectively discriminate between sexes. Canonical variates analysis (CVA) of tusks from male and female mastodons and male and female elephants shows that male tusks in both genera are larger than female tusks across all measurements, especially for maximum tusk circumference and pulp cavity depth. CVA’s emphasis of inter-group differences in tusk morphology also shows that mastodon tusks are more robust than elephant tusks. Overall, this study illustrates that there is a characteristic male and a characteristic female tusk form shared by elephants and mastodons. This shows that elephants and mastodons display a shared syndrome of traits beyond sex-linked differences in tusk size, supporting the hypothesis that mastodons exhibited behaviors similar to those we observe today in African elephants.

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References

  • Allen JA (1877) The influence of physical conditions in the genesis of species. Radical Rev 1:108-140

    Google Scholar 

  • Averianov AO (1996) Sexual dimorphism in the mammoth skull, teeth, and long bones. In: Shoshani J, Tassy P (eds) The Proboscidea: Evolution and Palaeoecology of Elephants and their Relatives. Oxford University Press, Oxford, pp 260-267

    Google Scholar 

  • Badyaev AV (2002) Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecol Evol 17(8):369-378

    Article  Google Scholar 

  • Berger J, Dulamtseren S, Calin S, Enkkhbileg D, Lichtman P, Namshir S, Wingard G, Reading R (2001) Back-casing sociality in extinct species: new perspectives using mass death assemblages and sex ratios. Proc R Soc Lond B 268(1463):131-139

    Article  CAS  Google Scholar 

  • Bininda-Edmonds OR, Gittleman JL, Purvis A (1999) Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biol Rev 74:143-175

    Article  Google Scholar 

  • Campbell NA, Atchley WR (1981) The geometry of canonical variates analysis. Syst Zool 30(3):268-280

    Article  Google Scholar 

  • Cerling TC, Harris JM, Leakey MG (1999) Browsing and grazing in elephants: the isotope record of modern and fossils proboscideans. Oecologia 120:364-374

    Article  Google Scholar 

  • Charnov EL, Schaffer WM (1973) Life-history consequences of natural selection: Cole’s result revisited. Am Nat 107:791-793

    Article  Google Scholar 

  • Clutton-Brock TH (1994) The costs of sex. In: Short RV, Balaban E (eds) The Differences Between the Sexes. Cambridge University Press, Cambridge, pp 347-362

    Google Scholar 

  • Darwin CR (1871) The Descent of Man, and Selection in Relation to Sex. Appleton, New York

    Google Scholar 

  • Debruyne R (2005) A case study of apparent conflict between molecular phylogenies: the interrelationships of African elephants. Cladistics 21:31–50

    Google Scholar 

  • Eberhardt LL (2002) A paradigm for population analysis of long-lived vertebrates. Ecology 83:2841-2854

    Article  Google Scholar 

  • Eisenberg JL, McKay GM, Jainudeen MR (1971) Reproductive behavior of the Asiatic elephant (Elephas maximus maximus L.). Behaviour 38:193-225

    Article  CAS  PubMed  Google Scholar 

  • Elder WH (1970) Morphometry of elephant tusks. Zool Afr 5:43-159

    Google Scholar 

  • Fisher DC (1990) Age, sex, and season of death of the Grandville mastodon. Mich Archaeol 36:141-160

    Google Scholar 

  • _____ (1996) Extinction of proboscideans in North America. In: Shoshani J, Tassy P (eds) The Proboscidea: Evolution and Palaeoecology of Elephants and their Relatives. Oxford University Press, Oxford, pp 121-135

    Google Scholar 

  • _____ (2008) Taphonomic analysis of the Hyde Park mastodon. In: Allmon WD, Nester PL, Chiment JJ (eds) Mastodon Paleobiology, Taphonomy, and Paleoenvironment in the Late Pleistocene of New York State: Studies on the Hyde Park, Chemung, and Java Sites. Palaeontographica Americana 61:197-290

  • _____ (2009) Paleobiology and extinction of proboscideans in the Great Lakes region of North America. In: Haynes G (ed) American Megafaunal Extinctions at the End of the Pleistocene. Springer Science, New York, pp 55-75

    Chapter  Google Scholar 

  • Fisher DC, Beld SG, Rountrey AN (2008) Tusk record of the North Java mastodon. In: Allmon WD, Nester PL, Chiment JJ (eds) Mastodon Paleobiology, Taphonomy, and Paleoenvironment in the Late Pleistocene of New York State: Studies on the Hyde Park, Chemung, and Java Sites. Palaeontographica Americana 61:417-463

  • Fisher DC, Fox DL (2003) Season of death and terminal growth histories of Hiscock mastodons. In: Laub RS (ed) The Hiscock Site: Late Pleistocene and Holocene Paleoecology and Archaeology of Western New York State. Bull Buffalo Soc of Nat Sci 37:83-101

  • _____ (2007) Life history and unilateral loss of molar function in the Cohoes mastodon: a case study in nutritional stress? J Vertebr Paleontol 27 (Suppl to 3):74A-75A

  • Gheerbrant E, Sudre J, Tassy P, Amaghzaz M, Bouya B, Iarochene M (2005) Nouvelles données sur Phosphatherium escuilliei (Mammalia, Proboscidea) de l’Éocène inférieur du Maroc, apports à la phylogénie des Proboscidea et des ongulés lophodontes. Geodiversitas 27(2):239-333

    Google Scholar 

  • Gheerbrant E, Tassy P (2009) L’origine et l’évolution des éléphants. CR Paleovol 8:281-294

    Article  Google Scholar 

  • Gingerich PD (1981) Variation, sexual dimorphism, and social structure in the early Eocene horse Hyracotherium. Paleobiology 7(4):443-455

    Google Scholar 

  • _____ (2000) Arithmetic or geometric normality of biological variation: an empirical test of theory. J Theor Biol 204:201-221

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Groves CP, Grubb P (2000) Do Loxodonta cyclotis and L. africana interbreed? Elephant 2(4):3-4

    Google Scholar 

  • Grubb P, Groves CP, Dudley JP, Shoshani J (2000) Living African elephants belong to two species: Loxodonta africana (Blumenbach, 1797) and Loxodonta cyclotis (Matschie, 1900). Elephant 2(4):1-3

    Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics software package for education and data analysis. Palaeontol Electron 4:1-9

    Google Scholar 

  • Hanks J (1972) Growth of the African elephant (Loxodonta africana). East Afr Wildl J 10:251-272

    Article  Google Scholar 

  • Haynes G (1991) Mammoths, Mastodonts, and Elephants: Biology, Behavior, and the Fossil Record. Cambridge University Press, Cambridge

    Google Scholar 

  • Holman JA, Fisher DC, Kapp RO (1986) Recent discoveries of fossil vertebrates in the lower peninsula of Michigan. Michigan Academician 28:431–463

    Google Scholar 

  • Huttunen K, Goelich UB (2002) A partial skeleton of Prodeinotherium bavaricum (Proboscidea, Mammalia) from the middle Miocene of Unterzolling (Upper Freshwater Molasse, Germany). Geobios 35:489–514

    Article  Google Scholar 

  • Johnson MB, Clifford SL, Goossens B, Nyakanna S, Curran B, White LJT, Wickings EJ, Bruford MW (2007) Complex phylogeographic history of central African forest elephants and its implications for taxonomy. BMC Evol Biol 7:244–257

    Google Scholar 

  • Jones ME, Cockburn AA, Hamede R, Hawkins C, Heserman H, Lachich S, Mann D, McCallum H, Pemberton D (2008) Life-history change in disease-ravaged Tasmanian devil populations. Proc Natl Acad Sci USA 105:10023-10027

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Joshi R, Singh R, Pushola R, Negi MS (2009) Reproductive behaviour of wild Asian Elephants Elephas maximus in the Rajaji National Park, North-West India. Researcher 1:76-84

    Google Scholar 

  • Koch PL, Tuross N, Fogel ML (1997) The effects of sample treatment and diagenesis on the isotopic integrity of carbonate in biogenic hydroxylapatite. J Archaeol Sci 24:417-429

    Article  Google Scholar 

  • Lee PC, Moss CJ (1986) Early maternal investment in male and female African elephant calves. Behav Ecol Sociobiol 18:353-361

    Article  Google Scholar 

  • ____ (1995) Statural growth in known-age African elephants (Loxodonta africana). J Zool 236:29-41

    Google Scholar 

  • ____ (1999) The social context for learning and behavioural development among wild African elephants. In: Box HO, Gibson KR (eds) Mammalian Social Learning. Cambridge University Press, Cambridge, pp 102-125

  • Lister A (1996) Sexual dimorphism in the mammoth pelvis: an aid to gender determination. In: Shoshani J, Tassy P (eds) The Proboscidea: Evolution and Palaeoecology of Elephants and Their Relatives. Oxford University Press, Oxford, pp 254-259

    Google Scholar 

  • Luckett WP (1996) Ontogenetic evidence for incisor homologies in proboscideans. In: Shoshani J, Tassy P (eds) The Proboscidea: Evolution and Palaeoecology of Elephants and Their Relatives. Oxford University Press, Oxford, pp 26-31

    Google Scholar 

  • Madden CT (1986) Stegomastodon associated with Mammuthus in Arizona during the Quaternary. Quaternary Res 26:266-271

    Article  Google Scholar 

  • Maglio VJ (1973) Origin and evolution of the Elephantidae. Trans Am Philos Soc 63:1-149

    Article  Google Scholar 

  • Mihlbachler MC (2003) Demography of late Miocene rhinoceroses (Teleoceras proterum and Aphelops malacorhinus) from Florida: linking mortality and sociality in fossil assemblages. Paleobiology 29:412-428

    Article  Google Scholar 

  • Moss CJ (1988) Elephant Memories: Thirteen Years in the Life of an Elephant Family. William Morrow, New York

    Google Scholar 

  • Noubhani A, Hautier L, Jaeger J, Mahboubi M, Tabuce R (2008) Dental and cranial variability of Numidotherium koholense (Mammalia, Proboscidea) from El Kohol, Eocene, Algeria. Geobios 41:515-531

    Article  Google Scholar 

  • Pilgram T, Western D (1986) Inferring the sex and age of African elephants from tusk measurements. Biol Conserv 36:39-52

    Article  Google Scholar 

  • Poole JH (1987) Rutting behavior in African elephants: the phenomenon of musth. Behaviour 102:283-316

    Article  Google Scholar 

  • _____ (1994) Sex differences in the behavior of African elephants, In: Short RV, Balaban E (eds) The Differences Between the Sexes. Cambridge University Press, Cambridge, pp 331-346

    Google Scholar 

  • Ralls K (1976) Mammals in which females are larger than males. Quart Rev Biol 51:245-276

    Article  CAS  PubMed  Google Scholar 

  • _____ (1977) Sexual dimorphism in mammals: avian models and unanswered questions. Am Nat 11:917-938

    Article  Google Scholar 

  • Reznick DA, Bryga H, Endler JA (1990) Experimentally induced life-history evolution in a natural population. Nature 346:357-359

    Article  Google Scholar 

  • Reynolds JD, Harvey PH (1994) Sexual selection and the evolution of sex differences. In: Short RV, Balaban E (eds) The Differences Between the Sexes. Cambridge University Press, Cambridge, pp 53-70

    Google Scholar 

  • Roca AL, Georgiadis N, Pecon-Slattery J, O’Brien SJ (2001) Genetic evidence for two species of elephant in Africa. Science 293:1473-1476

    Article  CAS  PubMed  Google Scholar 

  • Shoshani J (1992) Comparing the living elephants, In: Shoshani J (ed) Elephants: Majestic Creatures of the Wild. Rodale Press, Pennsylvania, pp 36-51

    Google Scholar 

  • Smith KM, Fisher DC (2008) Tusk growth record of a female American mastodon (Mammut americanum) from southwestern New York state. J Vertebr Paleontol 28 (suppl to No 3):144A

    Google Scholar 

  • _____ (2011) Sexual dimorphism in structures showing indeterminate growth: tusks of American mastodons (Mammut americanum). Paleobiology 37:175-194

    Google Scholar 

  • Spain AV, Heinsohn GE, Marsh H, Correll RL (1976) Sexual dimorphism and other sources of variation in a sample of dugong skulls from North Queensland. Aus Zool 24:491-497

    Article  Google Scholar 

  • Sukumar R (1989) The Asian Elephant. Cambridge University Press, Cambridge

    Google Scholar 

  • _____ (2006) A brief review of the status, distribution, and biology of wild Asian elephants. The Zool Soc Lond 40:1-8

    Google Scholar 

  • Sukumar R, Joshi NV, Krishnamurthy V (1988) Growth in the Asian elephant. Proc Indian Acad Sci (Anim Sci) 97:561-571

    Article  Google Scholar 

  • Tassy P (1996) Growth and sexual dimorphism among Miocene elephantoids: the example of Gomphotherium augustidens. In: Shoshani J, Tassy P (eds) The Proboscidea: Evolution and Palaeoecology of Elephants and Their Relatives. Oxford University Press, Oxford, pp 92-100

    Google Scholar 

  • van den Bergh GD (1999) The Late Neogene elephantoid-bearing faunas of Indonesia and their palaeozoogeographic implications: a study of the terrestrial faunal succession of Sulawesi, Flores and Java, including evidence for early hominid dispersal east of Wallace's Line. Scripta Geologica 117:1-419

    Google Scholar 

  • Vanpe C, Kjellander P, Galan M, Cosson J, Aulagnier S, Liberg O, Hewison AJM (2009) Mating system, sexual dimorphism, and the opportunity for sexual selection in a territorial ungulate. Behav Ecol 19:309-316

    Article  Google Scholar 

  • Vidya TNC, Sukumar R (2005) Social organization of the Asian elephant (Elephas maximus) in southern India inferred from microsatellite DNA. J Ethol 23:205-210

    Article  Google Scholar 

  • Weckerly FW (1998) Sexual-size dimorphism: influence of mass and mating systems in the most dimorphic mammals. J Mammal 79:33-52

    Article  Google Scholar 

  • Wilson DE, Reeder DM (eds) (2005) Mammal Species of the World: A Taxonomic and Geographic Reference (3rd edition). John Hopkins University Press, Baltimore

    Google Scholar 

  • Zalmout I, Gingerich P (2008) Sexual dimorphism in the bony pelvis of sea cows from the Eocene of Egypt (Mammalia, Sirenia). J Vertebr Paleontol 28 (suppl to no 3):164A

    Google Scholar 

  • Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004) Geometric Morphometrics for Biologists: A Primer. Elsevier Academic Press, New York

    Google Scholar 

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Acknowledgments

We thank W. Stanley and J. Phelps at the Field Museum of Natural History, Chicago, IL, L. Gordon and D. Schmidt at the National Museum of Natural History, Washington, D.C., and A. Fleming and E. Westwig at the American Museum of Natural History, New York, NY, for access to collections and assistance moving and measuring tusks; J. Johnson for his invaluable assistance during the data-collection portion of this project; C. Badgley, R. Bebej, P. Gingerich,. D. Fox, and one anonymous reviewer for comments and suggestions that improved this manuscript greatly; and A. Rountrey, W. Sanders, A. Wood, and M. Zelditch for contributions throughout this study. Funding was provided by a Scott Turner Award from the University of Michigan, Department of Earth and Environmental Sciences (KMS) and National Science Foundation grants EAR 9628063 and 054095 (DCF).

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Authors and Affiliations

  1. Department of Geology & Geography and Georgia Southern University Museum, Georgia Southern University, Statesboro, GA, USA

    Kathlyn M. Smith

  2. Museum of Paleontology and Department of Earth & Environmental Sciences, University of Michigan, Ann Arbor, MI, USA

    Daniel C. Fisher

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  1. Kathlyn M. Smith
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  2. Daniel C. Fisher
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Correspondence to Kathlyn M. Smith.

Appendices

Appendix I

Table 5 Measurements (cm) used in this study. Abbreviations as in Fig. 2. The dashed line separates mastodons (above) from African elephants (below)
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Appendix II

Table 6 Mastodons included in this study and the methods used to evaluate the sex of each (modified from Smith and Fisher 2011: table 1). Sex-1 lists sex assignment based on prior work utilizing non-tusk dental evidence of age (D), associated skeletal remains (S), or position within the univariate distributions (U) in Smith and Fisher (2011: fig. 1). Sex-2 lists sex assignments determined from a multivariate analysis in Smith and Fisher (2011). Age is the number of annual increments in tusk dentin on the tusk exterior (E) or on a longitudinal section (L)
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Smith, K.M., Fisher, D.C. Sexual Dimorphism and Inter-Generic Variation in Proboscidean Tusks: Multivariate Assessment of American Mastodons (Mammut americanum) and Extant African Elephants. J Mammal Evol 20, 337–355 (2013). https://doi.org/10.1007/s10914-013-9225-6

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