Abstract
Sexual dimorphism in body size and canine weaponry is commonly associated with high levels of male-male competition. When group living species do not rely heavily on male-male competition for access to females, sperm competition may represent a viable alternative strategy. Unlike most haplorhine primates, lemurs are typically monomorphic in body weight and canine height. We assessed variability of body mass dimorphism and canine size dimorphism in brown lemurs using morphometric data from 3 populations in southeastern Madagascar: Eulemur fulvus rufus, E. albocollaris, and hybrids of the species. We found significant male-biased canine dimorphism in E. albocollaris in conjunction with body-size monomorphism. We observed similar patterns in the hybrids, but E. fulvus rufus exhibited significant female-biased size dimorphism and canine monomorphism. Testes volume was relatively high across study populations. Thus, sperm competition appears to be strong in brown lemurs. E. albocollaris males combine sperm competition with large canines, but not higher body mass, indicating a difference in sexual strategy from most lemurs. Patterns of body mass and canine size dimorphism are not uniform across brown lemur populations, indicating that future work on these populations can explicitly test models that predict relationships between size dimorphism and various types of competition.
Similar content being viewed by others
References
Albrecht, G. H., Jenkins, P. D., and Godfrey, L. R. (1990). Ecogeographic size variation among the living and subfossil prosimians of Madagascar. A. J. Primatol. 22: 1–50.
Bradley, B., and Stumpf, R. M. (1997). Morphometrics of Eulemur fulvus albocollaris in Vevembe Forest, Madagascar. Am. J. Phys. Anthropol. (Suppl.) 24: 79–80.
Brown, L., Shumaker, R. W., and Downhower, J. F. (1995). Do primates experience sperm competition? Am. Natur. 146: 302–306.
Chernick, M. R. (1999). Bootstrap Methods: A Practitioner's Guide, John Wiley& Sons, New York.
Cheverud, J. M., Dow, M. M., and Leutenegger, W. (1985). The quantitative assessment of phylogenetic constraints in comparative analysis: sexual dimorphism in body weight among primates. Evolution 39: 1335–1351.
Clutton-Brock, T. H., Harvey, P. H., and Rudder, B. (1977). Sexual dimorphism, socionomic sex ratio and body weight in primates. Nature 269: 797–800.
Colquhoun, I. (1997). A Predictive Socioecological Study of the Black Lemur (Eulemur macaco macaco) in Northwestern Madagascar, Ph.D. dissertation, Washington University, St. Louis, Missouri.
Crook, J. H. (1972). Sexual selection, dimorphism, and social organization. In Campbell, B. (ed.), Sexual Selection and the Descent of Man 1871–1971, Aldine, Chicago, pp. 231–281.
Darwin, C. (1871). The Descent of Man, and Selection in Relation to Sex, J. Murray, London.
DeVore, I., and Washburn, S. L. (1963). Baboon ecology and human evolution. In Howell, F. C., and Bourlière, F. (eds.), African Ecology and Human Evolution., Aldine, Chicago, pp. 335–367.
Dixson, A. F. (1987). Observations on the evolution of genitalia and copulatory behavior in male primates. J. Zool. (21) 3: 423–443.
Dixson, A. F. (1995). Sexual selection and the evolution of copulatory behavior in nocturnal prosimians. In Alterman, L., Doyle, G. A., and Izard, M. K. (eds.), Creatures of the Dark: The Nocturnal Prosimians, Plenum Press, New York, pp. 93–118.
Dixson, A. F. (1998). Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes and Human Beings, Oxford University Press, Oxford.
Djlelati, R., Brun, B., and Rumpler, Y. (1997). Meiotic study of hybrids in the genus Eulemur and taxonomic considerations . Am. J. Primatol. 42: 235–245.
Emlen, S. T., and Oring, L. W. (1977). Ecology, sexual selection, and the evolution of mating systems . Science 197: 215–223.
Erhart, E. M., and Overdorff, D. J. (1999). Female coordination of group travel in wild Propithecus and Eulemur. Int. J. Primatol. 20: 927–940.
Fietz, J. (1999). Mating system of Microcebus murinus. Am. J. Primatol. 48: 127–133.
Freed, B. Z. (1996). Co-occurence Among Crowned Lemurs (Lemur coronatus) and Sanford's Lemurs Lemur fulvus sanford i) of Madagascar, Ph.D. dissertation, Washington University, St. Louis, Missouri.
Gerson, J. S. (1999). Size in Eulemur fulvus rufus from western Madagascar: sexual dimorphism and ecogeographic variation. Am. J. Phys. Anthropol. (Suppl.) 28: 134.
Gerson, J. S. (2000). Social Relationships in Wild Red-Fronted Brown Lemurs (Eulemur fulvus rufus), Ph.D. dissertation, Duke University, Durham, North Carolina.
Glander, K. E. (1993). Capture and marking techniques for arboreal primates. In Estrada, A., Rodriguez-Luna, E., Lopez–Wilchis, R., and Coates–Estrada, R. (eds.), Estudios Primatologicos en Mexico, Universidad Veracruzana, Veracruz, pp. 299–304.
Glander, K. E., Wright, P. C., Daniels, P. S., and Merenlender, A. M. (1992). Morphometrics and testicle size of rain forest lemur species from southeastern Madagascar . J. Hum. Evol. 22: 1–17.
Godfrey, L. R., Lyon, S. K., and Sutherland, M. R. (1993). Sexual dimorphism in large-bodied primates: the case of the subfossil lemurs. Am. J. Phys. Anthropol. 90: 315–334.
Godfrey, L. R., Razafimahzo, J. C., and Schwartz, M. (2002). Dental monorphism in a wild population of Propithecus verreauxi from Beza Mahafaly, Southwestern Madagascar. Am. J. Phys. Anthropol. (Suppl.) 34: 76.
Godfrey, L. R., Sutherland, M. R., Petto, A. J., and Boy, D. S. (1990). Size, space, and adaptation in some subfossil lemurs from Madagascar. Am. J. Phys. Anthropol. 81: 45–66.
Greenfield, L. O. (1992). Relative canine size, behavior, and diet in male ceboids. J. Hum. Evol. 23: 469–480.
Harcourt, A. H. (1991). Sperm competition and the evolution of nonfertilizing sperm in mammals. Evolution 45: 314–328.
Harcourt, A. H. (1995). Sexual selection and sperm competition in primates: What are male genitalia good for? Evol. Anthropol. 4: 121–129.
Harcourt, A. H., and Gardiner, J. (1994). Sexual selection and genital anatomy of male primates. Proc. R. Soc. Lond. [Biol. Sci.] 255: 47–53.
Harcourt, A. H., Harvey, P. H., Larson, S. G., and Short, R. V. (1981). Testis weight, body weight, and breeding system in primates . Nature 293: 55–57.
Harcourt, A. H., Purvis, A., and Liles, L. (1995). Sperm competition: mating system, not breeding season, affects testes size of primates. Funct. Ecol. 9: 468–476.
Harvey, P. H., and Harcourt, A. H. (1984). Sperm competition, testes size, and breeding systems in primates. In Smith, R. L. (ed.), Sperm Competition and the Evolution of Animal Mating Systems, Academic Press, San Diego, pp. 589–599.
Hemingway, C. A. (1995). Feeding and Reproductive Strategies of the Milne-Edwards' Sifaka (Propithecus diadema edwardsi), Ph.D. dissertation, Duke University, Durham, North Carolina.
Ihaka, R., and Gentleman, R. (1996). R: A language for data analysis and graphics. J. Comput. Graph. Statist. 5: 299–314.
Johnson, S., and Wyner, Y. (2000). Notes on the biogeography of E. f. albocollaris. Lemur News 5: 25–28.
Johnson, S. E. (2002). Ecology and Speciation in Brown Lemurs: White-Collared Lemurs (Eulemur albocollaris) and Hybrids Eulemur albocollaris X Eulemur fulvus rufus) in Southeastern Madagascar, Ph.D. dissertation, University of Texas at Austin, Austin, Texas.
Jolly, C. J., and Phillips-Conroy, J. E. (2003). Testicular size, mating system, and maturation schedules in wild anubis and hamadryas baboons . Int. J. Primatol. 24: 125–142.
Kappeler, P. M. (1990). The evolution of sexual size dimorphism in Prosimian primates. Am. J. Primatol. 21: 201–214.
Kappeler, P. M. (1991). Patterns of sexual dimorphism in body weight among prosimian primates. Folia Primatol. 57: 132–146.
Kappeler, P. M. (1996). Intrasexual selection and phylogenetic constraints in the evolution of sexual canine dimorphism in strepsirhine primates. J. Evol. Biol. 9: 43–65.
Kappeler, P. M. (1997). Intrasexual selection and testis size in strepsirhine primates. Behav. Ecol. 8: 10–19.
Kay, R. F., Plavcan, J. M., Glander, K. E., and Wright, P. C. (1988). Sexual selection and canine dimorphism in New World monkeys. Am. J. Phys. Anthropol. 77: 385–397.
Lande, R. (1980). Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 33: 292–305.
Leigh, S. R. (1995). Socioecology and the ontogeny of sexual size dimorphism in anthropoid primates . Am. J. Phys. Anthropol. 97: 339–356.
Leigh, S. R., and Terranova, C. J. (1998). Comparative perspectives in bimaturism, ontogeny, and dimorphism in lemurid primates . Int. J. Primatol. 19: 723–750.
Leutenegger, W., and Cheverud, J. M. (1982). Correlates of sexual dimorphism in primates: Ecological and size variables. Int. J. Primatol. 3: 387–402.
Leutenegger, W., and Kelly, J. T. (1977). Relationship of sexual dimorphism in canine size and body size to social, behavioral and ecological correlates in anthropoid primates. Primates 18: 117–136.
Lindenfors, P., and Tullberg, B. S. (1998). Phylogenetic analysis of primate size evolution: the consequences of sexual selection. Biol. J. Linnean Soc. 64: 413–447.
Martin, R. D., Willner, L. A., and Dettling, A. (1994). The evolution of sexual size dimorphism in primates. In Short, R. V., and Balaban, E. (eds.), The Differences Between the Sexes, Cambridge University Press, Cambridge, UK, pp. 159–200.
Masterson, T. J. (2003). Canine dimorphism and interspecific canine form in Cebus. Int. J. Primatol. 24: 160–178.
Milton, K. (1985). Multimale mating and absence of canine tooth dimorphism in wooly spider monkeys (Brachyteles arachnoides) . Am. J. Phys. Anthropol. 68: 519–523.
Mitani, J. C., Gros-Louis, J., and Richards, A. F. (1996). Sexual dimorphism, the operational sex ratio, and the intensity of male competition in polygynous primates. Am. Natur. 147: 966–980.
Møller, A. P. (1988). Ejaculate quality, testes size and sperm competition in primates. J. Hum. Evol. 17: 479–488.
Overdorff, D. J. (1991). Ecological Correlates to Social Structure in Two Prosimian Primates: Eulemur fulvus rufus and Eulemur rubriventer in Madagascar, Ph.D. dissertation, Duke University, Durham, North Carolina.
Overdorff, D. J. (1996). Ecological correlates to social structure in two lemur species in Madagascar. Am. J. Phys. Anthropol. 100: 487–506.
Overdorff, D. J. (1998). Are Eulemur species pair-bonded? Social organization and mating strategies in Eulemur fulvus rufus from 1988–1995 in southeast Madagascar. Am. Phys. Anthropol. 105: 153–166.
Overdorff, D. J., and Johnson, S. E. (2003). Eulemur, true lemurs. In Goodman, S. M., and Benstead, J. (eds.), The Natural History of Madagascar, University of Chicago Press, Chicago, pp. 1320–1324.
Overdorff, D. J., Merenlender, A. M., Talata, P., Telo, A., and Forward, Z. A. (1999). Life history of Eulemur fulvus rufus from 1988–1998 in southeastern Madagascar. Am. J. Phys. Anthropol. 108: 295–310.
Oxnard, C. E. (1987). Fossils, Teeth and Sex: New Perspectives on Human Evolution, University of Washington Press, Seattle.
Pereira, M. E., Kaufman, R., Kappeler, P. M., and Overdorff, D. J. (1990). Female dominance does not characterize all of the Lemuridae. Folia Primatol. 55: 96–103.
Pereira, M. E., and Weiss, M. (1991). Female mate choice, male migration and the threat of infanticide in ring tailed lemurs. Behav. Ecol. Sociobiol. 141–152.
Plavcan, J. M. (1999). Mating systems, intrasexual competition and sexual dimorphism in primates. In Lee, P. C. (ed.), Comparative Primate Socioecology, Cambridge University Press, Cambridge, UK, pp. 241–269.
Plavcan, J. M. (2001). Sexual dimorphism in primate evolution . Yearbk Phys. Anthropol. 44: 25–53.
Plavcan, J. M., and Kelley, J. (1996). Evaluating the “dual selection” hypothesis of canine reduction. Am. J. Phys. Anthropol. 99: 379–387.
Plavcan, J. M., and van Schaik, C. P. (1992). Intrasexual competition and canine dimorphism in anthropoid primates. Am. J. Phys. Anthropol. 87: 461–477.
Plavcan, J. M., and van Schaik, C. P. (1994). Canine dimorphism. Evol. Anthropol. 2: 208–214.
Plavcan, J. M., and van Schaik, C. P. (1997). Intrasexual competition and body weight dimorphism in anthropoid primates. Am. J. Phys. Anthropol. 103: 37–68.
Plavcan, J. M., van Schaik, C. P., and Kappeler, P. M. (1995). Competition, coalitions and canine size in primates . J. Hum. Evol. 28: 245–276.
Pochron, S. T., and Wright, P. C. (2002). Dynamics of testes size compensates for variation in male body size. Evol. Ecol. Res. 4: 577–585.
Pochron, S. T., Wright, P. C., Schaentzler, E., Ippolito, M., Rakotonirina, G., Ratsimbazafy, R., and Rakotosoa, R. (2002). Effect of season and age on the gonadosomatic index of Milne–Edward's sifakas (Propithecus diadema edwardsi) in Ranomafana National Park, Madagascar. Int. J. Primatol. 23: 355–364.
Pollock, J. I. (1979). Female dominance in Indri indri. Folia Primatol. 31: 143–164.
Powzyk, J. A. (1997). The Socio-ecology of Two Sympatric Indriids: Propithecus diadema diadema and Indri indri , a Comparison of Feeding Strategies and Their Possible Repercussions on Species-specific Behaviors, Ph.D. dissertation, Duke University, Durham, North Carolina.
Radespiel, U., and Zimmerman, E. (2001). Female dominance in captive gray mouse lemurs (Microcebus murinus) Am. J. Primatol. 54: 181–192.
Richard, A. F. (1992). Aggressive competition between males, female-controlled polygyny and sexual monomorphism in a Malagasy primate, Propithecus verreauxi. J. Hum. Evol. 22: 395–406.
Rowell, T. E., and Chism, J. (1986). Sexual dimorphism and mating systems: jumping to conclusions. In Pickford, M., and Chiarelli, B. (eds.), Sexual Dimorphism in Living and Fossil Primates, Il Sedicesimo, Florence, pp. 107–111.
Sauther, M. L. (1991). Reproductive behavior of free-ranging Lemur catta at Beza Mahafaly Special Reserve, Madagascar. Am. J. Phys. Anthropol. 84: 463–477.
Short, R. V. (1979). Sexual selection and its component parts, somatic and genital selection, as illustrated by man and the great apes. Adv. Study Behav. 9: 131–158.
Sterck, E. H. M., Watts, D. P., and van Schaik, C. P. (1997). The evolution of female social relationships in nonhuman primates. Behav. Ecol. Sociobiol. 41: 291–309.
Sussman, R. W. (1974). Ecological distinctions in sympatric species of Lemur. In Martin, R. D., Doyle, G. A., and Walker, A. C. (eds.), Prosimian Biology, University of Pittsburgh Press, Pittsburgh, pp. 74–108.
Sussman, R. W. (1992). Male life history and intergroup mobility among ringtailed lemurs (Lemur catta) . Int. J. Primatol. 13: 395–413.
Tattersall, I. (1982). The Primates of Madagascar, Columbia University Press, New York.
van Schaik, C. P., and Kappeler, P. M. (1993). Life history, activity period, and lemur social systems. In Kappeler, P. M., and Ganzhorn, J. U. (eds.), Lemur Social Systems and Their Ecological Basis, Plenum, New York, pp. 241–260.
van Schaik, C. P., and Kappeler, P. M. (1996). The social systems of gregarious lemurs: lack of convergence with anthropoids due to evolutionary disequilibrium? Ethology 102: 915–941.
Vasey, N. (2000). Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: I. Interspecific patterns. Am. J. Phys. Anthropol. 112: 411–432.
Wrangham, R. W. (1980). An ecological model of female-bonded primate groups . Behaviour 75: 262–300.
Wright, P. C. (1993). Variations in male-female dominance and offspring care in non–human primates. In Miller, B. D. (ed.), Sex and Gender Hierarchies, Cambridge University Press, Cambridge, UK, pp. 127–145.
Wright, P. C. (1995). Demography and life history of free-ranging Propithecus diadema edwardsi in Ranomafana National Park, Madagascar . Int. J. Primatol. 16: 835–854.
Wright, P. C. (1999). Lemur traits and Madagascar ecology: coping with an island environment. Yearbk Phys. Anthropol. 42: 31–72.
Wyner, Y., Absher, R., Amato, G., Sterling, E., Stumpf, R., Rumpler, Y., and DeSalle, R. (1999). Species concepts and the determination of historic gene flow patterns in the Eulemur fulvus (brown lemur) complex. Biol. J. Linnean Soc. 65: 39–56.
Wyner, Y. M., Johnson, S. E., Stumpf, R. M., and DeSalle, R. (2002). Genetic assessment of a white—collared X red—fronted lemur hybrid zone at Andringitra, Madagascar . Am. J. Primatol. 57: 51–66.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Johnson, S.E., Gordon, A.D., Stumpf, R.M. et al. Morphological Variation in Populations of Eulemur albocollaris and E. fulvus rufus . Int J Primatol 26, 1399–1416 (2005). https://doi.org/10.1007/s10764-005-8858-6
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10764-005-8858-6