Abstract
Sex-specific interests over the maximization of reproductive success lead to an inter-sexual conflict over the optimal mating system in a species. Traditionally, the outcome of this inter-sexual conflict has been studied from the male perspective but it also depends on female mating strategies, such as manipulating the temporal distribution of sexual activity, advertisement, and mate choice. We used a small nocturnal primate, the gray mouse lemur (Microcebus murinus) to determine the relative importance of female mating strategies on the outcome of this conflict in a species where females are solitary during their activity period. We studied their mating behavior over three consecutive annual mating seasons and determined the genetic relationships among more than 300 study animals to quantify individual reproductive success. We found that most females were receptive asynchronously. Females did not exhibit any obvious direct mate choice, probably due to a highly male-biased operational sex ratio and the corresponding costs of choosiness. However, females exercised indirect choice for multiple matings. They mated with 1–7 males up to 11 times during their single night of receptivity. As a result, mixed paternity was common but heavier males sired more offspring, meaning that indirect female choice for superior males cannot be excluded. Females exhibited a mixed mating strategy, avoiding costly direct mate choice but still counteracting male efforts to monopolize mating, successfully increasing genetic variability among offspring. Thus, females had a major influence on the outcome of the inter-sexual conflict despite male monopolization attempts.
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References
Agrell J, Wolff Jerry O, Ylönen H (1998) Counter-strategies to infanticide in mammals: costs and consequences. Oikos 83:507–517
Ahnesjö I, Vincent A, Alatalo R, Halliday T, Sutherland WJ (1992) The role of females in influencing mating patterns. Behav Ecol 4:187–189
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–265
Andrès M, Solignac M, Perret M (2003) Mating system in mouse lemurs: theories and facts, using analysis of paternity. Fol Primatol 74:355–366
Barre V, Lebec A, Petter J-J, Albignac R (1988) Etude du Microcèbe par radiotracking dans la foret de l’Ankarafantsika. In: Rakotovato L, Barre V, Sayer J (eds) L’Equilibre des Ecosystèmes Forestiers a Madagascar: Actes d’un Seminaire International. IUCN, Gland, pp 61–71
Beach FA (1976) Sexual attractivity, proceptivity, and receptivity in female mammals. Horm Behav 7:105–138
Berteaux D, Bêty J, Rengifo E, Bergeron J-M (1999) Multiple paternity in meadow voles (Microtus pennsylvanicus): investigating the role of the female. Behav Ecol Sociobiol 45:283–291
Birkhead TR (2000a) Defining and demonstrating postcopulatory female choice—again. Evolution 54:1057–1060
Birkhead TR (2000b) Hidden choices of females. Nat Hist 10:66–71
Birkhead TR, Kappeler PM (2004) Post-copulatory sexual selection in birds and primates. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, Cambridge, pp 151–171
Birkhead TR, Møller AP (1993) Female control of paternity. TREE 8:100–104
Brockman HJ (2001) The evolution of alternative strategies and tactics. Adv Stud Behav 30:1–51
Buesching CD, Heistermann M, Hodges JK, Zimmermann E (1998) Multimodal oestrus advertisement in a small nocturnal prosimian, Microcebus murinus. Fol Primatol 69:295–308
Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. TREE 18:41–47
Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton
Clutton-Brock TH, Parker GA (1992) Potential reproductive rates and the operation of sexual selection. Q Rev Biol 67:437–456
Clutton-Brock TH, Parker GA (1995) Sexual coercion in animal societies. Anim Behav 49:1345–1365
Corbin GD, Schmid J (1995) Insect secretions determine habitat use patterns by a female lesser mouse lemur (Microcebus murinus). Am J Primatol 37:317–324
Davies NB (1992) Dunnock behaviour and social evolution. Oxford University Press, Oxford
Dixson AF (1998) Primate sexuality. Oxford University Press, Oxford
Dominey WJ (1984) Alternative mating tactics and evolutionarily stable strategies. Am Zool 24:385–396
East ML, Burke T, Wilhelm K, Greig C, Hofer H (2003) Sexual conflicts in spotted hyenas: male and female mating tactics and their reproductive outcome with respect to age, social status and tenure. Proc R Soc Lond B 270:1247–1254
Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton
Eberhard WG (1998) Female roles in sperm competition. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, London, pp 91–116
Eberle M, Kappeler PM (2002) Mouse lemurs in space and time: a test of the socioecological model. Behav Ecol Sociobiol 51:131–139
Eberle M, Kappeler PM (2004) Sex in the dark: determinants and consequences of mixed male mating tactics in Microcebus murinus, a small solitary nocturnal primate. Behav Ecol Sociobiol (in press)
Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223
Fedorkaf KM, Mousseau TA (2002) Material and genetic benefits of female multiple mating and polyandry. Anim Behav 64:361–367
Ford RG, Pitelka FA (1984) Resource limitation in populations of the California vole Microtus californicus. Ecology 65:122–136
Gavrilets S, Scheiner SM (1993) The genetics of phenotypic plasticity. V. Evolution of reaction norm shape. J Evol Biol 6:31–48
Gavrilets S, Arnqvist G, Friberg U (2001) The evolution of female mate choice by sexual conflict. Proc R Soc Lond B 268:531–539
Ghiselin MT (1974) The economy of nature and the evolution of sex. University of California Press, Berkeley
Glatston ARH (1979) Reproduction and behaviour of the lesser mouse lemur (Microcebus murinus, Miller 1777) in captivity. PhD Thesis, University of London
Gowaty PA (2004) Sex roles, contests for the control of reproduction, and sexual selection. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, Cambridge, pp 37–54
Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212
Hapke A, Eberle M, Zischler H (2003) Isolation of new microsatellite markers and application in four species of mouse lemurs (Microcebus sp.). Mol Ecol Notes 3:205–208
Hazel WN, Smock R, Johnson MD (1990) A polygenic model for the evolution and maintenance of conditional strategies. Proc R Soc Lond B 242:181–187
Hladik CM, Charles-Dominique P, Petter J-J (1980) Feeding strategies of five nocturnal prosimians in the dry forest of the west coast of Madagascar. In: Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pages E, Pariente GF, Petter-Rousseaux A, Petter J-J, Schilling A (eds) Nocturnal Malagasy primates: ecology, physiology and behavior. Academic, New York, pp 41–73
Hrdy SB (1979) Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol Sociobiol 1:13–40
Huber S, Millesi E, Dittami JP (2002) Paternal effort and its relation to mating success in the European ground squirrel. Anim Behav 63:157–164
Ims RA (1988) The potential for sexual selection in males: effect of sex ratio and spatiotemporal distribution of receptive females. Evol Ecol 2:338–352
Ims RA (1990a) The ecology and evolution of reproductive synchrony. TREE 5:135–140
Ims RA (1990b) Mate detection success of male Clethrionomys rufocanus in relation to the spatial distribution of sexually receptive females. Evol Ecol 4:57–61
Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64
Kappeler PM (1993) Female dominance in primates and other mammals. In: Bateson PPG, Klopfer PH, Thompson NS (eds) Perspectives in ethology behaviour and evolution. Plenum, New York, pp 143–158
Kappeler PM (1997) Determinants of primate social organization: comparative evidence and new insights from Malagasy lemurs. Biol Rev 72:111–151
Kappeler PM (2000) Ecologie des microcèbes. Primatologie 3:145–171
Kappeler PM, van Schaik CP (2002) Evolution of primate social systems. Int J Primatol 23:707–740
Keller BL (1984) Reproductive patterns. Spec Publ Am Soc Mammal 8:725–778
Kempenaers B (1997) Does reproductive synchrony limit male opportunities or enhance female choice for extra-pair paternity? Behaviour 134:551–562
Kleiman DG, Malcolm JR (1981) The evolution of male parental investment in mammals. In: Gubernick DJ, Klopfer PH (eds) Parental care in mammals. Plenum, New York, pp 347–387
Kokko H, Brooks R, Jennions MD, Morley J (2003) The evolution of mate choice and mating biases. Proc R Soc Lond B 270:653–664
Koprowski JL (1992) Removal of copulatory plugs by female tree squirrels. J Mammal 73:572–576
Marshall TC, Slate J, Kruuk LEB, Pemperton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655
Martin RD (1973) A review of the behavior and ecology of the lesser mouse lemur (Microcebus murinus). In: Michael RP, Crook JH (eds) Comparative ecology and behavior of primates. Academic, London, pp 1–68
Moore AJ, Gowaty PA, Wallin WG, Moore PJ (2001) Sexual conflict and the evolution of female mate choice and male dominance. Proc R Soc Lond B 268:517–523
Noordwijk MA van, Schaik CP van (2000) Reproductive patterns in eutherian mammals: adaptions against infanticide? In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 322–360
Nunn CL, Altizer SM (2004) Sexual selection, behaviour and sexually transmitted diseases. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, Cambridge, pp 117–130
Pagès-Feuillade E (1988) Modalites de l’occupation de l’espace et relations interindividuelles chez un prosimien nocturne malgache (Microcebus murinus). Fol Primatol 50:204–220
Parga JA (2003) Copulatory plug displacement evidences sperm competition in Lemur catta. Int J Primatol 24:889–899
Paul A (2002) Sexual selection and mate choice. Int J Primatol 23:877–904
Pereira ME (1991) Asynchrony within estrous synchrony among ringtailed lemurs (Primates. Lemuridae). Physiol Behav 49:47–52
Perret M (1982) Influence du groupement social sur la reproduction de la femelle de Microcebus murinus (Miller 1777). Z Tierpsychol 60:47–65
Petter-Rousseaux A (1964) Reproductive physiology and behavior of the Lemuroidea. In: Buettner-Janusch J (ed) Evolutionary and genetic biology of primates. Academic, New York, pp 91–132
Pizzari T, Birkhead TR (2000) Female feral fowl eject sperm of subdominant males. Nature 405:787–789
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275
Radespiel U, Zimmermann E (2001) Female dominance in captive gray mouse lemurs (Microcebus murinus). Am J Primatol 54:181–192
Radespiel U, Cepok S, Zietemann V, Zimmermann E (1998) Sex-specific usage patterns of sleeping sites in grey mouse lemurs (Microcebus murinus) in northwestern Madagascar. Am J Primatol 46:77–84
Rensing S (1999) Immobilization and anesthesia of nonhuman primates. Primate Rep 55:33–38
Reynolds JD, Gross MR (1990) Costs and benefits of female mate choice: is there a lek paradoxon? Am Nat 136:230–243
Richard AF (1987) Malagasy prosimians: female dominance. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 25–33
Schaik CP van (2000) Infanticide by male primates: the sexual selection hypothesis revisited. In: van Schaik CP, Janson CH (eds) Infanticide by males and Its Implications. Cambridge University Press, Cambridge, pp 27–60
Schaik CP van, Janson CH (2000) Infanticide by males and its implications. Cambridge University Press, Cambridge
Schaik CP van, Hodges JK, Nunn CL (2000) Paternity confusion and the ovarian cycle of female primates. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 361–387
Schmid J (1998) Tree holes used for resting by gray mouse lemurs (Microcebus murinus) in Madagascar: insulation capacities and energetic consequences. Int J Primatol 19:797–809
Schwagmeyer PL (1988) Scramble-competition polygyny in an asocial mammal: male mobility and mating success. Am Nat 131:885–892
Schwagmeyer PL (1994) Competitive mate searching in thirteen-lined ground squirrels (Mammalia, Sciuridae): potential roles of spatial memory. Ethology 98:265–276
Schwagmeyer PL, Parker GA, Mock DW (1998) Information asymmetries among males: implications for fertilization success in the thirteen-lined ground squirrel. Proc R Soc Lond B 265:1861–1865
Setchell JM, Kappeler PM (2003) Selection in relation to sex in primates. Adv Stud Behav 33:87–174
Simmons LW (2001) The evolution of polyandry: an examination of the genetic incompatibility and good-sperm hypotheses. J Evol Biol 14:585–594
Smuts BB, Smuts RW (1993) Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Adv Stud Behav 22:1–63
Soltis J, Mitsunaga F, Shimizu K, Yanagihara Y, Nozaki M (1997) Sexual selection in Japanese macaques. I. Female mate choice or male sexual coercion? Anim Behav 54:725–736
Sorg J-P, Ganzhorn JU, Kappeler PM (2003) Forestry and research in the Kirindy Forest/Centre de Formation Professionelle Forestière. In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. The University of Chicago Press, Chicago, pp 1512–1519
Sterling EJ, Nguyen N, Fashing PJ (2000) Spatial patterning in nocturnal prosimians: a review of methods and relevance to studies of sociality. Am J Primatol 51:3–19
Strier KB (1999) Faces in the forest: the endangered Muriqui monkeys of Brazil. Harvard University Press, Cambridge
Stutchbury BJM (1998) Female mate choice of extra-pair males: breeding synchrony is important. Behav Ecol Sociobiol 43:213–215
Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1193
Vries H de, Netto W, Hanegraaf PLH (1993) MatMan: a program for the analysis of sociometric matrices and behavioural transition matrices. Behaviour 125:157–175
Weatherhead PJ (1997) Breeding synchrony and extra-pair mating in red-winged blackbirds. Behav Ecol Sociobiol 403:151–158
Wiley RH, Poston J (1996) Indirect mate choice, competition for mates and coevolution of the sexes. Evolution 50:1371–1381
Wimmer B (2000) Untersuchung der Paarungssysteme und Populationsstruktur von Lemuren an Coquerel’s Zwergmaki (Mirza coquereli), dem grauen Mauslemur (Microcebus murinus), dem Rotstirnmaki (Eulemur fulvus rufus) und dem Larvensifaka (Propithecus verreauxi verreauxi). PhD Thesis, University of Munich
Wolff JO, Macdonald DW (2004) Promiscuous females protect their offspring. TREE 19:127–134
Wrogemann D, Radespiel U, Zimmermann E (2000) Comparison of reproductive characteristics and changes in body weight between captive populations of rufous and gray mouse lemurs. Int J Primatol 22:91–108
Yezerinac SM, Weatherhead PJ (1997) Reproductive synchrony and extra-pair mating strategy in a socially monogamous bird, Dendroica petechia. Anim Behav 54:1393–1403
Zeh JA, Zeh DW (2003) Toward a new sexual selection paradigm: polyandry, conflict and incompatibility. Ethology 109:929–950
Zimmermann E (1995) Acoustic communication in nocturnal prosimians. In: Alterman L, Doyle GA, Izard MK (eds) Creatures of the dark. Plenum, New York, pp 311–330
Acknowledgements
We thank Berthe Rakotosamimanana (Département de Paléontologie et d’Anthropologie Biologique de l’Université d’Antananarivo), Olga Ramilijaona and Daniel Rakotondravony (Département de Biologie Animale, Université d’Antananarivo), Lucien Rakotozafy (Parc Botanique et Zoologique Tsimbazaza Antananarivo), the Commission Tripartite and the CAFF of the Direction des Eaux et Forêts, the CFPF Morondava, and Jörg U. Ganzhorn, Hans Zischler and Andreas Hapke for their authorization or support of this study. Thanks go to Tiana Andrianjanahary, Karoline Franz and Wiebke Plästerer for assistance in the field, and to Dietmar Zinner, Patty Gowaty, Lee C. Drickamer and an anonymous reviewer for their helpful comments on an earlier version of the manuscript. This article is part of a doctoral study by M. Eberle in the Faculty of Biology, University of Hamburg, with financial support from the Deutsches Primatenzentrum (DPZ) and the Deutsche Forschungsgemeinschaft (DFG, Ka 1082/5-1, 2).
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Eberle, M., Kappeler, P.M. Selected polyandry: female choice and inter-sexual conflict in a small nocturnal solitary primate (Microcebus murinus). Behav Ecol Sociobiol 57, 91–100 (2004). https://doi.org/10.1007/s00265-004-0823-4
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DOI: https://doi.org/10.1007/s00265-004-0823-4