Abstract
In mammals with solitary females, the potential for males to monopolize matings is relatively low, and scramble competition polygyny is presumed to be the predominant mating system. However, combinations of male traits and mating tactics within this type of polygyny have been described. The main aim of our study was to identify the relative importance of, and interactions among, potential determinants of contrasting male reproductive tactics, and to determine their consequences for male reproductive success in a small solitary nocturnal Malagasy primate, the gray mouse lemur (Microcebus murinus). We studied their mating behavior over three consecutive annual mating seasons. In addition, we determined the genetic relationships among more than 300 study animals to quantify the reproductive success of individual males. We found that, with a given relatively low overall monopolization potential, successful male mouse lemurs roamed extensively in search of mates, had superior finding ability and mated as early as possible. However, contest competition was important too, as temporary monopolization was also possible. Males exhibited different mating tactics, and heavier males had a higher reproductive success, although most litters had mixed paternities. Switching between tactics depended on short-term local variation in monopolization potential determined by a pronounced dynamic in fertilization probability, number of alternative mating opportunities, and the operational sex ratio. This study also revealed that the dynamics of these determinants, as well as the mutual interactions between them, necessitate a detailed knowledge of the mating behavior of a species to infer the impact of determinants of alternative mating tactics.
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References
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–265
Altmann J (1990) Primate males go where the females are. Anim Behav 39:193–195
Andrès M, Gachot-Neveu H, Perret M (2001) Genetic determination of paternity in captive grey mouse lemurs: pre-copulatory sexual competition rather than sperm competition in a nocturnal prosimian? Behaviour 138:1047–1063
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
Bartman S, Gerlach G (2001) Multiple paternity and similar variance in reproductive success of male and female wood mice (Apodemus sylvaticus) housed in an enclosure. Ethology 107:889–899
Beach FA (1976) Sexual attractivity, proceptivity, and receptivity in female mammals. Horm Behav 7:105–138
Birkhead TR (1995) Sperm competition: evolutionary causes and consequences. Reprod Fertil Dev 7:755–775
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
Charles-Dominique P, Martin RD (1970) Evolution of lorises and lemurs. Nature 227:257–260
Chism J, Rogers W (1997) Male competition, mating success and female choice in a seasonally breeding primate (Erythrocebus patas). Ethology 103:109–126
Clutton-Brock TH (1989) Mammalian mating systems. Proc R Soc Lond B 236:339–372
Clutton-Brock TH (1991) The evolution of sex differences and the consequences of polygyny in mammals. In: Bateson P (ed) The development and integration of behaviour. University of Cambridge Press, Cambridge, pp 229–253
Clutton-Brock TH, Parker GA (1992) Potential reproductive rates and the operation of sexual selection. Q Rev Biol 67:437–456
Cooper WE, Vitt LJ (2002) Increased predation risk while mate guarding as a cost of reproduction for male broad-headed skinks (Eumeces laticeps). Acta Ethol 5:19–23
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
Davis LS, Murie JO (1985) Male territoriality and the mating system of Richardson’s ground squirrel. J Mammal 66:268–279
Devine MC (1975) Copulatory plugs in snakes: enforced chastity. Science 187:844–845
Dixson AF, Anderson MJ (2002) Sexual selection, seminal coagulation and copulatory plug formation in primates. Fol Primatol 73:63–69
Dominey WJ (1984) Alternative mating tactics and evolutionarily stable strategies. Am Zool 24:385–396
Dunbar RIM (2000) Male mating strategies: a modeling approach. In: Kappeler PM (ed) Primate males. Cambridge University Press, Cambridge, pp 259–268
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) Selected polyandry: female choice and inter-sexual conflict in a small nocturnal solitary primate (Microcebus murinus). Behav Ecol Sociobiol (in press)
Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223
Fietz J, Zischler H, Schwiegk C, Tomiuk J, Dausmann KH, Ganzhorn JU (2000) High rates of extra-pair young in the pair-living fat-tailed dwarf lemur, Cheirogaleus medius. Behav Ecol Sociobiol 49:8–17
FitzGibbon CD (1997) The adaptive significance of monogamy in the golden-rumped elephant-shrew. J Zool Lond 242:167–177
Forchhammer MC, Boomsma JJ (1998) Optimal mating strategies in nonterritorial ungulates: a general model tested on muskoxen. Behav Ecol 9:136–143
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
Ghiselin MT (1974) The economy of nature and the evolution of sex. University of California Press, Berkeley
Gillott C (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu Rev Entomol 48:163–184
Glatston ARH (1979) Reproduction and behaviour of the lesser mouse lemur (Microcebus murinus, Miller 1777) in captivity. PhD Thesis, University of London
Goodman SM, O’Connor S, Langrand O (1993) A review of predation on lemurs: implications for the evolution of social behavior in small, nocturnal primates. In: Kappeler PM, Ganzhorn JU (eds) Lemur social systems and their ecological basis. Plenum, New York, pp 51–66
Gowaty PA, Drickamer LC, Schmid-Holmes S (2003) Male house mice produce fewer offspring with lower viability and poorer performance when mated with females they do not prefer. Anim Behav 65:95–103
Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. TREE 11:92–98
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
Hohoff C, Franzen K, Sachser N (2003) Female choice in a promiscuous wild guinea pig, the yellow-toothed cavy (Galea musteloides). Behav Ecol Sociobiol 53:341–349
Hooge PN, Eichenlaub W, Solomon E (1999) The animal movement program. USGS, Alaska Biological Science Center
Huck UW, Tonias BA, Lisk RD (1989) The effectiveness of competitive male inseminations in golden hamsters, Mesocricetus auratus, depends on an interaction of mating order, time delay between males, and the time of mating relative to ovulation. Anim Behav 37:674–680
Ims RA (1988a) The potential for sexual selection in males: effect of sex ratio and spatiotemporal distribution of receptive females. Evol Ecol 2:338–352
Ims RA (1988b) Spatial clumping of sexually receptive females induces space sharing among male voles. Nature 335:541–543
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
Ims RA (1994) Litter sex ratio variation in laboratory colonies of two geographically distinct strains of the root vole Microtus oeconomus. Ecography 17:141–146
Kappeler PM (1997) Determinants of primate social organization: comparative evidence and new insights from Malagasy lemurs. Biol Rev 72:111–151
Kappeler PM (2000a) Causes and consequences of unusual sex ratios among lemurs. In: Kappeler PM (ed) Primate males. Cambridge University Press, Cambridge, pp 55–63
Kappeler PM (2000b) Ecologie des microcèbes. Primatologie 3:145–171
Keller BL (1984) Reproductive patterns. Spec Publ Am Soc Mammal 8:725–778
Kleiman DG (1977) Monogamy in mammals. Q Rev Biol 52:39–69
Koga T, Backwell PRY, Jennions MD, Christy JH (1998) Elevated predation risk changes mating behaviour and courtship in fiddler crab. Proc R Soc Lond B 265:1385–1390
Kotiaho J, Alatalo RV, Mappes J, Parri S, Rivero A (1998) Male mating success and risk of predation in a wolf spider: a balance between sexual and natural selection? J Anim Ecol 67:287–291
Kraaijeveld-Smit FJL, Ward SJ, Temple-Smith PD (2002) Multiple paternity in a field population of a small carnivorous marsupial, the agile antechinus, Antechinus agilis. Behav Ecol Sociobiol 52:84–91
Kraus C, Künkele J, Trillmich F (2003) Spacing behaviour and its implications for the mating system of a presocial small mammal: an almost asocial cavy Cavia magna? Anim Behav 66:225–238
Kvarnemo C, Ahnesjö I (1996) The dynamics of operational sex ratios and competition for mates. TREE 11:404–408
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
Michener GR, McLean IG (1996) Reproductive behaviour and operational sex ratio in Richardson’s ground squirrels. Anim Behav 52:743–758
Mitani JC, Gros-Louis J, Richards AF (1996) Sexual dimorphism, the operational sex ratio, and the intensity of male competition in polygynous primates. Am Nat 147:966–980
Natoli E, de Vito E (1991) Agonistic behavior, dominance rank and copulatory success in a large multi-male feral cat Felis catus L. colony in central Rome Italy. Anim Behav 42:227–242
Nelson J (1995) Determinants of male spacing behaviour in microtines: an experimental manipulation of female spatial distribution and density. Behav Ecol Sociobiol 37:217–223
Paetkau D, Strobeck C (1994) Microsatellite analysis of genetic variation in black bear populations. Mol Ecol 3:489–495
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
Parijs SM van, Lydersen C, Kovacs KM (2003) Vocalizations and movements suggest alternative mating tactics in male bearded seals. Anim Behav 65:273–283
Parker GA, Ball MA, Stockley P, Gage MJG (1997) Sperm competition games: a prospective analysis of risk assessment. Proc R Soc Lond B 264:1793–1802
Paul A (2002) Sexual selection and mate choice. Int J Primatol 23:877–904
Pemberton JM, Coltman DW, Smith JA, Pilkington JG (1999) Molecular analysis of a promiscuous, fluctuating mating system. Biol J Linn Soc 68:289–301
Perret M (1982) Influence du groupement social sur la reproduction de la femelle de Microcebus murinus (Miller 1777). Z Tierpsychol 60:47–65
Perret M (1992) Environmental and social determinants of sexual function in the male lesser mouse lemur (Microcebus murinus). Fol Primatol 59:1–25
Perret M (2000) Reproduction saisonnière et succès reproducteur chez un prosimien malgache, Microcebus murinus. Primatologie 3:45–84
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
Plesner Jensen S, Gray SJ, Hurst JL (2003) How does habitat structure affect activity and use of space among house mice? Anim Behav 66:239–250
Preston BT, Stevenson IR, Pemberton JM, Coltman DW, Wilson K (2003) Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success. Proc R Soc Lond B 270:633–640
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275
Radespiel U (2000) Sociality in the gray mouse lemur (Microcebus murinus) in Northwestern Madagascar. Am J Primatol 51:21–40
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
Radespiel U, Dal Secco V, Drögemüller C, Braune P, Labes E, Zimmermann E (2002) Sexual selection, multiple mating and paternity in grey mouse lemurs, Microcebus murinus. Anim Behav 63:259–268
Radespiel U, Lutermann H, Schmelting B, Bruford MW, Zimmermann E (2003) Patterns and dynamics of sex-biased dispersal in a nocturnal primate, the grey mouse lemur, Microcebus murinus. Anim Behav 65:709–719
Randall JA, Hekkala ER, Cooper LD, Barfield J (2002) Familiarity and flexible mating strategies of a solitary rodent, Dipodomys ingens. Anim Behav 64:11–21
Rasoloarison RM, Goodman SM, Ganzhorn JU (2000) Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. Int J Primatol 21:963–1019
Rensing S (1999) Immobilization and anesthesia of nonhuman primates. Primate Rep 55:33–38
Rooney SM, Wolfe A, Hayden TJ (1998) Autocorrelational data in telemetry studies: time to independence and the problem of behavioural effects. Mammal Rev 28:89–98
Sandell M, Liberg O (1992) Roamers and stayers: a model on male mating tactics and mating systems. Am Nat 139:177–189
Say L, Pontier D, Natoli E (1999) High variation in multiple paternity of domestic cats (Felis catus L.) in relation to environmental conditions. Proc R Soc Lond B 266:2071–2073
Say L, Pontier D, Natoli E (2001) Influence of oestrus synchronization on male reproductive success in the domestic cat (Felis catus L.). Proc R Soc Lond B 268:1049–1053
Schafer JL (1997) Analysis of incomplete multivariate data. Monographs on statistics and applied probability, vol 72. Chapman & Hall, London
Schaik CP van, Kappeler PM (2003) The evolution of social monogamy in primates. In: Reichhard UH, Boesch C (eds) Monogamy: mating strategies and partnerships in birds, humans, and other mammals. Cambridge University Press, Cambridge, pp 59–80
Schmelting B, Ehresmann P, Lutermann H, Randrianambinina B, Zimmermann E (2000) Reproduction of two sympatrically living mouse lemur species (Microcebus murinus, M. ravelobensis) in north-western Madagascar. First results of a long-term study. Fol Primatol 2000 71:189–248
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
Schmid J, Kappeler PM (1998) Fluctuating sexual dimorphism and differential hibernation by sex in a primate, the grey mouse lemur (Microcebus murinus). Behav Ecol Sociobiol 43:125–132
Schradin C (2003) Social flexibility in the South African striped mouse (Rhabdomys pumilio): when to live alone and when to live in groups? 96. Jahresversammlung der Deutschen Zoologischen Gesellschaft & Deutschen Gesellschaft für Parasitologie, Berlin, p 212
Schülke O, Kappeler PM (2003) So near and yet so far: territorial pairs but low cohesion between pair partners in a nocturnal lemur, Phaner furcifer. Anim Behav 65:331–343
Schülke O, Kappeler PM, Zischler H (2004) Small testes size despite high extra-pair paternity in the pair-living nocturnal primate Phaner furcifer. Behav Ecol Sociobiol 55:293–301
Schulte-Hostedde AI, Millar JS (2002) “Little chipmunk” syndrome? Male body size and dominance in captive yellow-pine chipmunks (Tamias amoenus). Ethology 108:127–137
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, Foltz DW (1990) Factors affecting the outcome of sperm competition in thirteen-lined ground squirrels. Anim Behav 39:156–162
Schwagmeyer PL, Parker GA (1990) Male mate choice as predicted by sperm competition in thirteen-lined ground squirrels. Nature 348:62–64
Schwagmeyer PL, Parker GA (1994) Mate-quitting rules for male thirteen-lined ground squirrels. Behav Ecol 5:142–150
Schwagmeyer PL, Woontner SJ (1986) Scramble competition polygyny in thirteen-lined ground squirrels: the relative contributions of overt conflict and competitive mate searching. Behav Ecol Sociobiol 19:359–364
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
Sherman PW (1989) Mate guarding as paternity insurance in Idaho ground squirrels. Nature 338:418–420
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
Stockley P (1996) Synchrony of estrus in common shrews. J Mammal 77:383–387
Taberlet P, Luikart G (1999) Non-invasive genetic sampling and individual identification. Biol J Linn Soc 68:41–55
Taylor AC, Horsup A, Johnson CN, Sunnucks P, Sherwin B (1997) Relatedness structure detected by microsatellite analysis and attempted pedigree reconstruction in an endangered marsupial, the northern hairy-nosed wombat Lasiorhinus krefftii. Mol Ecol 6:9–19
Tegelström H, Searle JB, Brookfield J, Mercer S (1991) Multiple paternity in wild common shrews (Sorex araneus) is confirmed by DNA fingerprinting. Heredity 66:373–379
Voss R (1979) Male accessory glands and the evolution of copulatory plugs in rodents. Occ Pap Mus Zool Univ Mich 689:1–27
Weckerly FW (1998) Sexual-size dimorphism: influence of mass and mating systems in the most dimorphic mammals. J Mammal 79:33–52
Westneat DF, Sherman PW, Morton ML (1990) The ecology and evolution of extra-pair copulations in birds. Curr Ornithol 7:331–369
Whitehead H (1990) Rules for roving males. J Theor Biol 145:355–368
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
Wimmer B, Tautz D, Kappeler PM (2002) The genetic population structure of the gray mouse lemur (Microcebus murinus), a basal primate from Madagascar. Behav Ecol Sociobiol 52:166–175
Wittenberger JF, Tilson RL (1980) The evolution of monogamy: hypotheses and evidence. Annu Rev Ecol Syst 11:50–68
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
Xia X, Millar JS (1991) Genetic evidence of promiscuity in Peromyscus leucopus. Behav Ecol Sociobiol 28:171–178
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, Susan C. Alberts and anonymous reviewers for helpful comments on an earlier version of the manuscript. This article is based on a doctoral study by M. Eberle in the Faculty of Biology, University of Hamburg, with financial support from the Deutsches Primatenzentrum and Deutsche Forschungsgemeinschaft (Ka 1082/5-1,2).
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Eberle, M., Kappeler, P.M. Sex in the dark: determinants and consequences of mixed male mating tactics in Microcebus murinus, a small solitary nocturnal primate. Behav Ecol Sociobiol 57, 77–90 (2004). https://doi.org/10.1007/s00265-004-0826-1
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DOI: https://doi.org/10.1007/s00265-004-0826-1