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Extra-pair paternity and the evolution of testis size in a behaviorally monogamous tropical mammal, the large treeshrew (Tupaia tana)

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Abstract

Monogamy is rare in mammals (<5% spp.) but occurs in greater frequency among primates (15%) and their close relatives, the treeshrews (100%; Order: Scandentia). Two genetic studies of parentage in monogamous primates revealed high rates of extra-pair paternity (EPP), but to date parentage has not been studied in a treeshrew species. I analyzed the genetic parentage of 22 offspring from two populations of large treeshrews in Sabah, Malaysia (NE Borneo), using seven autosomal microsatellite loci and one mitochondrial DNA marker. Half of these offspring were sired by males that were not the presumed partner of the mother (50% EPP), and three litters exhibited evidence of multiple paternity. However, comparative analysis indicated that the high rate of EPP in Tupaia tana is not associated with intense sperm competition. Relative testis size of treeshrews was similar to testis size in 22 primate species with uni-male mating systems but smaller than 44 primates with multi-male mating systems. After factoring out the effects of body size and phylogeny, I also found that the evolution of multi-male mating systems was significantly associated with the evolution of larger testis size. Male–female pairs of T. tana occupy joint territories but forage and sleep alone (“dispersed pair-living”), and I argue that this form of behavioral monogamy renders mate guarding ineffective. The adaptive advantages of behavioral monogamy likely differ from the advantages driving EPP in large treeshrews. However, small testis size suggests that behavioral monogamy is not masking a dispersed multi-male mating system in this species.

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References

  • Albrecht T, Kreisinger J, Pialek J (2006) The strength of direct selection against female promiscuity is associated with rates of extrapair fertilizations in socially monogamous songbirds. Am Nat 167:739–744

    Article  PubMed  Google Scholar 

  • Arnason U, Adegoke J, Bodin K, Born E, Esa Y, Gullberg A, Nilsson M, Short R, Xu X, Janke A (2002) Mammalian mitogenomic relationships and the root of the eutherian tree. Proc Natl Acad Sci USA 99:8151–8156

    Article  PubMed  CAS  Google Scholar 

  • Arnqvist G, Kirkpatrick M (2005) The evolution of infidelity in socially monogamous passerines: the strength of direct and indirect selection on extrapair copulation behavior in females. Am Nat 165:S26–S37

    Article  PubMed  Google Scholar 

  • Brotherton P, Komers P (2003) Mate guarding and the evolution of social monogamy in mammals. In: Reichard U, Boesch C (eds) Monogamy: mating strategies and partnerships in birds, humans and other mammals. Cambridge University Press, Cambridge, UK, pp 42–58

    Google Scholar 

  • Brotherton P, Manser M (1997) Female dispersion and the evolution of monogamy in the dik-dik. Anim Behav 54:1413–1424

    Article  PubMed  Google Scholar 

  • Brotherton P, Rhodes A (1996) Monogamy without biparental care in a dwarf antelope. Proc R Soc Lond B 263:23–29

    Article  CAS  Google Scholar 

  • Carter C, DeVries A, Getz L (1995) Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci Biobehav Rev 19:303–314

    Article  PubMed  CAS  Google Scholar 

  • Cohas A, Yoccoz N, Da Silva A, Goossens B, Allaine D (2006) Extra-pair paternity in the monogamous alpine marmot (Marmota marmota): the role of social setting and female mate choice. Behav Ecol Sociobiol 59:597–605

    Article  Google Scholar 

  • Dakin E, Avise J (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504–509

    Article  PubMed  CAS  Google Scholar 

  • Dietz J (1984) Ecology and social organization of the maned wolf (Chrysocyon brachyurus). Smithson Contrib Zool 392:1–51

    Google Scholar 

  • Eberle M, Kappeler P (2004a) Selected polyandry: female choice and inter-sexual conflict in a small nocturnal solitary primate (Microcebus murinus). Behav Ecol Sociobiol 57:91–100

    Article  Google Scholar 

  • Eberle M, Kappeler P (2004b) Sex in the dark: determinants and consequences of mixed male mating tactics in Microcebus murinus, a small nocturnal primate. Behav Ecol Sociobiol 57:77–90

    Article  Google Scholar 

  • Emmons L (2000) Tupai: a field study of Bornean Treeshrews. University of California Press, Los Angeles

    Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Fietz J, Zischler H, Schwiegk C, Tomiuk J, Dausmann K, Ganzhorn J (2000) High rates of extra-pair young in the pair-living fat-tailed dwarf lemur, Cheirogaleus medius. Behav Ecol Sociobiol 49:8–17

    Article  Google Scholar 

  • Fleischer R, Tarr C, Morton E, Sangmeister A, Derrickson K (1997) Mating system of the dusky antbird, a tropical passerine, as assessed by DNA fingerprinting. The Condor 99:512–514

    Article  Google Scholar 

  • Foerster K, Delhey K, Johnsen A, Lifjeld J, Kempenaers (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717

    Article  PubMed  CAS  Google Scholar 

  • Gage M, Freckleton R (2003) Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length. Proc R Soc Lond B 270:625–632

    Article  Google Scholar 

  • Girman D, Mills M, Geffen E, Wayne R (1997) A molecular genetic analysis of social structure, dispersal, and interpack relationships of the African wild dog (Lycaon pictus). Behav Ecol Sociobiol 40:187–198

    Article  Google Scholar 

  • Goossens B, Graziani L, Waits LP, Farand E, Magnolon S, Coulon J, Bel M-C, Taberlet P, Allaine D (1998) Extra-pair paternity in the monogamous Alpine marmot revealed by nuclear DNA microsatellite analysis. Behav Ecol Sociobiol 43:281–288

    Article  Google Scholar 

  • Griffith S (2000) High fidelity on islands: a comparative study of extrapair paternity in passerine birds. Behav Ecol 11:265–273

    Article  Google Scholar 

  • Griffith S, Owens I, Thuman K (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212

    Article  PubMed  CAS  Google Scholar 

  • Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harcourt A, Purvis A, Liles L (1995) Sperm competition: mating system, not breeding season, affects testes size of primates. Funct Ecol 9:468–476

    Article  Google Scholar 

  • Hosken D (1998) Testes mass in megachiropteran bats varies in accordance with sperm competition theory. Behav Ecol Sociobiol 44:169–177

    Article  Google Scholar 

  • Isvaran K, Clutton-Brock T (2007) Ecological correlates of extra-group paternity in mammals. Proc R Soc Lond B 274:219–224

    Article  Google Scholar 

  • Johnsen A, Andersen V, Sunding C, Lifjeld J (2000) Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature 406:296–299

    Article  PubMed  CAS  Google Scholar 

  • Kalinowski S, Taper M (2006) Maximum likelihood estimation of the frequency of null alleles at microsatellite loci. Conservation Genetics 7:991–995

    Article  CAS  Google Scholar 

  • Kalinowski S, Wagner A, Taper M (2006) ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6:576–579

    Article  CAS  Google Scholar 

  • Kappeler P (1997) Intrasexual selection and testis size in stepsirrhine primates. Behav Ecol 8:10–19

    Article  Google Scholar 

  • Kitchen A, Gese E, Waits L, Karki S, Schauster E (2006) Multiple breeding strategies in the swift fox, Vulpes velox. Anim Behav 71:1029–1038

    Article  Google Scholar 

  • Kleiman DG (1977) Monogamy in mammals. Q Rev Biol 52:39–69

    Article  PubMed  CAS  Google Scholar 

  • Kleiman D, Malcolm J (1981) The evolution of male parental investment in mammals. In: Gubernick D, Klopfer P (eds) Parental Care in Mammals. Plenum, New York, pp 347–387

    Google Scholar 

  • Komers P, Brotherton P (1997) Female space use is the best predictor of monogamy in mammals. Proc R Soc London B 264:1261–1270

    Article  CAS  Google Scholar 

  • Lack D (1968) Ecological adaptations for breeding in birds. Methuen, London

    Google Scholar 

  • Marshall T, Slate J, Kruuk L, Pemberton J (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  PubMed  CAS  Google Scholar 

  • Martin R (1966) Tree shrews: unique reproductive mechanism of systematic importance. Science 152:1402–1404

    Article  PubMed  CAS  Google Scholar 

  • Martin R (1968) Reproduction and ontogeny in tree-shrews (Tupaia belangeri), with reference to their general behaviour and taxonomic relationships. Zeitschrift für Tierpyschologie 25:409–496, 505–532

    CAS  Google Scholar 

  • McCracken G, Wilkinson G (2000) Bat mating systems. In: Crichton E, Krutzsch P (eds) Reproductive biology of bats. Academic, New York, pp 321–362

    Google Scholar 

  • Milligan B (2003) Maximum-likelihood estimation of relatedness. Genetics 163:1153–1167

    PubMed  Google Scholar 

  • Müller A, Thalmann U (2000) Origin and evolution of primate social organisation: a reconstruction. Biol Rev 75:405–435

    Article  PubMed  Google Scholar 

  • Munshi-South J (2006) Asocial monogamy, extra-pair paternity, and dispersal in the large treeshrew (Tupaia tana). Ph.D. Dissertation, University of Maryland, College Park, MD. freely available at http://hdl.handle.net/1903/3467

  • Munshi-South J, Wilkinson G (2006) Isolation and characterization of polymorphic microsatellite loci in Bornean treeshrews (Tupaia spp.). Mol Ecol Notes 6:698–699

    Article  CAS  Google Scholar 

  • Munshi-South J, Emmons L, Bernard H (2007) Behavioral monogamy and fruit availability in the large treeshrew (Tupaia tana) in Sabah, Malaysia. Journal of Mammalogy (in press)

  • Murphy W, Eizirik E, Johnson W, Zhang Y, Ryder O, O’Brien S (2001) Molecular phylogenetics and the origins of placental mammals. Nature 409:614–618

    Article  PubMed  CAS  Google Scholar 

  • Parker G, Ball M, Stockley P, Gage M (1997) Sperm competition games: a prospective analysis of risk assessment. Proc R Soc Lond B 264:1793–1802

    Article  CAS  Google Scholar 

  • Petrie M, Doums C, Moller A (1998) The degree of extra-pair paternity increases with genetic variability. Proc Natl Acad Sci USA 95:9390–9395

    Article  PubMed  CAS  Google Scholar 

  • Purvis A (1995) A composite estimate of primate phylogeny. Philos Trans R Soc Lond B 348:405–421

    Article  CAS  Google Scholar 

  • Purvis A, Rambaut A (1995) Comparative analysis by independent contrasts (CAIC): an apple Macintosh application for analysing comparative data. Comput Appl Biosci 11:247–251

    PubMed  CAS  Google Scholar 

  • Purvis A, Webster A (1999) Phylogenetically independent comparisons and primate phylogeny. In: Lee P (ed) Comparative primate socioecology. Cambridge University Press, Cambridge, UK, pp 44–70

    Google Scholar 

  • Rathbun G (1979) The social structure and ecology of elephant-shrews. Adv Ethol 20:1–79

    Google Scholar 

  • Rathbun G, Rathbun C (2006) Social structure of the bushveld sengi (Elephantulus intufi) in Namibia and the evolution of monogamy in the Macroscelidea. J Zool 269:391–399

    Article  Google Scholar 

  • Reichard U (1995) Extra-pair copulations in a monogamous gibbon (Hylobates lar). Ethology 100:99–112

    Article  Google Scholar 

  • Reichard U (2003) Monogamy: past and present. In: Reichard U, Boesch C (eds) Monogamy: mating strategies and partnerships in birds, humans and other mammals. Cambridge University Press, Cambridge, pp 3–26

    Google Scholar 

  • Ribble D (2003) The evolution of social and reproductive monogamy in Peromyscus: evidence from Peromyscus californicus (the California mouse). In: Reichard U, Boesch C (eds) Monogamy: mating strategies and partnerships in birds, humans and other mammals. Cambridge University Press, Cambridge, pp 81–92

    Google Scholar 

  • Roemer G, Smith D, Garcelon D, Wayne R (2001) The behavioural ecology of the island fox (Urocyon littoralis). J Zool 255:1–14

    Article  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana, Totowa, NJ, pp 365–386

    Google Scholar 

  • SAS Institute (2003) JMP 5.0.1.2. SAS Institute, Cary, NC

    Google Scholar 

  • Schmitz J, Ohme M, Zischler H (2000) The complete mitochondrial genome of Tupaia belangeri and the phylogenetic affiliation of scandentia to other eutherian orders. Mol Biol Evol 17:1334–1343

    PubMed  CAS  Google Scholar 

  • Schmoll T, Dietrich V, Winkel W, Epplen J, Lubjuhn T (2003) Long-term fitness consequences of female extra-pair matings in a socially monogamous passerine. Proc R Soc Lond B 270:259–264

    Article  Google Scholar 

  • Schülke O (2005) Evolution of pair-living in Phaner furcifer. Int J Primatol 26:903–919

    Article  Google Scholar 

  • Schülke O, Ostner J (2005) Big times for dwarfs: social organization, sexual selection, and cooperation in the Cheirogaleidae. Evol Anthropol 14:170–185

    Article  Google Scholar 

  • Schülke O, Kappeler P, 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

    Article  Google Scholar 

  • Sheldon B, Merila J, Qvarnstrom A, Gustafsson L, Ellegren H (1997) Paternal genetic contribution to offspring condition predicted by size of male secondary sexual character. Proc R Soc Lond B 264:297–302

    Article  Google Scholar 

  • Slate J, Marshall T, Pemberton J (2000) A retrospective assessment of the accuracy of the paternity inference program CERVUS. Mol Ecol 9:801–808

    Article  PubMed  CAS  Google Scholar 

  • Solomon N, Keane B, Knoch L, Hogan P (2004) Multiple paternity in socially monogamous prairie voles (Microtus ochrogaster). Can J Zool 82:1667–1671

    Article  Google Scholar 

  • Sommer S, Tichy H (1999) Major histocompatibility complex (MHC) class II polymorphism and paternity in the monogamous Hypogeomys antimena, the endangered, largest endemic Malagasy rodent. Mol Ecol 8:1259–1272

    Article  PubMed  CAS  Google Scholar 

  • Spencer P, Horsup A, Marsh H (1998) Enhancement of reproductive success through mate choice in a social rock-wallaby, Petrogale assimilis (Macropodidae) as revealed by microsatellite markers. Behav Ecol Sociobiol 43:1–9

    Article  Google Scholar 

  • Stutchbury B, Morton E (1995) The effect of breeding synchrony on extra-pair mating systems in songbirds. Behaviour 132:675–690

    Google Scholar 

  • Stutchbury B, Morton E (2001) Behavioral ecology of tropical birds. Academic, New York

    Google Scholar 

  • Trivers R (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago

    Google Scholar 

  • van Schaik C, Kappeler P (2003) The evolution of social monogamy in primates. In: Reichard U, Boesch C (eds) Monogamy: mating strategies and partnerships in birds, humans and other mammals. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Vos R, Moores A (2007) A dated MRP supertree for the order Primates. Systematic Biology (in press)

  • Wolff J, Macdonald D (2004) Promiscuous females protect their offspring. Trends Ecol Evol 19:127–134

    Article  PubMed  Google Scholar 

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Acknowledgments

I am very grateful to the Economic Planning Unit of Malaysia and the Danum Valley Management Committee for permission to work in protected areas in Sabah; the Royal Society Southeast Asian Rainforest Research Programme, and especially Glen Reynolds, for substantial logistical support; the Animal Behavior Society, the University of Maryland Center for Biodiversity and Biology of Small Populations Research Training Grant, the Cleveland Zoological Society, Sigma Xi, the American Society of Mammalogists, and the Explorers Club for research funds; Jo Annah Jensen, Kenny Johnius, Adriene Leong, Tracy Misiewicz, Ronie E. Sham, Philip Ulok, and the staff of the Sabah Biodiversity Experiment for excellent field assistance; and to Devra Kleiman, Jerry Wilkinson, Charlie Nunn, and three anonymous reviewers for constructive comments on the manuscript. This work complies with all current laws governing research in both Malaysia and the USA.

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  1. Jason Munshi-South

    Present address: Department of Natural Sciences, Baruch College, City University of New York, 17 Lexington Avenue, New York, NY, 10010, USA

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  1. Program in Behavior, Ecology, Evolution and Systematics (BEES), Department of Biology, University of Maryland, College Park, MD, 20742, USA

    Jason Munshi-South

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Communicated by: C. Nunn

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Munshi-South, J. Extra-pair paternity and the evolution of testis size in a behaviorally monogamous tropical mammal, the large treeshrew (Tupaia tana). Behav Ecol Sociobiol 62, 201–212 (2007). https://doi.org/10.1007/s00265-007-0454-7

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  • DOI: https://doi.org/10.1007/s00265-007-0454-7

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