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Kin-preferential cooperation, dominance-dependent reproductive skew, and competition for mates in communally nesting female house mice

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Abstract

Little is known about the behavioural mechanisms facilitating kin-preferential communal breeding in wild house mice (Mus domesticus). We evaluated the effect of kinship and male availability on aggression, social structure and reproductive skew in groups of female mice freely interacting and reproducing in semi-natural indoor enclosures. Triplets of either sisters or non-sisters were established in enclosures provided with either one or three littermate males, which were unrelated and unfamiliar to the females. Sisters were more spatially associated and less aggressive than non-sisters, leading to higher incidences of communal breeding and reproduction. This is in agreement with theoretical considerations on kin selection in house mice. Reproductive success was highly skewed in favour of dominant females due to subordinate infertility or complete loss of first litters, which might have been caused by dominant females. In spite of this, subordinates only rarely dispersed from the enclosures, suggesting that perceived dispersal risk generally outweighed relatively reduced reproductive potentials. Aggression levels among females were significantly higher when one male was available, compared to when three males were available. We suggest that this might result from higher female-female competition for mates, due to the risk of missing fertilisation when synchronously oestrous females encounter limited numbers of males in a deme. Our results indicate that, first, communal nursing in house mice might have evolved to ‘make the best out of a bad job’ rather than to enhance offspring fitness; and, second, that female-female mate-competition might play an important role in shaping female social structure in this polygynous mammal.

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References

  • Albers PCH, De Vries H (2001) Elo-Rating as a tool in the sequential estimation of dominance strenghts. Anim Behav 61:489–495

    Article  Google Scholar 

  • Bronson FH (1979) The reproductive ecology of the house mouse. Q Rev Biol 54:265–299

    CAS  PubMed  Google Scholar 

  • Butler RG (1980) Population size, social behaviour, and dispersal in house mice: a quantitative investigation. Anim Behav 28:78–85

    Google Scholar 

  • Cant MA (2000) Social control of reproduction in banded mongooses. Anim Behav 59:147–158

    Article  PubMed  Google Scholar 

  • Cant MA, Johnstone RA (1999) Costly young and reproductive skew in animal societies. Behav Ecol 10:178–184

    Article  Google Scholar 

  • Cant MA, Otali E, Mwanguhya F (2001) Eviction and dispersal in co-operatively breeding banded mongooses (Mungos mungo). J Zool 254:155–162

    Article  Google Scholar 

  • Chapman JC, Christian JJ, Pawlikowski MA, Michael SD (1998) Analysis of steroid hormone levels in female mice at high population density. Physiol Behav 64:529–533

    Article  CAS  PubMed  Google Scholar 

  • Chovnick A, Yasukawa NJ, Monder H, Christian JJ (1987) Female behavior in populations of mice in the presence and absence of male hierarchy. Aggressive Behav 13:367–375

    Google Scholar 

  • De Catanzaro D (1991) Duration of mating relates to fertility in mice. Physiol Behav 50:393–395

    Article  PubMed  Google Scholar 

  • Dewsbury DA (1972) Patterns of copulatory behavior in male mammals. Q Rev Biol 47:1–33

    CAS  PubMed  Google Scholar 

  • Dewsbury DA (1979) Pregnancy and copulatory behavior in random-bred house mice mated in postpartum estrus. Bull Psychonom Soc 13:320–322

    Google Scholar 

  • Dobson FS, Baudoin C (2002) Experimental tests of spatial association and kinship in monogamous mice (Mus spicilegus) and polygynous mice (Mus musculus domesticus). Can J Zool 89:980–986

    Article  Google Scholar 

  • Dobson FS, Jacquot C, Baudoin C (2000) An experimental test of kin association in the house mouse. Can J Zool 78:1806–1812

    Article  Google Scholar 

  • Drews C (1993) The concept and definition of dominance in animal behaviour. Behaviour 125:283–313

    Google Scholar 

  • Drickamer LC (1992) Oestrus female house mice discriminate dominant from subordinate males and sons of dominant from sons of subordinate males by odour cues. Anim Behav 43:869–870

    Google Scholar 

  • Drickamer LC, Gowaty PA, Holmes CM (2000) Free female mate choice in house mice affects reproductive success and offspring viability and performance. Anim Behav 59:371–378

    PubMed  Google Scholar 

  • Drickamer LC, Wagner DM, Robinson AS (2003) Double captures of house mice (Mus musculus) with information on genetic relatedness. Am Mid Nat 150:308–320

    Google Scholar 

  • Eklund A (1997) The major histocompatibility complex and mating preferences in wild house mice (Mus domesticus). Behav Ecol 8:630–634

    Google Scholar 

  • Faulkes CG, Abbott DH, Jarvis JUM (1991) Social suppression of reproduction in male naked mole-rats, Heterocephalus glaber. J Reprod Fertil 91:593–604

    Article  CAS  PubMed  Google Scholar 

  • Ferguson GA (1965) Nonparametric trend analysis. McGill University Press, Montreal

  • Gerlach G (1990) Dispersal mechanisms in a captive wild house mouse population (Mus domesticus Rutty). Biol J Linn Soc Lond 41:271–277

    Google Scholar 

  • Gerlach G (1996) Emigration mechanisms in feral house mice—a laboratory investigation of the influence of social structure, population density, and aggression. Behav Ecol Sociobiol 39:159–170

    Article  Google Scholar 

  • Gerlach G (1998) Impact of social ties on dispersal, reproduction and dominance in feral house mice (Mus musculus domesticus). Ethology 104:487–499

    Google Scholar 

  • Gerlach G, Bartmann S (2002) Reproductive skew, costs, and benefits of cooperative breeding in female wood mice (Apodemus sylvaticus). Behav Ecol 13:408–418

    Article  Google Scholar 

  • Hayashi S (1990) Social condition influences sexual attractiveness of dominant male mice. Zool Sci 7:889–894

    Google Scholar 

  • Hayes LD (2000) To nest communally or not to nest communally: a review of rodent communal nesting and nursing. Anim Behav 59:677–688

    PubMed  Google Scholar 

  • Hoogland JL (1985) Infanticide in prairie dogs: lactating females kill offspring of close kin. Science 230:1037–1040

    Google Scholar 

  • Hurst JL (1987) Behavioural variation in wild house mice Mus domesticus Rutty: a quantitative assessment of female social organization. Anim Behav 35:1846–1857

    Google Scholar 

  • Kareem AM, Barnard CJ (1982) The importance of kinship and familiarity in social interactions between mice. Anim Behav 30:594–601

    Google Scholar 

  • Kareem AM, Barnard CJ (1986) Kin recognition in mice—age, sex and parental effects. Anim Behav 34:1814–1824

    Google Scholar 

  • König B (1989) Behavioural ecology of kin recognition in house mice. Ethol Ecol Evol 1:99–100

    Google Scholar 

  • König B (1993) Maternal investment of communally nursing female house mice (Mus musculus domesticus). Behav Proc 30:61–74

    Article  Google Scholar 

  • König B (1994a) Communal nursing in mammals. Verh Dtsch Zool Ges 87:115–127

    Google Scholar 

  • König B (1994b) Fitness effects of communal rearing in house mice. The role of relatedness versus familiarity. Anim Behav 48:1449–1457

    Article  Google Scholar 

  • Krackow S (1992) Sex ratio manipulation in wild house mice: The effect of fetal resorption in relation to the mode of reproduction. Biol Reprod 47:541–548

    CAS  PubMed  Google Scholar 

  • Krackow S (1997) Effects of mating dynamics and crowding on sex ratio variance in mice. J Reprod Fertil 110:87–90

    Article  CAS  PubMed  Google Scholar 

  • Krackow S (2003) Motivational and heritable determinants of dispersal latency in wild male house mice (Mus musculus musculus). Ethology 109:671–689

    Article  Google Scholar 

  • Krackow S, Tkadlec E (2001) Analysis of brood sex ratios. Behav Ecol Sociobiol 50:293–301

    Article  Google Scholar 

  • Lenington S, Egid K (1989) Environmental influences on the preferences of wild female house mice for males of differing t-complex genotypes. Behav Genet 19:257–266

    CAS  PubMed  Google Scholar 

  • Lidicker WZ (1976) Social behaviour and density regulation in house mice living in large enclosures. J Anim Ecol 45:677–697

    Google Scholar 

  • Lloyd JA (1975) Social structure and reproduction in two freely-growing populations of house mice (Mus musculus L.). Anim Behav 23:413–424

    Google Scholar 

  • Mackintosh JH (1981) Behaviour of the house mouse. Symp Zool Soc Lond 47:337–365

    Google Scholar 

  • Manning CJ, Dewsbury DA, Wakeland EK, Potts WK (1995) Communal nesting and communal nursing in house mice, Mus musculus domesticus. Anim Behav 50:741–751

    Article  Google Scholar 

  • Manning CJ, Wakeland EK, Potts WK (1992) Communal nesting patterns in mice implicate MHC genes in kin recognition. Nature 360:581–583

    CAS  PubMed  Google Scholar 

  • McCullagh P, Nelder JA (1989) Generalized linear models, vol 37, 2nd edn. Chapman and Hall, London

  • Nelson AR, Johnson CL, Matter WJ, Mannan RW (2002) Tests of emigration in small mammals under experimental conditions. Can J Zool 80:2056–2060

    Article  Google Scholar 

  • Noirot E (1969) Serial order of maternal responses in mice. Anim Behav 17:547–550

    CAS  PubMed  Google Scholar 

  • O’Riain MJ, Bennett NC, Brotherton PNM, McIlrath G, Clutton-Brock TH (2000) Reproductive suppression and inbreeding avoidance in wild populations of co-operatively breeding meerkats (Suricata suricatta). Behav Ecol Sociobiol 48:471–477

    Article  Google Scholar 

  • Palanza P, Re L, Mainardi D, Brain PF, Parmigiani S (1996) Male and female competitive strategies of wild house mice pairs (Mus musculus domesticus) confronted with intruders of different sex and age in artificial territories. Behaviour 133:863–882

    Google Scholar 

  • Parmigiani S, Mainardi M, Brain PF, Haug M, Brunoni V (1989) Variation in aggressive behavior and anatomo-physiological correlates generated by crowding without physical contact in the house mouse. Aggressive Behav 15:191–200

    Google Scholar 

  • Pennycuik PR, Johnston PG, Westwood NH, Reisner AH (1986) Variation in numbers in a house mouse population housed in a large outdoor enclosure: seasonal fluctuations. J Anim Ecol 55:371–379

    Google Scholar 

  • Reimer JD, Petras ML (1967) Breeding structure of the house mouse, Mus musculus, in a population cage. J Mammal 48:88–99

    CAS  PubMed  Google Scholar 

  • Rolland C, Macdonald DW, De Fraipont M, Berdoy M (2003) Free female choice in house mice: leaving best for last. Behaviour 140:1371–1388

    Article  Google Scholar 

  • SAS (1989) SAS/STAT User’s guide: version 6. SAS Institute, Cary, N.C.

  • Singleton GR, Hay DA (1983) The effect of social organization on reproductive success and gene flow in colonies of wild house mice, Mus musculus. Behav Ecol Sociobiol 12:49–56

    Google Scholar 

  • Whitten WK (1956) Modification of the oestrous cycle of the mouse by external stimuli associated with the male. J Endocrinol 13:399–404

    CAS  PubMed  Google Scholar 

  • Wilkinson GS, Baker MAE (1988) Communal nesting among genetically similar house mice. Ethology 77:103–114

    Google Scholar 

  • Wolff RJ (1985) Mating behavior and female choice: their relation to social structure in wild caught house mice (Mus musculus) housed in a semi-natural environment. J Zool (Lond) 207:43–51

    Google Scholar 

  • Yamazaki K, Boyse EA, Mike V, Thaler HT, Mathieson BJ, Abbott J, Boyse (1976) Control of mating preferences in mice by genes in the major histocompatability complex. J Exp Med 144:1324–1335

    CAS  PubMed  Google Scholar 

  • Yasukawa NJ, Monder H, Leff FR, Christian JJ (1985) Role of female behavior in controlling population growth in mice. Aggressive Behav 11:49–64

    Google Scholar 

  • Zegeren K van (1980) Variation in aggressiveness and the regulation of numbers in house mouse populations. Neth J Zool 30:635–770

    Google Scholar 

Download references

Acknowledgements

We thank Barbara König, Lee Drickamer, Alan McElligott and three anonymous reviewers for many useful comments on the manuscript. This research was funded by the Swiss National Foundation (SNF; no. 31-59609.99): Support to S.K. was granted by the German Research Council (DFG; KR1290/6). Animal experimentation was approved by the Swiss Animal Experimentation Commission (Kantonale Tierversuchskommission; no. 164/99).

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Correspondence to Alina S. Rusu.

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Communicated by F. Trillmich

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Rusu, A.S., Krackow, S. Kin-preferential cooperation, dominance-dependent reproductive skew, and competition for mates in communally nesting female house mice. Behav Ecol Sociobiol 56, 298–305 (2004). https://doi.org/10.1007/s00265-004-0787-4

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