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Microsatellite length polymorphisms associated with dispersal-related agonistic onset in male wild house mice (Mus musculus domesticus)

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Abstract

Dispersal propensity, reflecting one of the most decisive mammalian life history traits, has been suggested to vary heritably and to locally adapt to prevailing dispersal conditions in wild house mouse populations. Because individual dispersal propensity highly significantly covaries with the developmental timing of the onset of agonistic interactions between littermate brothers, we used agonistic onset as an endophenotype to explore the potential genetic basis of dispersal-related behavioral variation in male house mice. We found significant covariation of microsatellite marker compositions with the probability of fraternal pairs to exhibit agonistic relationships before the age of 2 months. In particular, the presence of two alleles associated with a serotonin transporter protein gene (Slc6a4) and a testosterone dehydrogenase gene (Cyp3a11), respectively, strongly covaried with the probability of early agonistic onset. These results are congruent with recent findings of microsatellite length polymorphisms marking regulatory variation of gene expression that is relevant for social behavior, including dispersal propensity development, in other mammals. Genetic variability for ontogenetic timing of agonistic onset would be in agreement with genotypic differentiation of the dispersive behavioral syndrome in natural populations that could lead to local adaptation.

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References

  • Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225

    Article  PubMed  Google Scholar 

  • Cheung VG, Spielman RS, Ewen KG, Weber TM, Morley M, Burdick JT (2005) Mapping determinants of human gene expression by regional and genome-wide association. Nature 437:1365–1369

    Article  PubMed  CAS  Google Scholar 

  • Clobert J, Danchin E, Dhondt AA, Nichols JD (2001) Dispersal. Oxford University Press, Oxford

    Google Scholar 

  • Compaan JC, Hutchison JB, Wozniak A, Deruiter AJH, Koolhaas JM (1994) Brain aromatase activity and plasma testosterone levels are elevated in aggressive male mice during early ontogeny. Dev Brain Res 82:185–192

    Article  CAS  Google Scholar 

  • Contente A, Dittmer A, Koch MC, Roth J, Dobbelstein M (2002) A polymorphic microsatellite that mediates induction of PIG3 by p53. Nature Genet 30:315–320

    Article  PubMed  Google Scholar 

  • Corti M, Rohlf FJ (2001) Chromosomal speciation and phenotypic evolution in the house mouse. Biol J Linn Soc 73:99–112

    Article  Google Scholar 

  • Gaines MS, McClenaghan LR (1980) Dispersal in mammals. Ann Rev Ecol Syst 11:163–169

    Article  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 39:159–70

    Article  Google Scholar 

  • Goldstein DB, Schlötterer C (1999) Microsatellites. Evolution and applications. Oxford University Press, Oxford

    Google Scholar 

  • Gottesman II, Gould TD (2003) The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry 160:636–645

    Article  PubMed  Google Scholar 

  • Grafen A, Hails R (2002) Modern statistics for the life sciences. Oxford University Press, Oxford

    Google Scholar 

  • Hammock EAD, Young LJ (2004) Functional microsatellite polymorphism associated with divergent social structure in vole species. Mol Biol Evol 21:1057–1063

    Article  PubMed  CAS  Google Scholar 

  • Hammock EAD, Young LJ (2005) Microsatellite instability generates diversity in brain and sociobehavioral traits. Science 308:1630–1634

    Article  PubMed  CAS  Google Scholar 

  • Hovatta I, Tennant RS, Helton R, Marr RA, Singer O, Redwine JM, Ellison JA, Schadt EE, Verma IM, Lockhart DJ, Barlow C (2005) Glyoxalase 1 and glutathione reductase 1 regulate anxiety in mice. Nature 438:662–666

    Article  PubMed  CAS  Google Scholar 

  • Ims RA, Hjermann DØ (2001) Condition-dependent dispersal. Disperal. Oxford University Press, Oxford, pp 203–216

    Google Scholar 

  • Insel TR, Wang ZX, Ferris CF (1994) Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J Neurosci 14:5381–5392

    PubMed  CAS  Google Scholar 

  • Kisdi É (2002) Dispersal: risk spreading versus local adaptation. Am Nat 159:579–596

    Article  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 (2005) Agonistic onset during development differentiates wild house mouse males (Mus domesticus). Naturwissenschaften 92:78–81

    Article  PubMed  CAS  Google Scholar 

  • Lank DB (1995) Genetic polymorphism for alternative mating behaviour in lekking male ruff, Phylomachus pugnax. Nature 378:59–62

    Article  CAS  Google Scholar 

  • Lesch KP, Meyer J, Glatz K, Flugge G, Hinney A, Hebebrand J, Klauck SM, Poustka A, Poustka F, Bengel D, Mossner R, Riederer P, Heils A (1997) The 5-HT transporter gene-linked polymorphic region (5-HTTLPR) in evolutionary perspective: alternative biallelic variation in rhesus monkeys. J Neural Transm 104:1259–1266

    Article  PubMed  CAS  Google Scholar 

  • Lim MM, Wang Z, Olazábal DE, Ren X, Terwilliger EF, Young LJ (2004) Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature 429:754–757

    Article  PubMed  CAS  Google Scholar 

  • Müllenbach R, Lagoda PJL, Welter C (1989) An efficient salt-chlorophorm extraction of DNA from blood and tissues. Trends Genet 5:391

    PubMed  Google Scholar 

  • O’Riain MJ, Jarvis JUM, Faulkes CG (1996) A dispersive morph in the naked mole-rat. Nature 380:619–621

    Article  PubMed  CAS  Google Scholar 

  • Parvinen K, Dieckmann U, Gyllenberg M, Metz JAJ (2003) Evolution of dispersal in metapopulations with local density dependence and demographic stochasticity. J Evol Biol 16:143–153

    Article  PubMed  CAS  Google Scholar 

  • Piálek J, Hauffe HC, Searle JB (2005) Chromosomal variation in the house mouse. Biol J Linn Soc 84:535–563

    Article  Google Scholar 

  • Pocock MJO, Hauffe HC, Searle JB (2005) Dispersal in house mice. Biol J Linn Soc 84:565–583

    Article  Google Scholar 

  • Pulido F, Berthold P, Mohr G, Querner U (2001) Heritability of the timing of autumn migration in a natural bird population. Proc R Soc Lond B 268:953–959

    Article  CAS  Google Scholar 

  • Rifkin SA, Houle D, Kim J, White KP (2005) A mutation accumulation assay reveals a broad capacity for rapid evolution of gene expression. Nature 438:220–223

    Article  PubMed  CAS  Google Scholar 

  • Rosenbrock H, Hagemeyer CE, Singec I, Knoth R, Volk B (1999) Testosterone metabolism in rat brain is differentially enhanced by phenytoin-inducible Cytochrome P450 isoforms. J Neurosci 11:597–604

    CAS  Google Scholar 

  • Rusu AS, Krackow S (2005) Agonistic onset marks emotional changes and dispersal propensity in wild house mouse males (Mus domesticus). J Comp Psychol 119:58–66

    Article  PubMed  Google Scholar 

  • Scantlebury M, Speakman JR, Oosthuizen MK, Roper TJ, Bennett NC (2006) Energetics reveals physiologically distinct castes in a eusocial mammal. Nature 440:795–797

    Article  PubMed  CAS  Google Scholar 

  • Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79:241–277

    Article  PubMed  Google Scholar 

  • Sinervo B, Clobert J (2003) Morphs, dispersal behavior, genetic similarity, and the evolution of cooperation. Science 300:1949–1951

    Article  PubMed  CAS  Google Scholar 

  • Sinervo B, Bleay C, Adamopoulou C (2001) Social causes of correlational selection and the resolution of a heritable throat color polymorphism in a lizard. Evolution 55:2040–2052

    PubMed  CAS  Google Scholar 

  • Stenseth NC, Lidicker WZ (1992) Animal dispersal. Small mammals as a model. Chapman & Hall, London

    Google Scholar 

  • Trefilov A, Berard J, Krawczak M, Schmidtke J (2000) Natal dispersal in rhesus macaques is related to serotonin transporter gene promoter variation. Behav Genet 30:295–301

    Article  PubMed  CAS  Google Scholar 

  • Wolf JB, Frankino WA, Agrawal AF, Brodie ED, Moore AJ (2001) Developmental interactions and the constituents of quantitative variation. Evolution 55:232–245

    PubMed  CAS  Google Scholar 

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Acknowledgment

We are greatly indebted to E. ‘Garby’ Garbely, eventually transformed into Jari ‘The Lucky Man’ Garbely, who performed the microsatellite typing in our group, and Gerald Kerth for the genetics lab work supervision. Alan G. McElligott kindly reviewed the English. Financial support from German Research Foundation (Heisenberg programme KR1290/6), Swiss National Science Foundation (research grant 3100-59609), and Julius-Klaus-Stiftung Zürich is kindly acknowledged. The experiments were done under approval of the Kantonales Veterinäramt, Zürich, license numbers 164/99 and 127/2002.

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  1. Sven Krackow

    Present address: Institut für Biologie, Humboldt-Universität zu Berlin, Invalidenstrasse 43, 10115, Berlin, Germany

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  1. Zoologisches Institut, Universität Zürich, Winterthurerstrasse 190, 8057, Zürich, Switzerland

    Sven Krackow & Barbara König

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  1. Sven Krackow
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  2. Barbara König
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Correspondence to Sven Krackow.

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Communicated by G. Wilkinson

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Krackow, S., König, B. Microsatellite length polymorphisms associated with dispersal-related agonistic onset in male wild house mice (Mus musculus domesticus). Behav Ecol Sociobiol 62, 813–820 (2008). https://doi.org/10.1007/s00265-007-0507-y

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  • DOI: https://doi.org/10.1007/s00265-007-0507-y

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