Skip to main content

Advertisement

Log in

Genetic relatedness and space use in a behaviorally flexible species of marmot, the woodchuck (Marmota monax)

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Solitary species show several patterns of space use and relatedness. Individuals may associate randomly or may live near female or male kin, often as a result of natal philopatry or dispersal patterns. Although usually described as solitary or asocial, woodchucks (Marmota monax) are behaviorally flexible marmots that exhibit greater sociality in some populations than others. I examined relationships between kinship, geographic distance, and home range overlap, as well as dispersal and philopatry, to determine the extent to which kin associated spatially. I used a combination of microsatellite DNA analysis, long-term behavioral observations, and radiotelemetry to test predictions that females, but not males, would associate with kin. Indeed, woodchucks lived closer and shared a greater proportion of their home range with more closely related animals. Overlap of females' and males' home ranges was positively correlated with kinship, and male–female dyads shared more area with closer kin. Most juveniles delayed dispersal beyond their first summer. Females often remained philopatric and settled near their natal range. Although males often dispersed as yearlings, some males also established territories within or immediately adjacent to their natal home ranges. A combination of factors can explain these spatial patterns, including high population density associated with the study site's location within a suburban environment, high dispersal costs, and abundant food. Thus, despite their asocial and solitary reputation, woodchucks displayed spatial patterns seen in other, more social species of ground-dwelling sciurids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Allainé D (2000) Sociality, mating system and reproductive skew in marmots: evidence and hypotheses. Behav Proc 51:21–34

    Article  Google Scholar 

  • Armitage KB (1981) Sociality as a life-history tactic of ground squirrels. Oecologia 48:36–49

    Article  Google Scholar 

  • Armitage KB (1986) Individuality, social behavior, and reproductive success in yellow-bellied marmots. Ecology 67:1186–1193

    Article  Google Scholar 

  • Armitage KB (1991) Social and population dynamics of yellow-bellied marmots: long term research. Annu Rev Ecol Syst 22:379–407

    Article  Google Scholar 

  • Armitage KB (1996a) Resource sharing and kinship in yellow-bellied marmots. In: Le Berre M, Ramousse R, Le Guelte L (eds) Biodiversity in marmots. International Network on Marmots, Moscow, pp 129–134

    Google Scholar 

  • Armitage KB (1996b) Social dynamics, kinship and population dynamics of marmots. In: Le Berre M, Ramousse R, Le Guelte L (eds) Biodiversity in marmots. International Network on Marmots, Moscow, pp 113–128

    Google Scholar 

  • Armitage KB (1999) Evolution of sociality in marmots. J Mammal 80:1–10

    Article  Google Scholar 

  • Armitage KB (2000) The evolution, ecology and systematics of marmots. Oecologia Montana 9:1–18

    Google Scholar 

  • Armitage KB (2003) Marmots. In: Feldhamer GA, Chapman JA (eds) Wild mammals of North America: Biology, management, and conservation. Johns Hopkins University Press, Baltimore, pp 188–210

    Google Scholar 

  • Armitage KB (2004) Lifetime reproductive success of territorial male yellow-bellied marmots. Oecologia Montana 13:28–34

    Google Scholar 

  • Arnold W, Dittami J (1997) Reproductive suppression in male marmots. Anim Behav 53:53–66

    Article  Google Scholar 

  • Balloux F, Goudet J, Perrin N (1998) Breeding system and genetic variance in the monogamous, semi-social shrew, Crocidura russula. Evolution 52:1230–1235

    Article  Google Scholar 

  • Barash DP (1989) Marmots: social behavior and ecology. Stanford University Press, Stanford

    Google Scholar 

  • Blumstein DT, Armitage KB (1998) Life history consequences of social complexity: a comparative study of ground-dwelling sciurids. Behav Ecol 9:8–19

    Article  Google Scholar 

  • Blumstein DT, Armitage KB (1999) Cooperative breeding in marmots. Oikos 84:369–382

    Article  Google Scholar 

  • Blundell GM, Ben-David M, Groves P, Bowyer RT, Geffen E (2002) Characteristics of sex-biased dispersal and gene flow in coastal river otters: implications for natural recolonization of extirpated populations. Molec Ecol 11:289–303

    Article  CAS  Google Scholar 

  • Blundell GM, Ben-David M, Groves P, Bowyer RT, Geffen E (2004) Kinship and sociality in coastal river otters: are they related? Behav Ecol 15:705–714

    Article  Google Scholar 

  • Bronson FH (1963) Some correlates of interaction rate in natural populations of woodchucks. Ecology 44:637–643

    Article  Google Scholar 

  • Bronson FH (1964) Agonistic behaviour in woodchucks. Anim Behav 12:470–478

    Article  Google Scholar 

  • Broquet T, Petit E (2004) Quantifying genotyping errors in noninvasive population genetics. Molec Ecol 13:3601–3608

    Article  CAS  Google Scholar 

  • Burton C, Krebs CJ (2003) Influence of relatedness on snowshoe hare spacing behavior. J Mammal 84:1100–1111

    Article  Google Scholar 

  • Cole LC (1949) The measurement of interspecific association. Ecology 30:411–424

    Article  Google Scholar 

  • Costello CM, Creel SR, Kalinowski ST, Vu NV, Quigley HB (2008) Sex-biased natal dispersal and inbreeding avoidance in American black bears as revealed by spatial genetic analyses. Molec Ecol 17:4713–4723

    Article  Google Scholar 

  • Csillery K, Johnson T, Beraldi D, Clutton-Brock T, Coltman D, Hansson B, Spong G, Pemberton JM (2006) Performance of marker-based relatedness estimators in natural populations of outbred vertebrates. Genetics 173:2091–2101

    Article  PubMed  CAS  Google Scholar 

  • Cutrera AP, Lacey EA, Busch C (2005) Genetic structure in a solitary rodent (Ctenomys talarum): implications for kinship and dispersal. Molec Ecol 14:2511–2523

    Article  CAS  Google Scholar 

  • da Silva A, Luikart G, Allaine D, Gautier P, Taberlet P, Pompanon F (2003) Isolation and characterization of microsatellites in European alpine marmots (Marmota marmota). Molec Ecol Notes 3:189–190

    Article  CAS  Google Scholar 

  • de Ruiter JR, Geffen E (1998) Relatedness of matrilines, dispersing males and social groups in long-tailed macaques (Macaca fascicularis). Proc R Soc Lond B Biol Sci 265:79–87

    Article  Google Scholar 

  • DeVos A, Gillespie DI (1960) A study of woodchucks on an Ontario farm. Can Field-Nat 74:130–145

    Google Scholar 

  • Ferron J (1996) How do woodchucks (Marmota monax) cope with harsh winter conditions? J Mammal 77:412–416

    Article  Google Scholar 

  • Ferron J, Ouellet JP (1989) Temporal and intersexual variations in the use of space with regard to social organization in the woodchuck (Marmota monax). Can J Zool 67:1642–1649

    Article  Google Scholar 

  • Fredsted T, Schierup MH, Groeneveld LF, Kappeler PM (2007) Genetic structure, lack of sex-biased dispersal and behavioral flexibility in the pair-living fat-tailed dwarf lemur, Cheirogaleus medius. Behav Ecol Sociobiol 61:943–954

    Article  Google Scholar 

  • Girman DJ, Mills MGL, Geffen E, Wayne RK (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, Coulon J, Allaine D, Graziani L, Bel M-C, Taberlet P (1996) Immigration of a pregnant female in an alpine marmot family group: behavioural and genetic data. C.R. Acad. Sci. Paris Sciences de la vie 319:241–246

    CAS  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 

  • Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162

    Article  Google Scholar 

  • Griffin AS, West SA (2002) Kin selection: fact and fiction. Trends Ecol Evol 17:15–21

    Article  Google Scholar 

  • Grizzell RAJ (1955) A study of the southern woodchuck, Marmota monax monax. Am Midl Nat 53:257–293

    Article  Google Scholar 

  • Hacklander K, Mostl E, Arnold W (2003) Reproductive suppression in female alpine marmots, Marmota marmota. Anim Behav 65:1133–1140

    Article  Google Scholar 

  • Hamilton WJ Jr (1934) The life history of the rufescent woodchuck, Marmota monax rufescens Howell. Ann Carnegie Mus 23:85–167

    Google Scholar 

  • Hanslik S, Kruckenhauser L (2000) Microsatellite loci for two European sciurid species (Marmota marmota and Spermophilus citellus). Molec Ecol 9:2163–2165

    Article  CAS  Google Scholar 

  • Hare JF, Murie JO (2007) Ecology, kinship, and ground squirrel sociality: insights from comparative analysis. In: Wolff JO, Sherman PW (eds) Rodent societies: an ecological and evolutionary perspective. University of Chicago Press, Chicago, pp 345–355

    Google Scholar 

  • Hartl DL, Clark AG (1997) Principles of population genetics, 3rd edn. Sinauer, Sunderland, MA

    Google Scholar 

  • Hooge PN, Eichenlaub B (1997) Animal movement extension to Arcview, 1.1 edn. Alaska Biological Service Center, U.S. Geological Survey, Anchorage

    Google Scholar 

  • Hughes C (1998) Integrating molecular techniques with field methods in studies of social behavior: a revolution results. Ecology 79:383–400

    Article  Google Scholar 

  • Jacquot JJ, Solomon NG (1997) Effects of site familiarity on movement patterns of male prairie voles Microtus ochrogaster. Am Midl Nat 138:414–417

    Article  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molec Ecol 16:1099–1106

    Article  Google Scholar 

  • Kays RW, Gittleman JL, Wayne RK (2000) Microsatellite analysis of kinkajou social organization. Molec Ecol 9:743–751

    Article  CAS  Google Scholar 

  • Kitchen AM, Gese EM, Waits LP, Karki SM, Schauster ER (2005) Genetic and spatial structure within a swift fox population. J Anim Ecol 74:1173–1181

    Article  Google Scholar 

  • Koenig WD, Pitelka FA, Carmen WJ, Mumme RL, Stanback MT (1992) The evolution of delayed dispersal in cooperative breeders. Q Rev Biol 67:111–150

    Article  PubMed  CAS  Google Scholar 

  • Kruckenhauser L, Pinsker W, Haring E, Arnold W (1999) Marmot phylogeny revisited: molecular evidence for a diphyletic origin of sociality. J Zool Syst Evol Res 37:49–56

    Article  Google Scholar 

  • Lacey EA, Sherman PW (2007) The ecology of sociality in rodents. In: Wolff JO, Sherman PW (eds) Rodent societies: an ecological and evolutionary perspective. University of Chicago Press, Chicago, pp 243–254

    Google Scholar 

  • Lott DF (1991) Intraspecific variation in the social systems of wild vertebrates. Cambridge University Press, Cambridge

    Google Scholar 

  • Lucia KE, Keane B, Hayes LD, Lin YK, Schaefer RL, Solomon NG (2008) Philopatry in prairie voles: an evaluation of the habitat saturation hypothesis. Behav Ecol 19:774–783

    Article  Google Scholar 

  • Maher CR (2004) Intrasexual territoriality in woodchucks (Marmota monax). J Mammal 85:1087–1094

    Article  Google Scholar 

  • Maher CR (2006) Social organization in woodchucks (Marmota monax) and its relationship to growing season. Ethology 112:313–324

    Article  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    PubMed  CAS  Google Scholar 

  • McEachern MB, Eadie JM, Van Vuren DH (2007) Local genetic structure and relatedness in a solitary mammal, Neotoma fuscipes. Behav Ecol Sociobiol 61:1459–1469

    Article  Google Scholar 

  • Meier PT (1992) Social organization of woodchucks (Marmota monax). Behav Ecol Sociobiol 31:393–400

    Article  Google Scholar 

  • Michener GR (1983) Kin identification, matriarchies, and the evolution of sociality in ground-dwelling sciurids. In: Eisenberg JF, Kleiman DG (eds) Advances in the study of mammalian behavior, vol 7. American Society of Mammalogists, Stillwater, OK, pp 528–572

  • Moyer MA, McCown JW, Eason TH, Oli MK (2006) Does genetic relatedness influence space use pattern? A test on Florida black bears. J Mammal 87:255–261

    Article  Google Scholar 

  • Munshi-South J (2008) Female-biased dispersal and gene flow in a behaviorally monogamous mammal, the large treeshrew (Tupaia tana). PLoS ONE 3:e3228. doi:10.1371/journal.pone.0003228

    Article  PubMed  CAS  Google Scholar 

  • Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Molec Ecol 4:347–354

    Article  CAS  Google Scholar 

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Molec Ecol 13:55–65

    Article  CAS  Google Scholar 

  • Peacock MM, Smith AT (1997) The effect of habitat fragmentation on dispersal patterns, mating behavior, and genetic variation in a pika (Ochotona princeps) metapopulation. Oecologia 112:324–335

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molec Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Ruibal M, Lindenmeyer DB (2003) Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution 57:1182–1195

    PubMed  Google Scholar 

  • Perrin N, Lehmann L (2001) Is sociality driven by the costs of dispersal or the benefits of philopatry? A role for kin-discrimination mechanisms. Am Nat 158:471–483

    Article  PubMed  CAS  Google Scholar 

  • Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    Article  PubMed  CAS  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  Google Scholar 

  • Ratnayeke S, Tuskan GA, Pelton MR (2002) Genetic relatedness and female spatial organization in a solitary carnivore, the raccoon, Procyon lotor. Molec Ecol 11:1115–1124

    Article  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Richlen ML, Barber PH (2005) A technique for the rapid extraction of microalgal DNA from single live and preserved cells. Molec Ecol Notes 5:688–691

    Article  CAS  Google Scholar 

  • SAS Institute I (2004) JMP 5.1 In. SAS Institute, Cary, NC

  • Schenk A, Obbard ME, Kovacs KM (1998) Genetic relatedness and home-range overlap among female black bears (Ursus americanus) in northern Ontario, Canada. Can J Zool 76:1511–1519

    Article  Google Scholar 

  • Snyder RL (1976) The biology of population growth. St. Martin's, New York

    Google Scholar 

  • Solomon NG (2003) A reexamination of factors influencing philopatry in rodents. J Mammal 84:1182–1197

    Article  Google Scholar 

  • Solomon NG, Getz LL (1997) Examination of alternative hypotheses for cooperative breeding in rodents. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 199–230

    Google Scholar 

  • Steppan SJ, Akhverdyan MR, Lyapunova EA, Fraser DG, Vorontosov NN, Hoffmann RS, Braun MJ (1999) Molecular phylogeny of the marmots (Rodentia: Sciuridae): tests of evolutionary and biogeographic hypotheses. Syst Biol 48:715–734

    Article  PubMed  CAS  Google Scholar 

  • Stevens S, Coffin J, Strobeck C (1997) Microsatellite loci in Columbian ground squirrels Spermophilus columbianus. Molec Ecol 6:493–495

    Article  CAS  Google Scholar 

  • Støen O-G, Belleman E, Saebo S, Swenson JE (2005) Kin-related spatial structure in brown bears Ursus arctos. Behav Ecol Sociobiol 59:191–197

    Article  Google Scholar 

  • Swihart RK (1992) Home range attributes and spatial structure of woodchuck populations. J Mammal 73:604–618

    Article  Google Scholar 

  • Swihart RK, Slade NA, Bergstrom BJ (1988) Relating body size to the rate of home range use in mammals. Ecology 69:393–399

    Article  Google Scholar 

  • Tchabovsky A, Bazykin G (2004) Females delay dispersal and breeding in a solitary gerbil, Meriones tamariscinus. J Mammal 85:105–112

    Article  Google Scholar 

  • Van de Casteele T, Galbusera P, Matthysen E (2001) A comparison of microsatellite-based pairwise relatedness estimators. Molec Ecol 10:1539–1549

    Article  Google Scholar 

  • van Horn RC, Altmann J, Alberts SC (2008) Can't get there from here: inferring kinship from pairwise genetic relatedness. Anim Behav 75:1173–1180

    Article  Google Scholar 

  • van Staaden MJ, Chesser RK, Michener GR (1994) Genetic correlations and matrilineal structure in a population of Spermophilus richardsonii. J Mammal 75:573–582

    Article  Google Scholar 

  • Van Vuren D (1989) Effects of intraperitoneal transmitter implants on yellow-bellied marmots. J Wildl Manage 53:320–323

    Article  Google Scholar 

  • Van Vuren D, Armitage KB (1994) Survival of dispersing and philopatric yellow-bellied marmots: what is the cost of dispersal? Oikos 69:179–181

    Article  Google Scholar 

  • Vestal BM, McCarley H (1984) Spatial and social relations of kin in thirteen-lined and other ground squirrels. In: Murie JO, Michener GR (eds) The biology of ground dwelling squirrels: annual cycles, behavioral ecology, and sociality. University of Nebraska Press, Lincoln, pp 404–423

    Google Scholar 

  • Walker FM, Sunnucks P, Taylor AC (2008a) Evidence for habitat fragmentation altering within-population processes in wombats. Molec Ecol 17:1674–1684

    Article  Google Scholar 

  • Walker FM, Taylor AC, Sunnucks P (2008b) Female dispersal and male kinship-based association in southern hairy-nosed wombats (Lasiorhinus latifrons). Molec Ecol 17:1361–1374

    Article  Google Scholar 

  • Walsh PS, Metzger DA, Higuschi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513

    PubMed  CAS  Google Scholar 

  • Waser PM, Jones WT (1983) Natal philopatry among solitary mammals. Q Rev Biol 58:355–390

    Article  Google Scholar 

  • West SA, Pen I, Griffin AS (2002) Cooperation and competition between relatives. Science 296:72–75

    Article  PubMed  CAS  Google Scholar 

  • Worton BJ (1989) Kernel methods for estimating the utilization distribution in home-range studies. Ecology 70:164–168

    Article  Google Scholar 

  • Wronski T, Apio A (2006) Home-range overlap, social vicinity and agonistic interactions denoting matrilineal organisation in bushbuck, Tragelaphus scriptus. Behav Ecol Sociobiol 59:819–828

    Article  Google Scholar 

Download references

Acknowledgments

I am grateful to the staff of the Maine Audubon Society for permission to work at Gilsland Farm Sanctuary and for their assistance over the years. I thank K. Armitage, E. Lacey, F. Walker, and three anonymous reviewers for comments on previous versions. Special thanks to J. Rhymer for hosting me in her lab and to her and J. Muhlin for their assistance with microsatellite DNA analyses, to S. Zervanos and C. Salsbury for training on surgical techniques, and to C. Radding for performing surgeries; and to over 60 undergraduate assistants, particularly T. Daigle, S. Long, Y. Seko, and J. Wright, and especially M. Duron for her dedicated work in both the field and the lab. This work was funded by the National Science Foundation (IBN-0074458), University of Southern Maine Faculty Senate Research Grants, University of Southern Maine Summer Research Award, and the Maine Economic Improvement Fund. All procedures were approved by the University of Southern Maine's Institutional Animal Care and Use Committee and comply with current laws of the USA.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christine R. Maher.

Additional information

Communicated by G. Wilkinson

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maher, C.R. Genetic relatedness and space use in a behaviorally flexible species of marmot, the woodchuck (Marmota monax). Behav Ecol Sociobiol 63, 857–868 (2009). https://doi.org/10.1007/s00265-009-0726-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-009-0726-5

Keywords

Navigation