Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Genetic relationships within colonies suggest genetic monogamy in the Eurasian beaver (Castor fiber)

Abstract

Social monogamy, considered rare in mammals, has been described in two species of beaver, the Eurasion beaver (Castor fiber), and the North American beaver (Castor Canadensis). Social monogamy, however, does not necessarily imply genetic monogamy. For example, in group living mammals, females may engage in extra-pair copulations as a result of increased female mate choice opportunities. Recently, following genetic analysis, a wide range of genetic relationships among colony members have been documented in the North American beaver, including extra-pair paternity. Here, we used microsatellite loci to provide parentage estimates from colonies of the Eurasian beaver in the Kirov region, Russia. No evidence for the presence of any extra-pair young was detected. However, in two cases, we found a pair of unrelated males inhabiting a single colony. Our results suggest that while colonies may comprise both related and unrelated individuals, the genetic mating system appears to match that of the previously inferred social monogamy.

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

Fig. 1

References

  1. Babik W, Durka W, Radwan J (2005) Sequence diversity of the MHC DRB gene in the Eurasian beaver (Castor fiber). Mol Ecol 14:4249–4257

  2. Baker BW, Hill EP (2003) Beaver (Castor canadensis). In: Feldhamer GA, Thompson BC, Chapman JA (eds) Wild Mammals of North America: Biology, Management, and Conservation, 2nd edn. The Johns Hopkins University Press, Baltimore, pp 288–310

  3. Bierla JB, Gizejewski Z, Leigh CM, Ekwall H, Söderquist L, Rodriguez-Martinez H, Zalewski K, Breed WG (2007) Sperm morphology of the Eurasian beaver, Castor fiber: An example of a species of rodent with highly derived and pleiomorphic sperm populations. J Morphol 268:683–689

  4. Brotherton PNM, Pemberton JM, Komers PE, Malarky G (1997) Genetic and behavioural evidence of monogamy in a mammal, Kirk's dik-dik (Madoqua kirkii). Proc R Soc Lond B 264:675–681

  5. Bryja J, Patzenhauerová H, Albrecht T, Mošanský L, Stanko M, Stopka P (2008) Varying levels of female promiscuity in four Apodemus mice species. Behav Ecol Sociobiol 63:251–260

  6. Busher PE, Warner RJ, Jenkins SH (1983) Population-density, colony composition, and local movements in two Sierra Nevadan beaver populations. J Mammal 64:314–318

  7. Campbell RD, Rosell F, Nolet BA, Dijkstra VAA (2005) Territory and group sizes in Eurasian beavers (Castor fiber): echoes of colony and reproduction? Behav Ecol Sociobiol 58:597–607

  8. Clutton-Brock TH, Isvaran K (2006) Paternity loss in contrasting mammalian societies. Biol Lett 2:513–516

  9. Cohas A, Allainé D (2009) Social structure influences extra-pair paternity in socially monogamous mammals. Biol Lett 5:313–316

  10. Crawford J, Liu Z, Nelson T, Nielsen C, Bloomquist C (2008a) Isolation and characterization of microsatellite loci in the beaver (Castor canadensis). Mol Ecol Res 8:616–618

  11. Crawford JC, Liu Z, Nelson TA, Nielsen CK, Bloomquist CK (2008b) Microsatellite analysis of mating and kinship in beavers (Castor canadensis). J Mammal 89:575–581

  12. Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504–509

  13. Ducroz JF, Stubbe M, Saveljev AP, Heidecke D, Samjaa R, Ulevicius A, Stubbe A, Durka W (2005) Genetic variation and population structure of the Eurasian beaver Castor fiber in Eastern Europe and Asia. J Mammal 86(6):1059–1067

  14. Durka W, Babik W, Ducroz JF, Heidecke D, Rosell F, Samjaa R, Saveljev AP, Stubbe A, Ulevicius A, Stubbe M (2005) Mitochondrial phylogeography of the Eurasian beaver Castor fiber L. Mol Ecol 14:3843–3856

  15. Ellegren H, Hartman G, Johansson M, Anderson L (1993) Major histocompatibility complex monomorphism and low levels of DNA fingerprinting variability in a reintroduced and rapidly expanding population of beavers. Proc Natl Acad Sci U S A 90(17):8150–8153

  16. Fischer JW, Joos RE, Neubaum MA, Taylor JD, Bergman DL, Nolte DL, Piaggio AJ (2010) Lactating North American beavers (Castor canadensis) sharing dens in the southwestern United States. Southwest Nat 55(2):273–277

  17. Frosch C, Haase P, Nowak C (2011) First set of microsatellite markers for genetic characterization of the Eurasian beaver (Castor fiber) based on tissue and hair samples. Eur J Wildl Res 57:679–682

  18. Frosch C, Kraus RHS, Angst C, Allgower R, Michaux J, Teubner J, Nowak C (2014) The genetic legacy of multiple beaver reintroductions in central Europe. PLoS ONE 9:e97619

  19. Gohli J, Anmarkrud JA, Johnsen A, Kleven O, Borge T, Lifjeld JT (2013) Female promiscuity is positively associated with neutral and selected genetic diversity in passerine birds. Evolution 67:1406–1419

  20. Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

  21. Hartman G (1997) Notes on age at dispersal of beaver (Castor fiber) in an expanding population. Can J Zool 75:959–962

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

  23. Hennessy CA, Dubach J, Gehrt SD (2012) Long-term pair bonding and genetic evidence for monogamy among urban coyotes (Canis latrans). J Mammal 93:732–742

  24. Herr J, Rosell F (2004) Use of space and movement patterns in monogamous adult Eurasian beavers (Castor fiber). J Zool 262(3):257–264

  25. Hinze G (1960) Unser Biber. Die Neue Brehm-Bücherei; Heft 111. Verlagsgesellschaft Geest & Portig, Leipzig

  26. Horn S, Durka W, Wolf R, Ermala A, Stubbe A, Stubbe M, Hofreiter M (2011) Mitochondrial genomes reveal slow rates of molecular evolution and the timing of speciation in beavers (Castor), one of the largest rodent species. PLoS ONE 6:e14622

  27. Huck M, Fernandez-Duque E, Babb P, Schurr T (2014) Correlates of genetic monogamy in socially monogamous mammals: insights from Azara's owl monkeys. Proc R Soc Lond B 281:20140195

  28. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64

  29. Jones O, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Res 10:551–555

  30. Jones AG, Small CM, Paczolt KA, Ratterman NL (2010) A practical guide to methods of parentage analysis. Mol Ecol Res 10:6–30

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

  32. Kenagy GJ, Trombulak SC (1986) Size and function of mammalian testes in relation to body size. J Mammal 67:1–22

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

  34. Konovalov DA, Manning C, Henshaw MT (2004) KINGROUP: a program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol Ecol Notes 4:779–782

  35. Lardy S, Cohas A, Desouhant E, Tafani M, Allainé D (2012) Paternity and dominance loss in male breeders: The cost of helpers in a cooperatively breeding mammal. PLoS ONE 7:e29508

  36. Lavrov LS (1960) Comments on biological and morphological distinction of European and Canadian beavers (K voprosu o biologicheskih i morphologicheskih razlichijah mezhdu evropeiskimi i kanadskimi bobrami). Proc. Voronezh State Zapovednik 11:103–120 [In Russian]

  37. Lavrov VL (1989) On the possibility of the polygamic breeding of the beavers in captivity (O vozmozhnosti poligamnogo razvedenia bobrov v uslovijah kletochnogo soderzhania). Byulleten’ Mosk Obs Ispyt Prir Otd Biol 94:41–43 [in Russian with Engl summary]

  38. Lott DF (1984) Intraspecific variation in the social systems of wild vertebrates. Behaviour 88:266–325

  39. Lukas D, Clutton-Brock T (2012) Cooperative breeding and monogamy in mammalian societies. Proc R Soc Lond B 279:2151–2156

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

  41. Milishnikov AN, Saveljev AP (2001) Genetic divergence and similarity of introduced populations of European beaver (Castor fiber L., 1758) from Kirov and Novosibirsk oblasts of Russia. Russ J Genet 37:108–111

  42. Møller AP, Garamszegi LZ, Spottiswoode CN (2008) Genetic similarity, breeding distribution range and sexual selection. J Evol Biol 21:213–225

  43. Müller-Schwarze D (2011) The beaver: Its life and impact, 2nd edn. Cornell University Press, Ithaca

  44. Nitsche KA (2001) Behaviour of beavers (Castor fiber albicus Matschie, 1907) during the flood periods. In: Czech A, Schwab G (eds) Proceedings of 2nd European Beaver Symposium. Carpathian Heritage Society, Krakow, pp 51–53

  45. Packer C, Pusey AE (1982) Cooperation and competition within coalitions of male lions – kin selection or game-theory. Nature 296:740–742

  46. Patenaude F (1983) Care of the young in a family of wild beavers, Castor canadensis. Acta Zool Fenn 174:121–122

  47. Pelz-Serrano K, Munguia-Vega A, Piaggio AJ, Neubaum M, Munclinger P, Partl A, Van Riper C, Culver M (2009) Development of nine new microsatellite loci for the American beaver, Castor canadensis (Rodentia: Castoridae), and cross-species amplification in the European beaver, Castor fiber. Mol Ecol Res 9:551–554

  48. Petrie M, Lipsitch M (1994) Avian polygyny is most likely in populations with high variability in heritable male fitness. Proc R Soc Lond B 256:275–280

  49. Petrie M, Doums C, Møller AP (1998) The degree of extra-pair paternity increases with genetic variability. Proc Natl Acad Sci U S A 95:9390–9395

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

  51. Ribble DO (1991) The monogamous mating system of Peromyscus californicus as revealed by DNA fingerprinting. Behav Ecol Sociobiol 29:161–166

  52. Rosell F, Bjørkøyli T (2002) A test of the dear enemy phenomenon in the Eurasian beaver. Anim Behav 63:1073–1078

  53. Rosell F, Thomsen LR (2006) Sexual dimorphism in territorial scent marking by adult Eurasian beavers (Castor fiber). J Chem Ecol 32:1301–1315

  54. Rosell F, Johansen G, Parker H (2000) Eurasian beavers (Castor fiber) behavioral response to simulated territorial intruders. Can J Zool 78:931–935

  55. Safonov VG (1965) Some features of ecology of the beaver during the winter period (Nekotorye osobennosti ekologii rechnogo bobra v zimnij period). Bull Sci and Techn Inf “Hunting-Fur-Game”. Kirov 12:26–35 [In Russian]

  56. Safonov VG (1971) Notes on biology of beaver reproduction in the European part of the USSR (Materialy po biologii razmnozhenia rechnyh bobrov v Evropejskoj chasti SSSR). Questions of biology of game animals and the organisation of the hunting husbandry. Proc Kirov Argic Inst 28:25–39 [In Russian]

  57. Saveljev AP (2001) Rettung des Bibers (Castor fiber) in Russland: offensichtlicher jagdwirtschaftlicher Erfolg mit zoologischen Problemen nach 70 Jahren. Beitr Jagd-Wildforsch 26:309–315

  58. Saveljev A, Milishnikov A (2002) Biological and genetic peculiarities of cross-composed and aboriginal beaver populations in Russia. Acta Zool Lit 12:397–402

  59. Saveljev AP, Stubbe M, Stubbe A, Putintsev NI, Oleynikov AY, Savelyev AA (2010) Movements of beavers under natural conditions and in places of introduction (Peremeshenia bobrov v estestvennoi obstanovke i v mestah introdukcii). Vestnik Ochotovedenia (Game Sci Bull) 7:340–344 [In Russian with English summary]

  60. Senn H, Ogden R, Cezard T, Gharbi K, Iqbal Z, Johnson E, Kamps-Hughes N, Rosell F, Mcewing R (2013) Reference-free SNP discovery for the Eurasian beaver from restriction site-associated DNA paired-end data. Mol Ecol 22:3141–3150

  61. Senn H, Ogden R, Frosch C, Syruckova A, Campbell-Palmer R, Munclinger P, Durka W, Kraus RHS, Saveljev AP, Nowak C, Stubbe A, Stubbe M, Michaux J, Lavrov V, Samiya R, Ulevicius A, Rosell F (2014) Nuclear and mitochondrial genetic structure in the Eurasian beaver (Castor fiber) – implications for future reintroductions. Evol Appl 7:645–662

  62. 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

  63. Soulsbury CD (2010) Genetic patterns of paternity and testes size in mammals. PLoS ONE 5:e9581

  64. Stubbe A, Stubbe M, Saveljev AP, Unžakov VV (2003) Der Lebendfang als Grundlage für Wachstumsanalysen und die Morphometrie von Körpermassen in autochthonen Biberpopulationen. In Stubbe M, Stubbe A (eds) Methoden feldökologischer Säugetierforschung 2. Martin-Luther-Universität Halle-Wittenberg, pp 329-347

  65. Sun L (2003) Monogamy correlates, socioecological factors, and mating systems in beavers. In: Reichard UH, Boesch C (eds) Monogamy: Mating Strategies and Partnerships in Birds. Humans and Other Mammals. Cambridge university press, Cambridge, pp 138–146

  66. Svendsen GE (1980) Patterns of scent-mounding in a population of beaver (Castor canadensis). J Chem Ecol 6:133–148

  67. Tinnesand HV, Jojola S, Zedrosser A, Rosell F (2013) The smell of desperadoes? Beavers distinguish between dominant and subordinate intruders. Behav Ecol Sociobiol 67:895–904

  68. van Oosterhout C, Hutchinson B, Wills D, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

  69. Wheatley M (1993) Report of two pregnant beavers, Castor canadensis, at one beaver lodge. Can Field Nat 107:103

  70. Wilsson L (1971) Observations and experiments on the ethology of the European beaver (Castor fiber L.). Viltrevy 8:115–266

Download references

Acknowledgments

We highly appreciate the help of hunters from the Kotelnich regional hunter union. CF is particularly grateful for the assistance given by C Nowak and RHS Kraus. AS was supported by the Charles University in Prague (projects GAUK 151210 and SVV 260 087/2014). PM and AS thank Z Csiebreiová for her technical assistance in the laboratory. We are also grateful to T Albrecht and three anonymous reviewers for insightful comments on the previous version of the manuscript.

Ethical standards

Research followed Russian federal hunting law (2009 N 209).

Author information

Correspondence to Pavel Munclinger.

Additional information

Communicated by: Mabel D. Giménez

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Syrůčková, A., Saveljev, A.P., Frosch, C. et al. Genetic relationships within colonies suggest genetic monogamy in the Eurasian beaver (Castor fiber). Mamm Res 60, 139–147 (2015). https://doi.org/10.1007/s13364-015-0219-z

Download citation

Keywords

  • Extra-pair paternity
  • Family group
  • Mating system
  • Spatial structure
  • Pairwise relatedness