Advertisement

Genetic Structure Within and Among Populations of the Common Marmoset, Callithrix jacchus: Implications for Cooperative Breeding

  • Christopher G. Faulkes
  • M. F. Arruda
  • M. A. O. Monteiro da Cruz
Chapter
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)

Abstract

Cooperative breeding and a reproductive division of labor are characteristic features of callitrichid primates. Of key importance in understanding this kind of social strategy is knowledge of the kin structure of groups, yet until recently the patterns of relatedness within and among social groups have remained unclear, even in the best-studied species such as the common marmoset Callithrix jacchus. Of particular interest is the role of kin selection in helping behavior and group dynamics, and the application of molecular genetic techniques to investigate group structure, dynamics, and parentage is now unequivocally addressing such issues. Both microsatellite genotyping and mitochondrial DNA sequence analysis have revealed that while social groups may often be composed of extended family groups, considerable genetic heterogeneity may also arise as a result of inter-group migrations. In one study, a group of nine animals was shown to contain individuals from five matrilines. The occurrence of groups of mixed lineages raises interesting questions about potential reproductive conflicts of interest and the extent of kin-selected altruism in the evolution and maintenance of cooperative behavior in this species.

Keywords

Common Marmoset Breeding Female Cooperative Breeding Breeding Male Golden Lion Tamarin 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Resumen

La crianza cooperativa y una división reproductiva de labores son rasgos característicos de los primates calitrícidos. El conocimiento de la estructura de parentesco de los grupos es de importancia clave en la comprensión de este tipo de estrategia social; sin embargo, hasta hace poco tiempo los patrones de las relaciones de parentesco dentro y entre los grupos sociales han permanecido poco claros, aún en las especies mejor estudiadas como es el caso de la marmoseta común Callithrix jacchus. De particular interés es el papel que juega la selección por parentesco en el comportamiento de ayuda y en las dinámicas de grupo. La aplicación de las técnicas de la genética molecular para investigar la estructura del grupo, las dinámicas y el parentesco claramente se está dirigiendo en esa dirección. Tanto el genotipado de microsatélites como el análisis de secuencias del ADN mitocondrial han revelado que mientras los grupos sociales pueden muchas veces estar compuestos por grupos de familias completas, considerable heterogeneidad genética podría también presentarse como resultado de migraciones intergrupales. En un estudio, un grupo de nueve animales mostró tener individuos provenientes de cinco matrilíneas. La ocurrencia de grupos con linajes mixtos conlleva preguntas interesantes sobre los potenciales conflictos de interés reproductivos y el grado de altruismo por selección de parentesco en la evolución y mantenimiento de los comportamientos de cooperación en esta especie.

Resumo

A reprodução cooperativa com a divisão do cuidado à prole constitui uma característica dos primatas calitriquídeos. O conhecimento da estrutura de parentesco dos grupos é de importância chave para a compreensão deste tipo de estratégia social, mas até recentemente, os padrões de parentesco dentro e entre os grupos sociais não eram conhecidos mesmo em espécies bem estudadas como o sagüi comum, Callithrix jacchus. É de particular interesse o papel da seleção de parentesco na participação de ajudantes na dinâmica dos grupos, e a aplicação de técnicas de genética molecular para investigar a estrutura, a dinâmica e o parentesco dentro do grupo está atualmente voltada para estas questões. As análises de genotipagem por microsatélite e seqüenciamento de DNA mitocondrial têm revelado que embora os grupos sejam compostos frequentemente por famílias ampliadas, pode haver uma considerável heterogeneidade genética resultante de migrações entre grupos. Em um estudo, foi encontrado que em um grupo de nove animais, os indivíduos apresentavam cinco linhagens maternas. A ocorrência de grupos com diferentes linhagens levanta questões interessantes sobre conflitos reprodutivos potenciais e os níveis de altruísmo voltado para os animais aparentados, na evolução e manutenção do cuidado cooperativo nesta espécie.

Notes

Acknowledgements

The authors are greatly indebted to Emilia Yamomoto and Hilary Box for all their help and support with the project. Thanks also to IBAMA/EFLEX and the support staff at Nísia Floresta Tapacurá, and to Steve Le Comber for comments on an early version of the manuscript. This work was funded by grants from the Royal Society of London, CnPq (Brazil) and a British Council/CAPES Links Programme, all of whom we gratefully thank.

References

  1. Abbott DH, Saltzman W, Schultz-Darken J, Tannenbaum PL (1998) Adaptations to subordinate status in female marmoset monkeys. Comp Biochem Physiol C 19:261–274Google Scholar
  2. Albuquerque ACSR, Sousa MBC, Santos HM, Ziegler TE (2001) Behavioral and hormonal analysis of social relationships between oldest females in a wild monogamous group of common marmosets (Callithrix jacchus). Int J Primatol 22:631–645CrossRefGoogle Scholar
  3. Arruda MF, Araújo A, Sousa MBC, Albuquerque FS, Albuquerque ACSR, Yamamoto ME (2005) Two-breeding females within free-living groups may not always indicate polygyny: alternative subordinate female strategies in common marmosets (Callithrix jacchus). Folia Primatol 76:10–20CrossRefPubMedGoogle Scholar
  4. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, MassachusettsGoogle Scholar
  5. Bales K, Dietz J, Baker A, Miller K, Tardif SD (2000) Effects of allocare-givers on fitness of infants and parents in callitrichid primates. Folia Primatol 71:27–38CrossRefPubMedGoogle Scholar
  6. Barrett J, Abbott DH, George LM (1993) Sensory cues and suppression of reproduction in subordinate female marmoset monkeys, Callithrix jacchus. J Reprod Fert 97:301–310CrossRefGoogle Scholar
  7. Benirschke K, Anderson JM, Brownhill LE (1962) Marrow chimerism in marmosets. Science 138:513–515CrossRefPubMedGoogle Scholar
  8. Bennett NC, Faulkes CG (2000) African mole-rats – ecology and eusociality. Cambridge University Press, CambridgeGoogle Scholar
  9. Burland TM, Worthington Wilmer J (2001) Seeing in the dark: molecular approaches to the study of bat populations. Biol Rev 76:389–409Google Scholar
  10. Canavez FC, Moreira MAM, Simon F, Parham P, Seuanez HN (1999) Phylogenetic relationships of the Callitrichinae (Platyrrhini, Primates) based on b2-microglobin DNA sequences. Am J Primatol 48:225–236CrossRefPubMedGoogle Scholar
  11. Di Fiore A, Fleischer RC (2004) Microsatellite markers for woolly monkeys (Lagothrix lagotricha) and their amplification in other New World primates (Primates: Platyrrhini). Mol Ecol Notes 4:246–249CrossRefGoogle Scholar
  12. Digby LJ (1996) Sexual behavior and extragroup copulations in a wild population of common marmosets (Callithrix jacchus). Folia Primatol 70:136–145CrossRefGoogle Scholar
  13. Digby LJ, Barreto CE (1993) Social organization in a wild population of Callithrix jacchus I. Group composition and dynamics. Folia Primatol 61:123–134CrossRefPubMedGoogle Scholar
  14. Digby LJ, Ferrari SF (1994) Multiple breeding females in free-ranging groups of Callithrix jacchus. Int J Primatol 15:389–397CrossRefGoogle Scholar
  15. Digby LJ, Saltzman W (this volume) Balancing cooperation and competition in callitrichid primates: examining the relative risk of infanticide across species. In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids: the marmoset/callimico radiation. Springer, New York, pp 135–153Google Scholar
  16. Dixson AF, Anzenberger G, Monteiro da Cruz MAO, Patel I, Jeffreys AJ (1992) DNA fingerprinting of free-ranging groups of common marmosets (Callithrix jacchus jacchus) in N.E. Brazil. In: Martin RD, Dixson AF, Wickings EJ (eds) Paternity in primates: genetic tests and theories. Basel, Karger, pp 192–202Google Scholar
  17. Escobar-Páramo P (2000) Microsatellite primers for the wild brown capuchin monkey Cebus apella. Mol Ecol 9:107–118CrossRefPubMedGoogle Scholar
  18. Faulkes CG, Arruda MF, Monteiro da Cruz MA (2003) Matrilineal genetic structure within and among populations of the cooperatively breeding common marmoset, Callithrix jacchus. Mol Ecol 12:1101–1108CrossRefPubMedGoogle Scholar
  19. Ferrari SF (1993) Ecological differentiation in the Callitrichidae. In: Rylands AB (ed) Marmosets and tamarins: systematics, ecology and behaviour. Oxford University Press, Oxford, pp 314–328Google Scholar
  20. Ferrari SF (this volume) Social hierarchy and dispersal in free-ranging buffy-headed marmosets (Callithrix flaviceps). In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids: the marmoset/callimico radiation. Springer, New York, pp 155–165Google Scholar
  21. Ferrari SF, Digby LJ (1996) Wild Callithrix groups: stable extended families? Am J Primatol 38:19–27CrossRefGoogle Scholar
  22. French JA (1997) Singular breeding in callitrichid primates. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 34–75Google Scholar
  23. Goldizen AW, Mendelson J, van Vlaardingen M, Terborgh J (1996) Saddle-back tamarin (Saguinus fuscicollis) reproductive strategies: evidence from a thirteen-year study of a marked population. Am J Primatol 38:57–83CrossRefGoogle Scholar
  24. Gonçalves EC, Ferrari SF, Silva A, Coutinho PEG, Menezes EV, Schneider MPC (2003) Effects of habitat fragmentation on the genetic variability of silvery marmosets, Mico argentatus. In: Marsh LK (ed) Primates in fragments: ecology and conservation. Kluwer/Plenum, New York, pp 17–28Google Scholar
  25. Gonçalves EC, Ferrari SF, Coutinho PEG, Menezes EV, Silva A, Schneider MPC (this volume) Limited dispersal and genetic structure of silvery marmosets (Mico argentatus) in the fragmented landscape of Central Amazonia. In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids: the marmoset/callimico radiation. Springer, New York, pp 205–220Google Scholar
  26. Grativol AD, Ballou JD, Fleischer RC (2001) Microsatellite variation within and among recently fragmented populations of the golden lion tamarin (Leontopithecus rosalia). Conserv Gen 2:1–9CrossRefGoogle Scholar
  27. Hauser MD, Chen MK, Chen F, Chuang E (2003) Give unto others: genetically unrelated tamarins preferentially give food to those that altruistically give food back. Proc R Soc Lond B 270:2363–2370CrossRefGoogle Scholar
  28. Hubrecht RC (1984) Field observations on group size and composition of the common marmoset (Callithrix jacchus jacchus), at Tapacura, Brazil. Primates 25:13–21CrossRefGoogle Scholar
  29. Lazaro-Perea C, Castro CSS, Harrison R, Araújo A, Arruda MF, Snowdon CT (2000) Behavioral and demographic changes following the loss of the breeding female in cooperatively breeding marmosets. Behav Ecol Sociobiol 48:137–146CrossRefGoogle Scholar
  30. Mendes Pontes AR, Monteiro da Cruz MAO (1995) Home range, inter-group transfers, and reproductive status of common marmosets Callithrix jacchus in a forest fragment in north-eastern, Brazil. Primates 36:335–347CrossRefGoogle Scholar
  31. Nievergelt CM, Digby LJ, Ramiakrishnan U, Woodruff DS (2000) Genetic analysis of group composition and breeding system in a wild common marmoset (Callithrix jacchus) population. Int J Primatol 21:1–20CrossRefGoogle Scholar
  32. Nievergelt CM, Mundy NI, Woodruff DS (1998) Microsatellite primers for genotyping common marmosets (Callithrix jacchus) and other callitrichids. Molecular Ecology 7:1431–1439CrossRefGoogle Scholar
  33. Perez-Sweeney BM, Valladares-Padua C, Burrell AS, Di Fiore A, Satkoski J, Van Coeverden De Groot PJ, Boag PT, Melnick DJ (2005) Dinucleotide microsatellite primers designed for a critically endangered primate, the black lion tamarin (Leontopithecus chrysopygus). Mol Ecol Notes 5:198–201CrossRefGoogle Scholar
  34. Ross KG (2001) Molecular ecology of social behaviour: analyses of breeding systems and genetic structure. Mol Ecol 10:265–284CrossRefPubMedGoogle Scholar
  35. Rossiter SJ, Ransome RD, Faulkes CG, Le Comber SC, Jones G (2005) Mate fidelity and intra-lineage polygyny in greater horseshoe bats. Nature 437:408–411CrossRefPubMedGoogle Scholar
  36. Rylands AB (1984) Exudate-eating and tree-gouging by marmosets (Callitrichidae, Primates). In: Chadwick AC, Sutton SL (eds) Tropical rain forest: the Leeds symposium. Leeds Philosophical and Literary Society, Leeds, pp 155–168Google Scholar
  37. Saltzman W, Schultz-Darken NJ, Abbott DH (1997) Familial influences on ovulatory function in common marmosets (Callithrix jacchus). Am J Primatol 41:159–177CrossRefPubMedGoogle Scholar
  38. Sánchez S, Peláez F, Gil-Bürmann C, Kaumanns W (1999) Costs of infant carrying in the cotton-top tamarin (Saguinus oedipus). Am J Primatol 48:99–111CrossRefPubMedGoogle Scholar
  39. Scanlon CE, Chalmers NR, Monteiro da Cruz MAO (1988) Changes in the size, composition, and reproductive condition of wild marmoset groups (Callithrix jacchus jacchus) in North East Brazil. Primates 29:295–305CrossRefGoogle Scholar
  40. Sena L, Vallinoto M, Sampaio I, Schneider H, Ferrari SF, Schneider MPC (2002) Mitochondrial COII gene sequences provide new insights into the phylogeny of marmoset species groups (Callitrichidae, Primates). Folia Primatol 73:240–51CrossRefPubMedGoogle Scholar
  41. Signer EN, Anzenberger G, Jeffreys AJ (2000) Chimaeric and constitutive DNA fingerprints in the common marmoset (Callithrix jacchus). Primates 41:49–61CrossRefGoogle Scholar
  42. Solomon NG, French JA (1997) Cooperative breeding in mammals. Cambridge University Press, CambridgeGoogle Scholar
  43. Sousa MBC de, Rocha Albuquerque ACS da, Yamamoto ME, Araújo A, Fátima Arruda M de (this volume) Emigration as a reproductive strategy of the common marmoset (Callithrix jacchus). In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids: the marmoset/callimico radiation. Springer, New York, pp 167–182Google Scholar
  44. Stevenson MF, Rylands AB (1988) The marmoset, genus Callithrix. In: Mittermeier RA, Rylands AB, Coimbra-Filho AF, da Fonseca GAB (eds) Ecology and behavior of Neotropical primates, vol 2. World Wildlife Fund, Washington DC, pp 131–222Google Scholar
  45. Suárez SS, Böhle UR, Jolly CJ, Disotell TR (2004) Behavioural and genetic data illustrate alternative reproductive strategies in monogamous groups of wild red-bellied tamarins (Saguinus labiatus) in northwestern Bolivia. Folia Primatol 75(suppl 1):89Google Scholar
  46. Tagliaro CH, Schneider MPC, Schneider H, Sampaio IC, Stanhope MJ (1997) Marmoset phylogenetics, conservation perspectives, and evolution of the mtDNA control region. Mol Biol Evol 14:674–684PubMedGoogle Scholar
  47. Tardif SD (1997) Parental behavior and evolution of alloparental care. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 11–33Google Scholar
  48. Tardif SD, Bales K (1997) Is infant carrying a courtship strategy in captive callitrichids? Animal Behaviour 53:1001–1007CrossRefGoogle Scholar
  49. Tardif SD, Harrison ML, Simek MA (1993) Communal infant care in marmosets and tamarins: relations to energetics, ecology and social organisation. In: Rylands AB (ed) Marmosets and tamarins: systematics, behaviour and ecology. Oxford University Press, Oxford, pp 220–234Google Scholar
  50. Yamamoto ME, Arruda M de F, Alencar AI, de Sousa MBC, Araújo A (this volume) Mating systems and female–female competition in the common marmosets, Callithrix jacchus. In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids: the marmoset/callimico radiation. Springer, New York, pp 119–133Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Christopher G. Faulkes
    • 1
  • M. F. Arruda
  • M. A. O. Monteiro da Cruz
  1. 1.School of Biological and Chemical SciencesQueen Mary, University of LondonLondonUK

Personalised recommendations