Behavioral Ecology and Sociobiology

, Volume 69, Issue 2, pp 169–181 | Cite as

Group composition, relatedness, and dispersal in the cooperatively breeding cichlid Neolamprologus obscurus

  • Hirokazu Tanaka
  • Dik Heg
  • Hirohiko Takeshima
  • Tomohiro Takeyama
  • Satoshi Awata
  • Mutsumi Nishida
  • Masanori Kohda
Original Paper

Abstract

Cooperative breeding has been studied intensively in many species of birds and mammals but remain less well studied in fish. We report a remarkable new example of a cooperatively breeding cichlid from Lake Tanganyika, Neolamprologus obscurus. Using field observations and microsatellite DNA analyses, we studied group structure, helping behavior, relatedness, and dispersal of this species. We present four major observations. First, large territorial breeding males mated with one to eight breeding females, each of which was territorial and unrelated to another. Second, one to ten smaller fish (“subordinates”) of both sexes were allowed to stay inside the breeding females’ territories. Subordinates were often highly related to both the respective breeding male and female and performed territory defense and shelter maintenance, which is regarded as helping behaviors. Third, one to three subordinate males, similar in size to breeding females, were allowed to stay inside a breeding male’s territory but were not tolerated in the breeding females’ territories. Pairwise relatedness suggests these individuals are usually sons of the respective breeding male. Fourth, pairwise relatedness estimates suggest that juveniles delay dispersal and assist their mothers in raising offspring. As female subordinates grow up, they leave the father’s territory and disperse into other groups. In contrast, male subordinates leave their mother’s territory but remain within the territory of their father. The described social system makes N. obscurus a promising new model species to study the evolution of cooperative breeding.

Keywords

Cooperative breeding Social system Related helper Delayed dispersal Fish 

Supplementary material

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265_2014_1830_MOESM2_ESM.xlsx (12 kb)
ESM 2(XLSX 12 kb)

References

  1. Awata S, Kohda M (2004) Parental roles and the amount of care in a bi-parental substrate brooding cichlid: the effect of size differences within pairs. Behaviour 141:1135–1149CrossRefGoogle Scholar
  2. Awata S, Munehara H, Kohda M (2005) Social system and reproduction of helpers in the cooperatively breeding cichlid fish Julidochromis ornatus in Lake Tanganyika: field observations and parentage analyses. Behav Ecol Sociobiol 58:506–516CrossRefGoogle Scholar
  3. Awata S, Heg D, Kohda M, Munehara H, Kohda M (2006) Testis size depends on social status and the presence of male helpers in the cooperatively breeding cichlid Julidochromis ornatus. Behav Ecol 17:372–379CrossRefGoogle Scholar
  4. Balshine-Earn S, Neat F, Reid H, Taborsky M (1998) Paying to stay or paying to breed? Field evidence for direct benefits of helping behavior in a cooperatively breeding fish. Behav Ecol 9:432–438Google Scholar
  5. Bates D, Maechler M, Bolker B (2011) lme4: linear mixed-effects models using S4 classes. R package version 0.999375-39. http://CRAN.R-project.org/package=lme4
  6. Bergmüller R, Heg D, Taborsky M (2005) Helpers in a cooperatively breeding cichlid stay and pay or disperse and breed, depending on ecological constraints. Proc R Soc Lond B 272:325–331CrossRefGoogle Scholar
  7. Bolker BM, Brooks ME, Clark CI, Geange SW, Poulsen JR, Stevens MH, White JS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trend Ecol Evol 24:127–135CrossRefGoogle Scholar
  8. Brouwer L, Heg D, Taborsky M (2005) Experimental evidence for helper effects in a cooperatively breeding cichlid. Behav Ecol 16:667–673CrossRefGoogle Scholar
  9. Clarke A, Saether B, Roskaft E (1997) Sex biases in avian dispersal: a reappraisal. Oikos 79:429–438CrossRefGoogle Scholar
  10. Clutton-Brock TH, Lukas D (2012) The evolution of social philopatry and dispersal in female mammals. Mol Ecol 21:472–492PubMedCrossRefGoogle Scholar
  11. Cockburn A (2006) Prevalence of different modes of parental care in birds. Proc R Soc Lond B 273:1375–1383CrossRefGoogle Scholar
  12. Creel SR (1994) Inclusive fitness and reproductive strategies in dwarf mongooses. Behav Ecol 5:339–348CrossRefGoogle Scholar
  13. Desjardins JK, Fitzpatrick JL, Stiver KA, van der Kraak GJ, Balshine S (2008) Costs and benefits of polygyny in the cichlid Neolamprologus pulcher. Anim Behav 75:1771–1779CrossRefGoogle Scholar
  14. Dierkes P, Heg D, Taborsky M, Skubic E, Achmann R (2005) Genetic relatedness in groups is sex-specific and declines with age of helpers in a cooperatively breeding cichlid. Ecol Lett 8:968–975CrossRefGoogle Scholar
  15. Duftner N, Sefc K, Koblmüller S, Salzburger W, Taborsky M, Sturmbauer C (2007) Parallel evolution of facial stripe patterns in the Neolamprologus brichardi/pulcher species complex endemic to Lake Tanganyika. Mol Phylogenet Evol 45:706–715PubMedCrossRefGoogle Scholar
  16. Eikenaar C, Richardson DS, Brouwer L, Komdeur J (2007) Parent presence, delayed dispersal, and territory acquisition in the Seychelles warbler. Behav Ecol 18:874–879CrossRefGoogle Scholar
  17. Eikenaar C, Richardson DS, Brouwer L, Komdeur J (2008) Sex biased natal dispersal in a closed, saturated population of Seychelles warblers Acrocephalus sechellensis. J Avian Biol 39:73–80CrossRefGoogle Scholar
  18. Ekman J, Bylin A, Tegelström H (1999) Parental nepotism enhances survival of retained offspring in the Siberian jay. Behav Ecol 11:416–420CrossRefGoogle Scholar
  19. Feeney W, Medina I, Somveille M, Heinsohn R, Hall ML, Mulder RA, Stain JA, Kilner RM, Langmore NE (2013) Brood parasitism and the evolution of cooperative breeding in birds. Science 342:1506–1508PubMedCrossRefGoogle Scholar
  20. Fitzpatrick JL, Desjardins JK, Stiver KA, Montgomerie R, Balshine S (2005) Male reproductive suppression in the cooperatively breeding fish Neolamprologus pulcher. Behav Ecol 17:25–33CrossRefGoogle Scholar
  21. Fitzpatrick JL, Desjardins JK, Milligan N, Stiver KA, Montgomerie R, Balshine S (2008) Female-mediated causes and consequences of social status change in a social fish. Proc R Soc Lond B 275:929–936CrossRefGoogle Scholar
  22. Goodnight KF, Queller DC (1999) Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol Ecol 8:1231–1234CrossRefGoogle Scholar
  23. Grantner A, Taborsky M (1998) The metabolic rates associated with resting, and with the performance of agonistic, submissive and digging behaviours in the cichlid fish Neolamprologus pulcher (Pisces: Cichlidae). J Comp Physiol B 168:427–433CrossRefGoogle Scholar
  24. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162Google Scholar
  25. Greenwood PJ (1983) Mating systems and the evolutionary consequences of dispersal. In: Swingland IR, Greenwood PJ (eds) The ecology of animal movement. Oxford University Press, Oxford, pp 116–131Google Scholar
  26. Greenwood PJ, Harvey PH (1982) The natal and breeding dispersal of birds. Annu Rev Ecol Syst 13:1–21Google Scholar
  27. Griffin AS, West SA (2003) Kin discrimination and the benefit of helping in cooperatively breeding vertebrates. Science 302:634–636PubMedCrossRefGoogle Scholar
  28. Heg D, Bachar Z (2006) Cooperative breeding in the Lake Tanganyika cichlid Julidochromis ornatus. Environ Biol Fish 76:265–281CrossRefGoogle Scholar
  29. Heg D, Bachar Z, Brouwer L, Taborsky M (2004) Predation risk is an ecological constraint for helper dispersal in a cooperatively breeding cichlid. Proc R Soc Lond B 271:2367–2374CrossRefGoogle Scholar
  30. Heg D, Bachar Z, Taborsky M (2005) Cooperative breeding and group structure in the Lake Tanganyika cichlids Neolamprologus savory. Ethology 111:1017–1043CrossRefGoogle Scholar
  31. Heg D, Rothenberger S, Schürch R (2011) Habitat saturation, benefits of philopatry, relatedness, and the extent of co-operative breeding in a cichlid. Behav Ecol 22:82–92CrossRefGoogle Scholar
  32. Koenig WD, Dickinson JL (2004) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  33. Kohler U (1998) Zur Struktur und Evolution des Sozialsystems von Neolamprologus multifasciatus (Cichlidae, Pisces), dem kleinsten Schneckenbuntbarsch des Tanganjikasees. Shaker Verlag, AachenGoogle Scholar
  34. Kokko H, Johnstone RA, Clutton-Brock TH (2001) The evolution of cooperative breeding through group augmentation. Proc R Soc Lond B 268:187–196CrossRefGoogle Scholar
  35. Komdeur J, Edelaar P (2001) Male Seychelles warblers use territory budding to maximize lifetime fitness in a saturated environment. Behav Ecol 12:706–715CrossRefGoogle Scholar
  36. Konings A (1998) Tanganyika cichlids in their natural habitat. Cichlid Press, El PasoGoogle Scholar
  37. Konovalov DA, Heg D (2008) TECHNICAL ADVANCES: a maximum-likelihood relatedness estimator allowing for negative relatedness values. Mol Ecol Resour 8:256–263PubMedCrossRefGoogle Scholar
  38. Konovalov DA, Manning C, Henshaw MT (2004) KINGROUP: a program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol Ecol Notes 4:779–782CrossRefGoogle Scholar
  39. Lukas D, Clutton-Brock T (2012) Cooperative breeding and monogamy in mammalian societies. Proc R Soc Lond B 279:2151–2156CrossRefGoogle Scholar
  40. Lukas D, Clutton-Brock TH (2013) The evolution of social monogamy in mammals. Science 341:526–530PubMedCrossRefGoogle Scholar
  41. Munehara H, Awata S, Katoh R, Kohda M, Sunobe T (2001) Primer sequences and cross-species amplification for parentage discrimination of Tanganyikan cichlid fishes. Bull Fac Fish, Hokkaido Univ 52:131–133Google Scholar
  42. Parker A, Kornfield I (1996) Polygynandry in Pseudotropheus zebra, a cichlid fish from Lake Malawi. Environ Biol Fish 47:345–352CrossRefGoogle Scholar
  43. Poll M (1978) A new cichlid fish genus-Lamprologus Schth. Description of four new species from Lake Tanganyika [in Central Africa]. B Cl Sci Ac Roy Belg 64:725–758Google Scholar
  44. Pusey AE (1987) Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trend Ecol Evol 2:295–299CrossRefGoogle Scholar
  45. Pusey AE, Wolf M (1996) Inbreeding avoidance in animals. Trend Ecol Evol 11:201–206Google Scholar
  46. R development core team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  47. Rossiter A (1993) Studies on the biology of Neolamprologus multifasciatus. In: Nagoshi M, Yanagisawa Y, Kawanabe H (eds) Ecological and limnological study on Lake Tanganyika and its adjacent regions VIII. Kyoto University Press, Kyoto, pp 32Google Scholar
  48. Sato T, Gashagaza MM (1997) Shell-brooding cichlid fishes of Lake Tanganyika: their habitats and mating systems. In: Kawanabe H, Hori M, Nagoshi M (eds) Fish communities in Lake Tanganyika. Kyoto University Press, Kyoto, pp 221–240Google Scholar
  49. Schliewen U, Rassmann K, Markmann M, Markert J, Kocker T, Tautz D (2001) Genetic and ecological divergence of a monophyletic cichlid species pair under fully sympatric conditions in the Lake Ejagham, Cameroon. Mol Ecol 10:1471–1488PubMedCrossRefGoogle Scholar
  50. Schradin C, Lamprecht J (2000) Female-biased immigration and male peace-keeping in groups of the shelldwelling cichlid fish Neolamprologus multifasciatus. Behav Ecol Sociobiol 48:236–242CrossRefGoogle Scholar
  51. Schradin C, Lamprecht J (2002) Causes of female emigration in the group-living cichlid fish Neolamprologus multifasciatus. Ethology 108:237–248CrossRefGoogle Scholar
  52. Stiver KA, Dierkes P, Taborsky M, Balshine S (2004) Dispersal patterns and status change in a co-operatively breeding cichlids Neolamprologus pulcher: evidence from microsatellite analyses and behavioural observations. J Fish Biol 65:91–105CrossRefGoogle Scholar
  53. Stiver KA, Dierkes P, Taborsky M, Gibbs HL, Balshine S (2005) Relatedness and helping in fish: examining the theoretical predictions. Proc R Soc Lond B 272:1593–1599CrossRefGoogle Scholar
  54. Stiver KA, Desjardins JK, Fitzpatrick JL, Neff B, Quinn JS, Balshine S (2007) Evidence for size and sex-specific dispersal in a cooperatively breeding cichlid fish. Mol Ecol 16:2974–2984PubMedCrossRefGoogle Scholar
  55. Sturmbauer C, Salzburger W, Duftner N, Schelly R, Koblmuller S (2010) Evolutionary history of the Lake Tanganyika cichlid tribe Lamprologini (Teleostei: Perciformes) derived from mitochondrial and nuclear DNA data. Mol Phylogenet Evol 57:266–284PubMedCentralPubMedCrossRefGoogle Scholar
  56. Sunobe T, Munehara H (2003) Mating system and kin relationship between adults and young in the shell-brooding cichlid fish Neolamprologus meeli in Lake Tanganyika. J Ethol 21:87–92Google Scholar
  57. Taborsky M (1984) Broodcare helpers in the cichlid fish Lamprologus brichardi: their costs and benefits. Anim Behav 32:1236–1252CrossRefGoogle Scholar
  58. Taborsky M (1985) Breeder-helper conflict in a cichlid fish with broodcare helpers: an experimental analysis. Behaviour 95:45–75CrossRefGoogle Scholar
  59. Taborsky M (1994) Sneakers, satellites, and helpers: parasitic and cooperative behavior in fish reproduction. Adv Stud Behav 23:1–100CrossRefGoogle Scholar
  60. Taborsky M (2001) The evolution of parasitic and cooperative reproductive behaviors in fishes. J Hered 92:100–110PubMedCrossRefGoogle Scholar
  61. Taborsky M, Limberger D (1981) Helpers in fish. Behav Ecol Sociobiol 8:143–145Google Scholar
  62. Tommkins JL, Simmons LW (2002) Measuring relative investment: a case study of testes investment in species with alternative male reproductive tactics. Anim Behav 63:1009–1016CrossRefGoogle Scholar
  63. van Oppen MJH, Rico C, Deutsch JC, Turner GF, Hewitt GM (1997) Isolation and characterization of microsatellite loci in the cichlid fish Pseudotropheus zebra. Mol Ecol 6:387–388PubMedCrossRefGoogle Scholar
  64. West SA, Pen I, Griffin AS (2002) Cooperation and competition between relatives. Science 296:72–75PubMedCrossRefGoogle Scholar
  65. Wisenden BD (1999) Alloparental care in fishes. Rev Fish Biol Fish 9:45–70CrossRefGoogle Scholar
  66. Wong M, Balshine S (2010) The evolution of cooperative breeding in the African cichlid fish, Neolamprologus pulcher. Biol Rev 86:511–530PubMedCrossRefGoogle Scholar
  67. Woolfenden GE, Fitzpatrick JW (1990) Florida Scrub Jays: a synopsis after 18 years of study. In: Stacey PB, Koenig WD (eds) Cooperative breeding in birds: long-term studies of ecology and behavior. Cambridge University Press, New York, pp 241–266Google Scholar
  68. Yamagishi S, Kohda M (1996) Is the cichlid fish Julidochromis marlieri polyandrous? Ichthyol Res 43:469–471CrossRefGoogle Scholar
  69. Zardoya R, Vollmer DM, Craddock C, Streelman JT, Karl S, Meyer A (1996) Evolutionary conservation of microsatellite flanking regions and their use in resolving the phylogeny of cichlid fishes (Pisces: Perciformis). Proc R Soc Lond B 263:1589–1598CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Hirokazu Tanaka
    • 1
  • Dik Heg
    • 2
  • Hirohiko Takeshima
    • 3
  • Tomohiro Takeyama
    • 1
  • Satoshi Awata
    • 4
  • Mutsumi Nishida
    • 3
  • Masanori Kohda
    • 1
  1. 1.Laboratory of Animal Sociology, Department of Biology and Geosciences, Graduate School of ScienceOsaka City UniversityOsakaJapan
  2. 2.Department of Clinical Research, Clinical Trials UnitUniversity of BernBernSwitzerland
  3. 3.Atmosphere and Ocean Research InstituteUniversity of TokyoKashiwa-shiJapan
  4. 4.Sado Marine Biological Station, Faculty of ScienceNiigata UniversitySadoJapan

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