Advertisement

Multiple paternity in the cooperatively breeding fish Neolamprologus pulcher

  • P. Dierkes
  • M. TaborskyEmail author
  • R. Achmann
Original Paper

Abstract

In cooperative breeders, mature males may compete for fertilizations. In this study, we measured the degree of multiple paternity in a natural population of a cooperatively breeding fish. Neolamprologus pulcher (Perciformes: Cichlidae) is a highly social cichlid endemic to Lake Tanganyika. We used highly variable microsatellite loci to survey 12 groups with an average number of 10.6 brood care helpers per group and a total of 43 offspring (mean 3.6 per brood). In 11 of 12 groups, all young were assigned to the dominant female. The dominant male sired all offspring in three groups, part of the offspring in four groups, and in five groups, he had no paternity at all. In total, 44.2% of young were not fathered by the current male territory owner. Multiple paternity was found in 5 of 12 broods (41.7 %), with 8 of 35 young (22.9 %) being sired by males other than the respective territory owners. This is an exceptionally high rate of extra-pair paternity among cooperatively breeding vertebrates. Neither helpers present in these territories during collection nor neighbouring males were unequivocally assigned to have sired these extra-pair young. However, behavioural observations suggest that male helpers may have produced these young before being expelled from the territory in response to this reproductive parasitism. We discuss these results in the light of reproductive skew theory, cooperative breeding in vertebrates and alternative reproductive tactics in fish.

Keywords

Parentage Microsatellites Cichlids Lake Tanganyika Alternative mating tactics 

Notes

Acknowledgements

We would like to thank Matthias Müller and Gottfried Brem for providing lab facilities. Andrea Kunz assisted in the field. Dolores Schütz, Gudrun Pachler and Sigal Balshine-Earn contributed by numerous discussions. Special thanks to Eva Skubic and Dik Heg for discussion, help and constructive comments on the manuscript. The work was funded by the Austrian Science Fund (FWF: project P10916-BIO) and the Swiss National Science Foundation (SNSF: project 3100A0-105626). This study complies with the current laws of Zambia, Austria and Switzerland.

References

  1. Avise JC, Jones AG, Walker D, DeWoody JA, Dakin B, Fiumera A, Fletcher D, Mackiewicz M, Pearse D, Porter B, Wilkins SD (2002) Genetic mating systems and reproductive natural histories of fishes: lessons for ecology and evolution. Annu Rev Genet 36:19–45PubMedCrossRefGoogle Scholar
  2. Awata S, Munehara H, Kohda M (2005) Social system and reproduction of helpers in a cooperatively breeding fish (Julidochromis ornatus) in Lake Tanganyika: field observations and parentage analyses. Behav Ecol Sociobiol 58:506–516CrossRefGoogle Scholar
  3. Balshine-Earn S, Neat FC, 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 9:432–438CrossRefGoogle Scholar
  4. Balshine-Earn S, Leach B, Neat F, Reid H, Taborsky M, Werner N (2001) Correlates of group size in a cooperatively breeding cichlid fish. Behav Ecol and Sociobiol 50:134–140CrossRefGoogle Scholar
  5. Bergmüller R, Taborsky M (2005) Experimental manipulation of helping in a cooperative breeder: helpers ‘pay to stay’ by pre-emptive appeasement. Anim Behav 69:19–28CrossRefGoogle Scholar
  6. Bergmuller R, Heg D, Taborsky M (2005a) Helpers in a cooperatively breeding cichlid stay and pay or disperse and breed, depending on ecological constraints. Proc R Soc B 272:325–331PubMedCrossRefGoogle Scholar
  7. Bergmuller R, Heg D, Peer K, Taborsky M (2005b) Extended safe havens and between-group dispersal of helpers in a cooperatively breeding cichlid. Behaviour 142:1643–1667CrossRefGoogle Scholar
  8. Brandtmann G, Scandura M, Trillmich F (1999) The female–female conflict in the harem of a snail cichlid (Lamprologus ocellatus): behavioural interactions and fitness consequences. Behaviour 136:1123–1144CrossRefGoogle Scholar
  9. Brooker MG, Rowley I, Adams M, Baversock PR (1990) Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species? Behav Ecol Sociobiol 26:191–199Google Scholar
  10. Brouwer L, Heg D, Taborsky M (2005) Experimental evidence for helper effects in a cooperatively breeding cichlid. Behav Ecol 16:667–673CrossRefGoogle Scholar
  11. Bruce JP, Quinn JS, Sloane SA, White BN (1996) DNA fingerprinting reveals monogamy in the bushtit, a cooperatively breeding species. Auk 113:511–516Google Scholar
  12. Cant MA (1998) A model for the evolution of reproductive skew without reproductive suppression. Anim Behav 55:163–169PubMedCrossRefGoogle Scholar
  13. Clutton-Brock TH (1998) Reproductive skew, concessions and limited control. Trends Ecol Evol 13:288–292CrossRefGoogle Scholar
  14. Clutton-Brock TH, Gaynor D, Kansky R, MacColl ADC, McIlrath G, Chadwick P, Brotherton PNM, O'Riain JM, Manser M, Skinner JD (1998) Costs of cooperative behaviour in suricates (Suricata suricatta). Proc R Soc B 265:185–190PubMedCrossRefGoogle Scholar
  15. Clutton-Brock TH, Russell AF, Sharpe LL, Brotherton PNM, McIlrath GM, White S, Cameron EZ (2001) Effects of helpers on juvenile development and survival in meerkats. Science 293:2446–2449PubMedCrossRefGoogle Scholar
  16. Clutton-Brock TH, Hodge SJ, Spong G, Russell AF, Jordan NR, Bennett NC, Sharpe LL, Manser MB (2006) Intrasexual competition and sexual selection in cooperative mammals. Nature 444:1065–1068PubMedCrossRefGoogle Scholar
  17. Conrad KF, Clarke MF, Robertson RJ, Boag PT (1998) Paternity and the relatedness of helpers in the cooperatively breeding bell miner. Condor 100:343–349CrossRefGoogle Scholar
  18. Dierkes P, Taborsky M, Kohler U (1999) Reproductive parasitism of broodcare helpers in a cooperatively breeding fish. Behav Ecol 10:510–515CrossRefGoogle Scholar
  19. 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. Ecology Letters 8:968–975CrossRefGoogle Scholar
  20. Duftner N, Sefc KM, 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 Phylogen Evol 45:706–715CrossRefGoogle Scholar
  21. Ellegren H (2000) Heterogeneous mutation processes in microsatellite DNA sequences. Nat Genet 24:400–402PubMedCrossRefGoogle Scholar
  22. Emlen ST (1982) The evolution of helping. I. An ecological constraints model. Am Nat 119:29–39Google Scholar
  23. Gaston AJ (1978a) Demography of the jungle babbler, Turdoides striatus. J Anim Ecol 47:845–870CrossRefGoogle Scholar
  24. Gaston AJ (1978b) The evolution of group territorial behavior and cooperative breeding. Am Nat 112:1091–1100CrossRefGoogle Scholar
  25. 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
  26. Haig SM, Walters JR, Plissner JH (1994) Genetic evidence for monogamy in the cooperatively breeding red-cockaded woodpecker. Behav Ecol Sociobiol 34:295–303CrossRefGoogle Scholar
  27. Hamilton WD (1964) The genetical evolution of social behaviour I and II. J Theor Biol 7:1–52PubMedCrossRefGoogle Scholar
  28. Haydock J, Parker G, Rabenold KN (1996) Extra pair paternity uncommon in the cooperatively breeding bicolored wren. Behav Ecol Sociobiol 38:1–16CrossRefGoogle 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 B 271:2367–2374PubMedCrossRefGoogle Scholar
  30. Heg D, Bergmuller R, Bonfils D, Otti O, Bachar Z, Burri R, Heckel G, Taborsky M (2006) Cichlids do not adjust reproductive skew to the availability of independent breeding options. Behav Ecol 17:419–429CrossRefGoogle Scholar
  31. Heinsohn R, Cockburn A (1994) Helping is costly to young birds in cooperatively breeding white-winged choughs. Proc R Soc Lond B 256:293–298CrossRefGoogle Scholar
  32. Jones AG (2005) GERUD 2.0: a computer program for the reconstruction of parental genotypes from half-sib progeny arrays with known or unknown parents. Mol Ecol Notes 5:708–711CrossRefGoogle Scholar
  33. Johnstone RA (2000) Models of reproductive skew: A review and synthesis. Ethology 106:5–26CrossRefGoogle Scholar
  34. Johnstone RA, Cant MA (1999) Reproductive skew and the threat of eviction: a new perspective. Proc R Soc B 266:275–279CrossRefGoogle Scholar
  35. Keller L, Reeve HK (1994) Partitioning of reproduction in animal societies. Trends Ecol Evol 9:98–103CrossRefGoogle Scholar
  36. Kohler U (1998) Zur Struktur und Evolution des Sozialsystems von Neolamprologus multifasciatus (Cichlidae, Pisces), dem kleinsten Schneckenbuntbarsch des Tanganjikasees. PhD thesis, Ludwig-Maximilians Universität München, GermanyGoogle Scholar
  37. Komdeur J (1996) Influence of helping and breeding experience on reproductive performance in the Seychelles warbler: a translocation experiment. Behav Ecol 7:326–333CrossRefGoogle Scholar
  38. Komdeur J (2006) Variation in individual investment strategies among social animals. Ethology 112:729–747CrossRefGoogle Scholar
  39. Lawton MF, Guindon CF (1981) Flock composition, breeding success, and learning in the brown jay. Condor 83:27–33CrossRefGoogle Scholar
  40. Legge S, Cockburn A (2000) Social and mating system of cooperatively breeding laughing kookaburra (Dacelo novaeguineae). Behav Ecol Sociobiol 47:220–229CrossRefGoogle Scholar
  41. Limberger D (1983) Pairs and harems in a cichlid fish, Lamprologus brichardi. Z Tierpsychol 62:115–144Google Scholar
  42. Lundy KJ, Parker PG, Zahavi A (1998) Reproduction by subordinates in cooperatively breeding Arabian babblers is uncommon but predictable. Behav Ecol Sociobiol 43:173–180CrossRefGoogle Scholar
  43. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655PubMedCrossRefGoogle Scholar
  44. Martin E, Taborsky M (1997) Alternative male mating tactics in a cichlid, Pelvicachromis pulcher: a comparison of reproductive effort and success. Behav Ecol Sociobiol 41:311–319CrossRefGoogle Scholar
  45. Mulder RA, Dunn PO, Cockburn A, Lazenby-Cohen KA, Howell MJ (1994) Helpers liberate female fairy wrens from constraints on extra-pair mate choice. Proc R Soc Lond B 255:223–229CrossRefGoogle Scholar
  46. Mulder RA, Langmore N (1993) Dominant males punish helpers for temporary defection in superb fairy-wrens. Anim Behav 45:830–833CrossRefGoogle Scholar
  47. O’Riain MJ, Bennett NC, Brotherton PNM, McIlrath G, Clutton-Brock TH (2000) Reproductive suppression and inbreeding avoidance in wild populations of co- operatively breeding meerkats (Suricata suricatta). Behav Ecol Sociobiol 48:471–477CrossRefGoogle Scholar
  48. Parker A, Kornfield I (1996) Polygynandry in Pseudotropheus zebra, a cichlid fish from Lake Malawi. Environ Biol Fishes 47:345–352CrossRefGoogle Scholar
  49. Poldmaa T, Montgomerie R, Boag P (1995) Mating system of the cooperatively breeding noisy miner Manorina melanocephala, as revealed by DNA profiling. Behav Ecol Sociobiol 337:137–143CrossRefGoogle Scholar
  50. Rabenold PP, Rabenold KN, Piper WH, Haydock J, Zack SW (1990) Shared paternity revealed by genetic analysis in cooperatively breeding tropical wrens. Nature 348:538–540CrossRefGoogle Scholar
  51. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249Google Scholar
  52. Reeve HK, Emlen ST, Keller L (1998) Reproductive sharing in animal societies: reproductive incentives or incomplete control by dominant breeders? Behav Ecol 9:267–278CrossRefGoogle Scholar
  53. Reyer HU (1984) Investment and relatedness: a cost/benefit analysis of breeding and helping in the pied kingfisher (Ceryle rudis). Anim Behav 32:1163–1178CrossRefGoogle Scholar
  54. Richardson DS, Jury FL, Blakmeer K, Komdeur J, Burke T (2001) Parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis). Mol Ecol 10:2263–2273PubMedCrossRefGoogle Scholar
  55. Rood JP (1990) Group size, survival, reproduction and routes to breeding in dwarf mongooses. Anim Behav 39:566–572CrossRefGoogle Scholar
  56. Russell AF, Hatchwell BJ (2001) Experimental evidence for kin-biased helping in a cooperatively breeding vertebrate. Proc R Soc B 268:2169–2174PubMedCrossRefGoogle Scholar
  57. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  58. Schliewen UK, Rassmann K, Markmann M, Markert J, Kocher TD, Tautz D (2001) Genetic and ecological divergence of a monophyletic cichlid species pair under fully sympatric conditions in Lake Ejagham, Cameroon. Mol Ecol 10:1471–1488PubMedCrossRefGoogle Scholar
  59. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–92CrossRefGoogle Scholar
  60. Skubic E, Taborsky M, McNamara JM, Houston AI (2004) When to parasitize? A dynamic optimization model of reproductive strategies in a cooperative breeder. J Theor Biol 227:487–501PubMedCrossRefGoogle Scholar
  61. Stiver KA, Dierkes P, Taborsky M, Balshine S (2004) Dispersal pattern and status change in a co-operatively breeding cichlid fish. Neolamprologus pulcher: evidence form microsatellite analyses and behavioural observations. J Fish Biol 65:91–105CrossRefGoogle Scholar
  62. Stiver KA, Dierkes P, Taborsky M, Gibbs HL, Balshine S (2005) Relatedness and helping in fish: examining the theoretical predictions. Proc R Soc B 272:1593–1599PubMedCrossRefGoogle Scholar
  63. Taborsky M (1984) Broodcare helpers in the cichlid fish Lamprologus brichardi—their costs and benefits. Anim Behav 32:1236–1252CrossRefGoogle Scholar
  64. Taborsky M (1985) Breeder–helper conflict in a cichlid fish with broodcare helpers—an experimental analysis. Behaviour 95:45–75CrossRefGoogle Scholar
  65. Taborsky M (1994) Sneakers, satellites, and helpers: parasitic and cooperative behavior in fish reproduction. Adv Stud Behav 23:1–100CrossRefGoogle Scholar
  66. Taborsky M (1997) Bourgeois and parasitic tactics: do we need collective, functional terms for alternative reproductive behaviours? Behav Ecol Sociobiol 41:361–362CrossRefGoogle Scholar
  67. Taborsky M (1998) Sperm competition in fish: bourgeois males and parasitic spawning. Trends in Ecology and Evolution 13:222–227CrossRefGoogle Scholar
  68. Taborsky M (1999) Conflict or cooperation: what determines optimal solutions to competition in fish reproduction? In: Oliveira RF, Almada V, Goncalves E (eds) Behaviour and conservation of littoral fishes. ISPA, Lisboa, pp 301–349Google Scholar
  69. Taborsky M (2001) The evolution of bourgeois, parasitic and cooperative reproductive behaviors in fishes. J Heredity 92:100–110CrossRefGoogle Scholar
  70. Taborsky M (2008) Alternative reproductive tactics in fish. In: Oliveira RF, Taborsky M, Brockmann HJ (eds) Alternative reproductive tactics: an integrative approach. Cambridge University Press, Cambridge, pp 251–299Google Scholar
  71. Taborsky M, Limberger D (1981) Helpers in Fish. Behav Ecol Sociobiol 8:143–145CrossRefGoogle Scholar
  72. Taborsky M, Grantner A (1998) Behavioural time-energy budgets of cooperatively breeding Neolamprologus pulcher (Pisces: Cichlidae). Anim Behav 56:1375–1382PubMedCrossRefGoogle Scholar
  73. Vehrencamp SL (1983a) A model for the evolution of despotic versus egalitarian societies. Anim Behav 31:667–682CrossRefGoogle Scholar
  74. Vehrencamp SL (1983b) Optimal degree of skew in cooperative societies. Am Zool 23:327–335Google Scholar
  75. West SA, Pen I, Griffin AS (2002) Cooperation and competition between relatives. Science 296:72–75PubMedCrossRefGoogle Scholar
  76. Woolfenden GE, Fitzpatrick JW (1978) The inheritance of territory in group-breeding birds. Biosci 28:104–108CrossRefGoogle Scholar
  77. Wrege PH, Emlen TE (1987) Biochemical determination of parental uncertainty in white-fronted bee-eaters. Behav Ecol Sociobiol 20:153–160CrossRefGoogle Scholar
  78. Young AJ, Carlson AA, Monfort SL, Russell AF, Bennett NC, Clutton-Brock T (2006) Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proc Natl Acad Sci U S A 103:12005–12010PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Konrad Lorenz Institut für Vergleichende VerhaltensforschungViennaAustria
  2. 2.Department of Behavioural Ecology, Institute of ZoologyUniversity of BerneHinterkappelen/BernSwitzerland
  3. 3.Ludwig-Boltzmann-Institute for Cyto-, Immuno- and Molecular Genetic ResearchUniversity of Veterinary MedicineViennaAustria

Personalised recommendations