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.
References
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 36:19–45
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 58:506–516
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 9:432–438
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 50:134–140
Bergmüller R, Taborsky M (2005) Experimental manipulation of helping in a cooperative breeder: helpers ‘pay to stay’ by pre-emptive appeasement. Anim Behav 69:19–28
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 272:325–331
Bergmuller R, Heg D, Peer K, Taborsky M (2005b) Extended safe havens and between-group dispersal of helpers in a cooperatively breeding cichlid. Behaviour 142:1643–1667
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 136:1123–1144
Brooker MG, Rowley I, Adams M, Baversock PR (1990) Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species? Behav Ecol Sociobiol 26:191–199
Brouwer L, Heg D, Taborsky M (2005) Experimental evidence for helper effects in a cooperatively breeding cichlid. Behav Ecol 16:667–673
Bruce JP, Quinn JS, Sloane SA, White BN (1996) DNA fingerprinting reveals monogamy in the bushtit, a cooperatively breeding species. Auk 113:511–516
Cant MA (1998) A model for the evolution of reproductive skew without reproductive suppression. Anim Behav 55:163–169
Clutton-Brock TH (1998) Reproductive skew, concessions and limited control. Trends Ecol Evol 13:288–292
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 265:185–190
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 293:2446–2449
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 444:1065–1068
Conrad KF, Clarke MF, Robertson RJ, Boag PT (1998) Paternity and the relatedness of helpers in the cooperatively breeding bell miner. Condor 100:343–349
Dierkes P, Taborsky M, Kohler U (1999) Reproductive parasitism of broodcare helpers in a cooperatively breeding fish. Behav Ecol 10:510–515
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 8:968–975
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 45:706–715
Ellegren H (2000) Heterogeneous mutation processes in microsatellite DNA sequences. Nat Genet 24:400–402
Emlen ST (1982) The evolution of helping. I. An ecological constraints model. Am Nat 119:29–39
Gaston AJ (1978a) Demography of the jungle babbler, Turdoides striatus. J Anim Ecol 47:845–870
Gaston AJ (1978b) The evolution of group territorial behavior and cooperative breeding. Am Nat 112:1091–1100
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 168:427–433
Haig SM, Walters JR, Plissner JH (1994) Genetic evidence for monogamy in the cooperatively breeding red-cockaded woodpecker. Behav Ecol Sociobiol 34:295–303
Hamilton WD (1964) The genetical evolution of social behaviour I and II. J Theor Biol 7:1–52
Haydock J, Parker G, Rabenold KN (1996) Extra pair paternity uncommon in the cooperatively breeding bicolored wren. Behav Ecol Sociobiol 38:1–16
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 271:2367–2374
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 17:419–429
Heinsohn R, Cockburn A (1994) Helping is costly to young birds in cooperatively breeding white-winged choughs. Proc R Soc Lond B 256:293–298
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 5:708–711
Johnstone RA (2000) Models of reproductive skew: A review and synthesis. Ethology 106:5–26
Johnstone RA, Cant MA (1999) Reproductive skew and the threat of eviction: a new perspective. Proc R Soc B 266:275–279
Keller L, Reeve HK (1994) Partitioning of reproduction in animal societies. Trends Ecol Evol 9:98–103
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, Germany
Komdeur J (1996) Influence of helping and breeding experience on reproductive performance in the Seychelles warbler: a translocation experiment. Behav Ecol 7:326–333
Komdeur J (2006) Variation in individual investment strategies among social animals. Ethology 112:729–747
Lawton MF, Guindon CF (1981) Flock composition, breeding success, and learning in the brown jay. Condor 83:27–33
Legge S, Cockburn A (2000) Social and mating system of cooperatively breeding laughing kookaburra (Dacelo novaeguineae). Behav Ecol Sociobiol 47:220–229
Limberger D (1983) Pairs and harems in a cichlid fish, Lamprologus brichardi. Z Tierpsychol 62:115–144
Lundy KJ, Parker PG, Zahavi A (1998) Reproduction by subordinates in cooperatively breeding Arabian babblers is uncommon but predictable. Behav Ecol Sociobiol 43:173–180
Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655
Martin E, Taborsky M (1997) Alternative male mating tactics in a cichlid, Pelvicachromis pulcher: a comparison of reproductive effort and success. Behav Ecol Sociobiol 41:311–319
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 255:223–229
Mulder RA, Langmore N (1993) Dominant males punish helpers for temporary defection in superb fairy-wrens. Anim Behav 45:830–833
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 48:471–477
Parker A, Kornfield I (1996) Polygynandry in Pseudotropheus zebra, a cichlid fish from Lake Malawi. Environ Biol Fishes 47:345–352
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 337:137–143
Rabenold PP, Rabenold KN, Piper WH, Haydock J, Zack SW (1990) Shared paternity revealed by genetic analysis in cooperatively breeding tropical wrens. Nature 348:538–540
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249
Reeve HK, Emlen ST, Keller L (1998) Reproductive sharing in animal societies: reproductive incentives or incomplete control by dominant breeders? Behav Ecol 9:267–278
Reyer HU (1984) Investment and relatedness: a cost/benefit analysis of breeding and helping in the pied kingfisher (Ceryle rudis). Anim Behav 32:1163–1178
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 10:2263–2273
Rood JP (1990) Group size, survival, reproduction and routes to breeding in dwarf mongooses. Anim Behav 39:566–572
Russell AF, Hatchwell BJ (2001) Experimental evidence for kin-biased helping in a cooperatively breeding vertebrate. Proc R Soc B 268:2169–2174
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
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 10:1471–1488
Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–92
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 227:487–501
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 65:91–105
Stiver KA, Dierkes P, Taborsky M, Gibbs HL, Balshine S (2005) Relatedness and helping in fish: examining the theoretical predictions. Proc R Soc B 272:1593–1599
Taborsky M (1984) Broodcare helpers in the cichlid fish Lamprologus brichardi—their costs and benefits. Anim Behav 32:1236–1252
Taborsky M (1985) Breeder–helper conflict in a cichlid fish with broodcare helpers—an experimental analysis. Behaviour 95:45–75
Taborsky M (1994) Sneakers, satellites, and helpers: parasitic and cooperative behavior in fish reproduction. Adv Stud Behav 23:1–100
Taborsky M (1997) Bourgeois and parasitic tactics: do we need collective, functional terms for alternative reproductive behaviours? Behav Ecol Sociobiol 41:361–362
Taborsky M (1998) Sperm competition in fish: bourgeois males and parasitic spawning. Trends in Ecology and Evolution 13:222–227
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 301–349
Taborsky M (2001) The evolution of bourgeois, parasitic and cooperative reproductive behaviors in fishes. J Heredity 92:100–110
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 251–299
Taborsky M, Limberger D (1981) Helpers in Fish. Behav Ecol Sociobiol 8:143–145
Taborsky M, Grantner A (1998) Behavioural time-energy budgets of cooperatively breeding Neolamprologus pulcher (Pisces: Cichlidae). Anim Behav 56:1375–1382
Vehrencamp SL (1983a) A model for the evolution of despotic versus egalitarian societies. Anim Behav 31:667–682
Vehrencamp SL (1983b) Optimal degree of skew in cooperative societies. Am Zool 23:327–335
West SA, Pen I, Griffin AS (2002) Cooperation and competition between relatives. Science 296:72–75
Woolfenden GE, Fitzpatrick JW (1978) The inheritance of territory in group-breeding birds. Biosci 28:104–108
Wrege PH, Emlen TE (1987) Biochemical determination of parental uncertainty in white-fronted bee-eaters. Behav Ecol Sociobiol 20:153–160
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 103:12005–12010
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.
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Dierkes, P., Taborsky, M. & Achmann, R. Multiple paternity in the cooperatively breeding fish Neolamprologus pulcher . Behav Ecol Sociobiol 62, 1581–1589 (2008). https://doi.org/10.1007/s00265-008-0587-3
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DOI: https://doi.org/10.1007/s00265-008-0587-3