, Volume 176, Issue 4, pp 965–974 | Cite as

Sex biases in kin shoaling and dispersal in a cichlid fish

  • Wouter F. D. van DongenEmail author
  • Richard H. Wagner
  • Yoshan Moodley
  • Franziska C. Schaedelin
Behavioral ecology - Original research


Animal dispersal is associated with diverse costs and benefits that vary among individuals based on phenotype and ecological conditions. For example, females may disperse when males benefit more from defending territories in familiar environments. Similarly, size differences in dispersal propensity may occur when dispersal costs are size-dependent. When individuals do disperse, they may adopt behavioral strategies that minimize dispersal costs. Dispersing fish, for example, may travel within shoals to reduce predation risks. Further, kin shoaling may augment inclusive fitness by reducing predation of relatives. However, studies are lacking on the role of kin shoaling in dispersal. We explored how sex and size influence dispersal and kin shoaling in the cichlid Neolamprologus caudopunctatus. We microsatellite genotyped over 900 individuals from two populations separated by a potential dispersal barrier, and documented patterns of population structure, migration and within-shoal relatedness. Genetic differentiation across the barrier was greater for smaller than larger fish, suggesting larger fish had dispersed longer distances. Females exhibited weaker genetic differentiation and 11 times higher migration rates than males, indicating longer-distance female-biased dispersal. Small females frequently shoaled with siblings, possibly offsetting dispersal costs associated with higher predation risks. In contrast, small males appeared to avoid kin shoaling, possibly to avoid local resource competition. In summary, long-distance dispersal in N. caudopunctatus appears to be female-biased, and kin-based shoaling by small females may represent a behavioral adaptation that reduces dispersal costs. Our study appears to be the first to provide evidence that sex differences in dispersal influence sex differences in kin shoaling.


Animal movements Fish shoals Grouping behavior Kin selection Population genetics 



We thank Florian Sammer for conducting the laboratory work for this study, Valeria Montana for assistance with the IM analyses and Marlene Mann for helping with many aspects of the project. We are grateful to Stefan Fischer, Stefanie Schwamberger, Peter Turai and Hartmut Lemmel for their great field assistance, John, Enoch, and Maxwell Juma for their support in the field, and Bornfirst and family for managing the Tanganyika Lodge. We thank Michael and Barbara Taborsky for the provision of diving bottles and Drs Harris Phiri, Patrick Nagalda, and Justina Kasabila of the Zambian Ministry of Agriculture, Food and Fisheries, as well as Rueben Shappola and the Department of Fisheries in Mpulungu for their logistical support of our research. Thank you to Andrea Manica and three anonymous referees for their comments on earlier versions of this manuscript. This project was funded by the Austrian Academy of Sciences, the Veterinary University of Vienna and by the Austrian Science Fund (FWF; projects P17468 and P20401).

Supplementary material

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Supplementary material 1 (PDF 18 kb)
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Supplementary material 2 (PDF 40 kb)
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Supplementary material 3 (PDF 23 kb)


  1. Arnold KE (2000) Kin recognition in rainbowfish (Melanotaenia eachamensis): sex, sibs and shoaling. Behav Ecol Sociobiol 48:385–391CrossRefGoogle Scholar
  2. Aubin-Horth N, Desjardins JK, Martei YM, Balshine S, Hofmann HA (2007) Masculinized dominant females in a cooperatively breeding species. Mol Ecol 16:1349–1358PubMedCrossRefGoogle Scholar
  3. Banks SC, Lindenmayer DB (2014) Inbreeding avoidance, patch isolation and matrix permeability influence dispersal and settlement choices by male agile antechinus in a fragmented landscape. J Anim Ecol 83:515–524CrossRefGoogle Scholar
  4. Belkhir K, Castric V, Bonhomme F (2002) IDENTIX, a software to test for relatedness in a population using permutation methods. Mol Ecol Notes 2:611–614CrossRefGoogle Scholar
  5. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05. Université de Montpellier IIGoogle Scholar
  6. Bisol GD, Capocasa M, Anagnostou P (2012) When gender matters: new insights into the relationships between social systems and the genetic structure of human populations. Mol Ecol 21:4917–4920CrossRefGoogle Scholar
  7. Bonte D, Van Dyck H, Bullock JM, Coulon A, Delgado M, Gibbs M, Lehouck V, Matthysen E, Mustin K, Saastamoinen M, Schtickzelle N, Stevens VM, Vandewoestijne S, Baguette M, Barton K, Benton TG, Chaput-Bardy A, Clobert J, Dytham C, Hovestadt T, Meier CM, Palmer SCF, Turlure C, Travis JMJ (2012) Costs of dispersal. Biol Rev 87:290–312PubMedCrossRefGoogle Scholar
  8. Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev Camb Phil Soc 80:205–225CrossRefGoogle Scholar
  9. Carleton KL, Streelman JT, Lee BY, Garnhart N, Kidd M, Kocher TD (2002) Rapid isolation of CA microsatellites from the tilapia genome. Anim Genet 33:140–144PubMedCrossRefGoogle Scholar
  10. Consuegra S, García de Leániz C (2007) Fluctuating sex ratios, but not sex-biased dispersal, in a promiscuous fish. Evol Ecol 21:229–245CrossRefGoogle Scholar
  11. Duchesne P, Étienne C, Bernatchez L (2006) PERM: a computer program to detect structuring factors in meaningful social units. Mol Ecol Notes 6:965–976CrossRefGoogle Scholar
  12. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  13. Excoffier L, Lischer HEL (2010) Arlequin suite version 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567CrossRefGoogle Scholar
  14. Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, SeattleGoogle Scholar
  15. Fisher R, Bellwood DR, Job SD (2000) Development of swimming abilities in reef fish larvae. Mar Ecol Prog Ser 202:163–173CrossRefGoogle Scholar
  16. Frommen JG, Bakker TCM (2004) Adult three-spined sticklebacks prefer to shoal with familiar kin. Behaviour 141:1401–1409CrossRefGoogle Scholar
  17. Frommen JG, Luz C, Bakker TCM (2007) Nutritional state influences shoaling preference for familiars. Zoology 110:369–376PubMedCrossRefGoogle Scholar
  18. Gerlach G, Lysiak N (2006) Kin recognition and inbreeding avoidance in zebrafish, Danio rerio, is based on phenotype matching. Anim Behav 71:1371–1377CrossRefGoogle Scholar
  19. Gerlach G, Hodgins-Davis A, MacDonald B, Hannah RC (2007) Benefits of kin association: related and familiar zebra fish (Danio rerio) show improved growth. Behav Ecol Sociobiol 61:1765–1770CrossRefGoogle Scholar
  20. Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-Statistics. J Hered 86:485–486Google Scholar
  21. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162CrossRefGoogle Scholar
  22. Griffiths SW, Magurran AE (1998) Sex and schooling behaviour in the Trinidadian guppy. Anim Behav 56:689–693PubMedCrossRefGoogle Scholar
  23. Gundersen G, Andreassen HP, Ims RA (2002) Individual and population level determinants of immigration success on local habitat patches: an experimental approach. Ecol Lett 5:294–301CrossRefGoogle Scholar
  24. Handley LJL, Perrin N (2007) Advances in our understanding of mammalian sex-biased dispersal. Mol Ecol 16:1559–1578CrossRefGoogle Scholar
  25. Hatchwell BJ (2010) Cryptic kin selection: kin structure in vertebrate populations and opportunities for kin-directed cooperation. Ethology 116:203–216CrossRefGoogle Scholar
  26. Helfman GB, Collette BB, Facey DE (1997) The diversity of fishes. Blackwell, MaldenGoogle Scholar
  27. Hey J, Nielsen EE (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc Natl Acad Sci USA 104:2785–2790PubMedCentralPubMedCrossRefGoogle Scholar
  28. Hiddink JG, Kock RP, Wolff WJ (2002) Active pelagic migrations of the bivalve Macoma balthica are dangerous. Mar Biol 140:1149–1156CrossRefGoogle Scholar
  29. Jadwiszczack P (2002) Rundom projects: An application for randomization and bootstrap testing.
  30. Kalinowski S, Taper M, Marshall T (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106PubMedCrossRefGoogle Scholar
  31. Koblmueller S, Sefc KM, Duftner N, Warum M, Sturmbauer C (2006) Genetic population structure as indirect measure of dispersal ability in a Lake Tanganyika cichlid. Genetica 128:121–131Google Scholar
  32. Konings A (1998) Tanganyika cichlids in their natural habitat. Cichlid Press, El PasoGoogle Scholar
  33. Koops MA, Grant JWA (1993) Weight asymmetry and sequential assessment in convict cichlid contests. Can J Zool 71:475–479CrossRefGoogle Scholar
  34. Lee WJ, Kocher TD (1996) Microsatellite DNA markers for genetic mapping in Oreochromis niloticus. J Fish Biol 49:169–171Google Scholar
  35. Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766PubMedCentralPubMedGoogle Scholar
  36. Mathieu E, Autem M, Roux M, Bonhomme F (1990) Preuves de validation dans l’analyse de structures génétiques multivariées: comment tester l’équilibre panmictique? Rev Statist Appl 38:47–66Google Scholar
  37. Nagy M, Gunther L, Knornschild M, Mayer F (2013) Female-biased dispersal in a bat with a female-defence mating strategy. Mol Ecol 22:1733–1745PubMedCrossRefGoogle Scholar
  38. Nielsen EG, Bach LA, Kotlicki P (2006) Hybridlab (version 1.0): a program for generating simulated hybrids from population samples. Mol Ecol Notes 6:971–973CrossRefGoogle Scholar
  39. Ochi H, Yanagisawa Y (1999) Sand-transfer behavior outside the nest by guarding parents of the Tanganyikan cichlid, Neolamprologus caudopunctatus. Ichthyol Res 46:419–422CrossRefGoogle Scholar
  40. Parker A, Kornfield I (1996) Polygynandry in Pseudotropheus zebra, a cichlid fish from Lake Malawi. Environ Biol Fish 47:345–352CrossRefGoogle Scholar
  41. Pitcher TJ, Parrish JK (1993) Functions of shoaling behaviour in teleosts. In: Pitcher TJ (ed) The behaviour of teleost fishes, 2nd edn. Croom Helm, London, pp 363–439CrossRefGoogle Scholar
  42. Piyapong C, Butlin RK, Faria JJ, Scruton KJ, Wang J, Krause J (2011) Kin assortment in juvenile shoals in wild guppy populations. Heredity 106:749–756PubMedCentralPubMedCrossRefGoogle Scholar
  43. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  44. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  45. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedCentralPubMedGoogle Scholar
  46. Rowland WJ (1989) The effects of body size, aggression and nuptial coloration on competition for territories in male threespine sticklebacks, Gasterosteus aculeatus. Anim Behav 37:282–289CrossRefGoogle Scholar
  47. Ruhl N, McRobert SP (2005) The effect of sex and shoal size on shoaling behaviour in Danio rerio. J Fish Biol 67:1318–1326CrossRefGoogle Scholar
  48. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  49. Schaedelin FC, van Dongen WFD, Wagner RH (2013) Non-random brood mixing suggests adoption in a colonial cichlid. Behav Ecol 24:540–546CrossRefGoogle Scholar
  50. Scharf FS, Juanes F, Rountree RA (2000) Predator size - prey size relationships of marine fish predators: interspecific variation and effects of ontogeny and body size on trophic-niche breadth. Mar Ecol Prog Ser 208:229–248CrossRefGoogle Scholar
  51. Schliewen U, Rassmann K, Markmann M, Markert J, Kocher T, 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
  52. Schradin C, Lamprecht J (2000) Female-biased immigration and male peace-keeping in groups of the shell-dwelling cichlid fish Neolamprologus multifasciatus. Behav Ecol Sociobiol 48:236–242CrossRefGoogle Scholar
  53. Sheridan CM, Spotila JR, Bien WF, Avery HW (2010) Sex-biased dispersal and natal philopatry in the diamondback terrapin, Malaclemys terrapin. Mol Ecol 19:5497–5510PubMedCrossRefGoogle Scholar
  54. Stiver KA, Dierkest P, Taborsky M, Balshine S (2004) Dispersal patterns and status change in a co-operatively breeding cichlid Neolamprologus pulcher: evidence from microsatellite analyses and behavioural observations. J Fish Biol 65:91–105CrossRefGoogle Scholar
  55. Stobutzki I, Bellwood DR (1997) Sustained swimming abilities of the late pelagic stages of coral reef fishes. Mar Ecol Prog Ser 149:35–41CrossRefGoogle Scholar
  56. Taylor MI, Morley JI, Rico C, Balshine S (2003) Evidence for genetic monogamy and female-biased dispersal in the biparental mouthbrooding cichlid Eretmodus cyanostictus from Lake Tanganyika. Mol Ecol 12:3173–3177PubMedCrossRefGoogle Scholar
  57. van Oppen MJH, Rico C, Deutsch TC, Turner GF, Hewitt GM (1997) Isolation and characterization of microsatellite loci in the cichlid fish Pseudotropheus zebra. Mol Ecol 6:387–388PubMedCrossRefGoogle Scholar
  58. Ward AJW, Hart PJB (2003) The effects of kin and familiarity on interactions between fish. Fish Fish 4:348–358CrossRefGoogle Scholar
  59. West SA, Pen I, Griffin AS (2002) Conflict and cooperation–cooperation and competition between relatives. Science 296:72–75PubMedCrossRefGoogle Scholar
  60. Yoder JM, Marschall EA, Swanson DA (2004) The cost of dispersal: predation as a function of movement and site familiarity in ruffed grouse. Behav Ecol 15:469–476CrossRefGoogle Scholar
  61. 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: Perciformes). Proc R Soc Lond B 263:1589–1598CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Wouter F. D. van Dongen
    • 1
    • 2
    Email author
  • Richard H. Wagner
    • 1
  • Yoshan Moodley
    • 1
  • Franziska C. Schaedelin
    • 1
  1. 1.Konrad Lorenz Institute of Ethology, Department of Integrative Biology and EvolutionUniversity of Veterinary Medicine ViennaViennaAustria
  2. 2.Applied Ecology Research Group and Institute for Sustainability and Innovation, College of Engineering and ScienceVictoria UniversityMelbourneAustralia

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