Sex biases in kin shoaling and dispersal in a cichlid fish

Abstract

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Arnold KE (2000) Kin recognition in rainbowfish (Melanotaenia eachamensis): sex, sibs and shoaling. Behav Ecol Sociobiol 48:385–391

    Article  Google Scholar 

  2. Aubin-Horth N, Desjardins JK, Martei YM, Balshine S, Hofmann HA (2007) Masculinized dominant females in a cooperatively breeding species. Mol Ecol 16:1349–1358

    PubMed  Article  Google 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 83:515–524

    Article  Google 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 2:611–614

    Article  Google Scholar 

  5. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05. Université de Montpellier II

  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 21:4917–4920

    Article  Google 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 87:290–312

    PubMed  Article  Google 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 80:205–225

    Article  Google 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 33:140–144

    CAS  PubMed  Article  Google Scholar 

  10. Consuegra S, García de Leániz C (2007) Fluctuating sex ratios, but not sex-biased dispersal, in a promiscuous fish. Evol Ecol 21:229–245

    Article  Google Scholar 

  11. Duchesne P, Étienne C, Bernatchez L (2006) PERM: a computer program to detect structuring factors in meaningful social units. Mol Ecol Notes 6:965–976

    Article  Google 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 14:2611–2620

    CAS  PubMed  Article  Google 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 10:564–567

    Article  Google Scholar 

  14. Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

  15. Fisher R, Bellwood DR, Job SD (2000) Development of swimming abilities in reef fish larvae. Mar Ecol Prog Ser 202:163–173

    Article  Google Scholar 

  16. Frommen JG, Bakker TCM (2004) Adult three-spined sticklebacks prefer to shoal with familiar kin. Behaviour 141:1401–1409

    Article  Google Scholar 

  17. Frommen JG, Luz C, Bakker TCM (2007) Nutritional state influences shoaling preference for familiars. Zoology 110:369–376

    PubMed  Article  Google Scholar 

  18. Gerlach G, Lysiak N (2006) Kin recognition and inbreeding avoidance in zebrafish, Danio rerio, is based on phenotype matching. Anim Behav 71:1371–1377

    Article  Google 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 61:1765–1770

    Article  Google Scholar 

  20. Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-Statistics. J Hered 86:485–486

    Google Scholar 

  21. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162

    Article  Google Scholar 

  22. Griffiths SW, Magurran AE (1998) Sex and schooling behaviour in the Trinidadian guppy. Anim Behav 56:689–693

    PubMed  Article  Google 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 5:294–301

    Article  Google Scholar 

  24. Handley LJL, Perrin N (2007) Advances in our understanding of mammalian sex-biased dispersal. Mol Ecol 16:1559–1578

    Article  Google Scholar 

  25. Hatchwell BJ (2010) Cryptic kin selection: kin structure in vertebrate populations and opportunities for kin-directed cooperation. Ethology 116:203–216

    Article  Google Scholar 

  26. Helfman GB, Collette BB, Facey DE (1997) The diversity of fishes. Blackwell, Malden

    Google 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 104:2785–2790

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  28. Hiddink JG, Kock RP, Wolff WJ (2002) Active pelagic migrations of the bivalve Macoma balthica are dangerous. Mar Biol 140:1149–1156

    Article  Google Scholar 

  29. Jadwiszczack P (2002) Rundom projects: An application for randomization and bootstrap testing. http://pjadw.tripod.com/soft.htm

  30. Kalinowski S, Taper M, Marshall T (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    PubMed  Article  Google 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 128:121–131

    Google Scholar 

  32. Konings A (1998) Tanganyika cichlids in their natural habitat. Cichlid Press, El Paso

    Google Scholar 

  33. Koops MA, Grant JWA (1993) Weight asymmetry and sequential assessment in convict cichlid contests. Can J Zool 71:475–479

    Article  Google Scholar 

  34. Lee WJ, Kocher TD (1996) Microsatellite DNA markers for genetic mapping in Oreochromis niloticus. J Fish Biol 49:169–171

    CAS  Google Scholar 

  35. Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766

    CAS  PubMed Central  PubMed  Google 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 38:47–66

    Google 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 22:1733–1745

    PubMed  Article  Google 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 6:971–973

    Article  Google Scholar 

  39. Ochi H, Yanagisawa Y (1999) Sand-transfer behavior outside the nest by guarding parents of the Tanganyikan cichlid, Neolamprologus caudopunctatus. Ichthyol Res 46:419–422

    Article  Google Scholar 

  40. Parker A, Kornfield I (1996) Polygynandry in Pseudotropheus zebra, a cichlid fish from Lake Malawi. Environ Biol Fish 47:345–352

    Article  Google 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 363–439

    Chapter  Google 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 106:749–756

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  43. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  Google Scholar 

  45. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed Central  PubMed  Google 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 37:282–289

    Article  Google Scholar 

  47. Ruhl N, McRobert SP (2005) The effect of sex and shoal size on shoaling behaviour in Danio rerio. J Fish Biol 67:1318–1326

    Article  Google Scholar 

  48. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  49. Schaedelin FC, van Dongen WFD, Wagner RH (2013) Non-random brood mixing suggests adoption in a colonial cichlid. Behav Ecol 24:540–546

    Article  Google 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 208:229–248

    Article  Google 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 10:1471–1488

    CAS  PubMed  Article  Google 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 48:236–242

    Article  Google 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 19:5497–5510

    PubMed  Article  Google 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 65:91–105

    Article  Google Scholar 

  55. Stobutzki I, Bellwood DR (1997) Sustained swimming abilities of the late pelagic stages of coral reef fishes. Mar Ecol Prog Ser 149:35–41

    Article  Google 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 12:3173–3177

    PubMed  Article  Google 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 6:387–388

    PubMed  Article  Google Scholar 

  58. Ward AJW, Hart PJB (2003) The effects of kin and familiarity on interactions between fish. Fish Fish 4:348–358

    Article  Google Scholar 

  59. West SA, Pen I, Griffin AS (2002) Conflict and cooperation–cooperation and competition between relatives. Science 296:72–75

    CAS  PubMed  Article  Google 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 15:469–476

    Article  Google 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 263:1589–1598

    CAS  Article  Google Scholar 

Download references

Acknowledgments

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).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Wouter F. D. van Dongen.

Additional information

Communicated by Aaron J. Wirsing.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

van Dongen, W.F.D., Wagner, R.H., Moodley, Y. et al. Sex biases in kin shoaling and dispersal in a cichlid fish. Oecologia 176, 965–974 (2014). https://doi.org/10.1007/s00442-014-3079-3

Download citation

Keywords

  • Animal movements
  • Fish shoals
  • Grouping behavior
  • Kin selection
  • Population genetics