Skip to main content
Springer Nature Link
Log in

Shoaling decisions in three-spined sticklebacks (Gasterosteus aculeatus)—familiarity, kinship and inbreeding

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Shoaling with familiar kin is a well-known phenomenon. It has been described both for adult and for fry of three-spined sticklebacks (Gasterosteus aculeatus). However, evidence of preference for kin independent of familiarity is scarce. Furthermore, inbreeding effects have not been studied for shoaling preferences and there is a lack of studies about changes in individuals’ ability to recognise kin during different phases of life history. We gave inbred and outbred, nonreproductive sticklebacks of different age the choice to shoal with a group of familiar siblings vs unfamiliar non-siblings and with unfamiliar siblings vs unfamiliar non-siblings. Subadult sticklebacks preferred to shoal with familiar kin over unfamiliar non-kin, but inbred and outbred individuals had similar preferences. When given the choice between unfamiliar siblings and unfamiliar non-sibs, adult outbred fish preferred the shoal of kin, while inbred fish behaved indifferently. Body characteristics of the group such as body mass, standard length and condition of its members did not significantly explain the shoaling preferences for kin. Thus, sticklebacks were capable of recognising familiar and unfamiliar kin. The latter capability was lost by inbreeding.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

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

    Article  Google Scholar 

  • Behrmann-Godel J, Gerlach G, Eckmann R (2006) Kin and population recognition in sympatric Lake Constance perch (Perca fluviatilis L.): can assortative shoaling drive population divergence? Behav Ecol Sociobiol 59:461–468

    Article  Google Scholar 

  • Blaustein AR (1983) Kin recognition mechanisms—phenotype matching or recognition alleles? Am Nat 121:749–754

    Article  Google Scholar 

  • Bolger T, Connolly PL (1989) The selection of suitable indices for the measurement and analysis of fish condition. J Fish Biol 34:171–182

    Article  Google Scholar 

  • Brown C, Warburton K (1997) Predator recognition and anti-predator responses in the rainbowfish Melanotaenia eachamensis. Behav Ecol Sociobiol 41:61–68

    Article  Google Scholar 

  • Brown GE, Brown JA (1993) Social dynamics in salmonid fishes—do kin make better neighbors? Anim Behav 45:863–871

    Article  Google Scholar 

  • Farr JA (1983) The inheritance of quantitative fitness traits in guppies, Poecilia reticulata (Pisces, Poeciliidae). Evolution 37:1193–1209

    Article  Google Scholar 

  • Farr JA, Peters K (1984) The inheritance of quantitative fitness traits in guppies, Poecilia reticulata (Pisces, Poeciliidae). 2. Tests for inbreeding effects. Heredity 52:285–296

    Google Scholar 

  • Fisher HS, Wong BBM, Rosenthal GG (2006) Alteration of the chemical environment disrupts communication in a freshwater fish. Proc R Soc Lond B 273:1187–1193

    Article  CAS  Google Scholar 

  • FitzGerald GJ, Morrissette J (1992) Kin recognition and choice of shoal mates by threespine sticklebacks. Ethol Ecol Evol 4:273–283

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Frommen JG, Bakker TCM (2006) Inbreeding avoidance through non-random mating in sticklebacks. Biol Lett 2:232–235

    Article  PubMed  Google Scholar 

  • Gallardo JA, Neira R (2005) Environmental dependence of inbreeding depression in cultured Coho salmon (Oncorhynchus kisutch): aggressiveness, dominance and intraspecific competition. Heredity 95:449–456

    Article  PubMed  CAS  Google Scholar 

  • Gómez-Laplaza LM (2005) The influence of social status on shoaling preferences in the freshwater angelfish (Pterophyllum scalare). Behaviour 142:827–844

    Article  Google Scholar 

  • Grafen A (1990) Do animals really recognise kin? Anim Behav 39:42–54

    Article  Google Scholar 

  • Griffiths SW, Brockmark S, Höjesjö J, Johnsson JI (2004) Coping with divided attention: the advantage of familiarity. Proc R Soc Lond B 271:695–699

    Article  CAS  Google Scholar 

  • Griffiths SW, Magurran AE (1997) Schooling preferences for familiar fish vary with group size in a wild guppy population. Proc R Soc Lond B 264:547–551

    Article  Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behaviour 1. J Theor Biol 7:1–16

    Article  PubMed  CAS  Google Scholar 

  • Johannes MRS (1993) Prey aggregation is correlated with increased predation pressure in lake fish communities. Can J Fish Aquat Sci 50:66–73

    Google Scholar 

  • Keenleyside MHA (1955) Some aspects of the schooling behaviour of fish. Behaviour 8:183–248

    Google Scholar 

  • Krause J (1993) The influence of hunger on shoal size choice by three-spined sticklebacks, Gasterosteus aculeatus. J Fish Biol 43:775–780

    Article  Google Scholar 

  • Krause J (1994) The influence of food competition and predation risk on size-assortative shoaling in juvenile chub (Leuciscus cephalus). Ethology 96:105–116

    Google Scholar 

  • Krause J, Godin J-GJ (1994) Shoal choice in the banded killifish (Fundulus diaphanus, Teleostei, Cyprinodontidae)—effects of predation risk, fish size, species composition and size of shoals. Ethology 98:128–136

    Article  Google Scholar 

  • Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford

    Google Scholar 

  • MacPherson E (1998) Ontogenetic shifts in habitat use and aggregation in juvenile sparid fishes. J Exp Mar Biol Ecol 220:127–150

    Article  Google Scholar 

  • Magurran AE (1990) The adaptive significance of schooling as an anti-predator defence in fish. Ann Zool Fenn 27:51–66

    Google Scholar 

  • Mateo JM (2004) Recognition systems and biological organization: the perception component of social recognition. Ann Zool Fenn 41:729–745

    Google Scholar 

  • Mateo JM, Johnston RE (2000) Kin recognition and the ‘armpit effect’: evidence of self-referent phenotype matching. Proc R Soc Lond B 267:695–700

    Article  CAS  Google Scholar 

  • Mazzi D, Künzler R, Largiadèr CR, Bakker TCM (2004) Inbreeding affects female preference for symmetry in computer-animated sticklebacks. Behav Genet 34:417–424

    Article  PubMed  Google Scholar 

  • McRobert SP, Bradner J (1998) The influence of body coloration on shoaling preferences in fish. Anim Behav 56:611–615

    Article  PubMed  Google Scholar 

  • Metcalfe NB, Thomson BC (1995) Fish recognize and prefer to shoal with poor competitors. Proc R Soc Lond B 259:207–210

    Article  Google Scholar 

  • Milinski M, Külling D, Kettler R (1990) Tit for tat: sticklebacks (Gasterosteus aculeatus) “trusting” a cooperating partner. Behav Ecol 1:7–11

    Article  Google Scholar 

  • Modarressie R, Rick IP, Bakker TCM (2006) UV matters in shoaling decisions. Proc R Soc Lond B 273:849–854

    Article  Google Scholar 

  • Peuhkuri N, Seppä P (1998) Do three-spined sticklebacks group with kin? Ann Zool Fenn 35:21–27

    Google Scholar 

  • Pitcher TJ, Magurran AE, Winfield IJ (1982) Fish in larger shoals find food faster. Behav Ecol Sociobiol 10:149–151

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Poulin R (1999) Parasitism and shoal size in juvenile sticklebacks: conflicting selection pressures from different ectoparasites? Ethology 105:959–968

    Article  Google Scholar 

  • Ranta E, Lindström K, Peuhkuri N (1992) Size matters when three-spined sticklebacks go to school. Anim Behav 43:160–162

    Article  Google Scholar 

  • Reusch TBH, Häberli MA, Aeschlimann PB, Milinski M (2001) Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414:300–302

    Article  PubMed  CAS  Google Scholar 

  • Steck N, Wedekind C, Milinski M (1999) No sibling odor preference in juvenile three-spined sticklebacks. Behav Ecol 10:493–497

    Article  Google Scholar 

  • Tiira K, Laurila A, Peuhkuri N, Piironen J, Ranta E, Primmer CR (2003) Aggressiveness is associated with genetic diversity in landlocked salmon (Salmo salar). Mol Ecol 12:2399–2407

    Article  PubMed  Google Scholar 

  • Utne-Palm AC, Hart PJB (2000) The effects of familiarity on competitive interactions between threespined sticklebacks. Oikos 91:225–232

    Article  Google Scholar 

  • Waldman B, McKinnon JS (1993) Inbreeding and outbreeding in fishes, amphibians and reptiles. In: Thornhill NW (ed) The natural history of inbreeding and outbreeding: theoretical and empirical perspectives. University of Chicago Press, Chicago, pp 250–282

    Google Scholar 

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

    Google Scholar 

  • Ward AJW, Duff AJ, Krause J, Barber I (2005a) Shoaling behaviour of sticklebacks infected with the microsporidian parasite, Glugea anomala. Environ Biol Fishes 72:155–160

    Article  Google Scholar 

  • Ward AJW, Holbrook RI, Krause J, Hart PJB (2005b) Social recognition in sticklebacks: the role of direct experience and habitat cues. Behav Ecol Sociobiol 57:575–583

    Article  Google Scholar 

  • Wedekind C (1996) Lek-like spawning behaviour and different female mate preferences in roach (Rutilus rutilus). Behaviour 133:681–695

    Google Scholar 

  • Wootton RJ (1976) The biology of the sticklebacks. Academic, London

    Google Scholar 

  • Wootton RJ (1984) A functional biology of sticklebacks. Croom Helm, London

    Google Scholar 

Download references

Acknowledgements

We are grateful to Ricarda Modarressie, Julia Schwarzer, Ingolf Rick and Timo Thünken for discussions and Leif Engqvist for improving our English and statistical advice. We thank Marc Zbinden for rearing, Julia Strelau for caring and Jan Hottentot for catching the sticklebacks. The manuscript greatly benefited from the comments of two anonymous referees. All experiments complied with the current laws of Germany.

Author information

Authors and Affiliations

  1. Institute for Evolutionary Biology and Ecology, University of Bonn, An der Immenburg 1, D-53121, Bonn, Germany

    Joachim G. Frommen, Marion Mehlis, Christina Brendler & Theo C. M. Bakker

Authors
  1. Joachim G. Frommen
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Marion Mehlis
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Christina Brendler
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Theo C. M. Bakker
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Joachim G. Frommen.

Additional information

Communicated by J. Krause

Rights and permissions

Reprints and permissions

About this article

Cite this article

Frommen, J.G., Mehlis, M., Brendler, C. et al. Shoaling decisions in three-spined sticklebacks (Gasterosteus aculeatus)—familiarity, kinship and inbreeding. Behav Ecol Sociobiol 61, 533–539 (2007). https://doi.org/10.1007/s00265-006-0281-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-006-0281-2

Keywords