Advertisement

Behavioral Ecology and Sociobiology

, Volume 59, Issue 4, pp 461–468 | Cite as

Kin and population recognition in sympatric Lake Constance perch (Perca fluviatilis L.): can assortative shoaling drive population divergence?

  • Jasminca Behrmann-Godel
  • Gabriele Gerlach
  • Reiner Eckmann
Original Article

Abstract

Prior studies have shown that perch (Perca fluviatilis L.) of Lake Constance belong to two genetically different but sympatric populations and that local aggregations of juveniles and adults contain closely related kin. In this study, we analysed the genetic structure of pelagic perch larvae to investigate if kin-structured shoals already exist during early ontogenetic development or might be the result of homing to natal sites. Analysis of the gene frequencies at five microsatellite loci revealed that three out of five pelagic aggregations of larvae showed significant accumulation of kin. To investigate possible mechanisms of shoal formation, we tested if perch use olfactory cues to recognize their kin. Choice tests in a fluviarium showed preference for odours of unfamiliar kin vs unfamiliar non-kin. Additionally, we showed that perch could differentiate between the odours of the two sympatric populations and significantly preferred unfamiliar and unrelated conspecifics of their own over the foreign population. Our results present a behavioural mechanism that can lead to the observed formation of kin-structured shoals in perch. We further discuss if the ability to discriminate between their own and a foreign population can result in assortative mating within populations and thus form the basis of “socially mediated speciation” in perch.

Keywords

Kin recognition Population recognition Kin structure Microsatellites Relatedness 

Notes

Acknowledgements

We thank Louis Bernatchez, Vincent Castric and Jelle Atema for discussion and comments and Khalid Belkhir for providing a special version of IDENTIX to calculate relatedness in subsamples. We further thank two anonymous referees whose comments greatly improved the manuscript. Funding was provided by Deutsche Forschungsgemeinschaft within the collaborative research centre SFB 454, Littoral of Lake Constance, the “Fonds der Chemischen Industrie”, the University of Konstanz, and the “Konrad Adenauer-Stiftung”. We declare that the experiments we have presented here comply with the current laws of Germany.

References

  1. Aalto SK, Newsome GE (1989) Evidence of demic structure for a population of yellow perch (Perca flavescens). Can J Fish Aquat Sci 46:184–190Google Scholar
  2. Apanius V, Penn D, Slev PR, Ruff LR, Potts WK (1997) The nature of selection on the major histocompatibility complex. Crit Rev Immunol 17:179–224PubMedGoogle Scholar
  3. Arnold KE (2000) Kin recognition in rainbowfish (Melanotaenia eachamensis): sex, sibs and shoaling. Behav Ecol Sociobiol 48:385–391CrossRefGoogle Scholar
  4. Atema J, Kingsford M, Gerlach G (2002) Larval reef fish could use odour for detection, retention and orientation to reefs. Mar Ecol Prog Ser 241:151–160CrossRefGoogle Scholar
  5. Avise JC, Shapiro DY (1986) Evaluating kinship of newly settled juveniles within social groups of the coral reef fish Anthias squamipinnis. Evolution 40:1051–1059CrossRefGoogle Scholar
  6. Barber I, Ruxton GD (2000) The importance of stable schooling: do familiar sticklebacks stick together? Proc R Soc Lond B Biol Sci 267:151–155CrossRefGoogle Scholar
  7. Barnett C (1986) Rearing conditions affect chemosensory preferences in young cichlid fish. Ethology 72:227–235CrossRefGoogle Scholar
  8. Belkhir K, Borsa P, Goudet J, Chikhi L, Bonhomme F (1997) Genetix v. 3.0, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UPR 9060, Université Montpellier 2, MontpellierGoogle Scholar
  9. 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
  10. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 16:363–377PubMedCrossRefGoogle Scholar
  11. Borer SO, Miller LM, Kapuscinski AR (1999) Microsatellites in walleye Stizostedion vitreum. Mol Ecol 8:336–338PubMedGoogle Scholar
  12. Brown GE, Brown JA (1992) Do rainbow trout and Atlantic salmon discriminate kin? Can J Zool 70:1636–1640Google Scholar
  13. Brown GE, Brown JA (1993) Do kin always make better neighbours? The effects of territory quality. Behav Ecol Sociobiol 33:225–231CrossRefGoogle Scholar
  14. Brown GE, Brown JA (1996) Does kin-biased territorial behavior increase kin-biased foraging in juvenile salmonids. Behav Ecol 7:24–29CrossRefGoogle Scholar
  15. Brown GE, Brown JA, Crosbie AM (1993) Phenotype matching in juvenile rainbow trout. Anim Behav 46:1223–1225CrossRefGoogle Scholar
  16. Castric V, Bernatchez L, Belkhir K, Bonhomme F (2002) Heterozygote deficiencies in small lacustrine populations of brook charr Salvelinus fontinalis Mitchill (Pisces, Salmonidae): a test of alternative hypotheses. Heredity 89:27–35PubMedCrossRefGoogle Scholar
  17. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Ann Rev Ecolog Syst 18:287–368CrossRefGoogle Scholar
  18. Courtenay SC, Quinn TP, Dupuis HMC, Groot C, Larkin PA (1997) Factors affecting the recognition of population-specific odours by juvenile coho salmon. J Fish Biol 50:1042–1060Google Scholar
  19. Dowling TE, Moore WS (1986) Absence of population subdivision in the common shiner N. cornutus (Cyprinidae). Environ Biol Fishes 15:151–155CrossRefGoogle Scholar
  20. Dugatkin LA, Wilson DS (1992) The prerequisites for strategic behaviour in bluegill sunfish Lepomis macrochirus. Anim Behav 44:223–230CrossRefGoogle Scholar
  21. Ferguson MM, Noakes DLG (1981) Social grouping and genetic variation in common shiners, Notropis cornutus (Pisces, Cyprinidae). Environ Biol Fishes 6:357–360CrossRefGoogle Scholar
  22. Fontaine PM, Dodson JJ (1999) An analysis of the distribution of juvenile Atlantic salmon (Salmo salar) in nature as a function of relatedness using microsatellites. Mol Ecol 8:189–198CrossRefGoogle Scholar
  23. Frommen J, Bakker TCM (2004) Adult threespine sticklebacks prefer to shoal with familiar kin. Behaviour 141:1401–1409CrossRefGoogle Scholar
  24. Gerlach G, Schardt U, Eckmann R, Meyer A (2001) Kin-structured subpopulations in Eurasian perch (Perca fluviatilis L.). Heredity 86:213–221PubMedCrossRefGoogle Scholar
  25. Griffiths SW, Armstrong JD (2001) The benefits of genetic diversity outweigh those of kin association in a territorial animal. Proc R Soc Lond B Biol Sci 268:1293–1296CrossRefGoogle Scholar
  26. Griffiths SW, Magurran AE (1999) Schooling decisions in guppies (Poecilia reticulata) are based on familiarity rather than kin recognition by phenotype matching. Behav Ecol Sociobiol 45:437–443CrossRefGoogle Scholar
  27. Hamilton WD (1964) The genetical evolution of social behaviour. J Theor Biol 7:1–16PubMedCrossRefGoogle Scholar
  28. Hasler AD, Scholz AT (1983) Olfactory imprinting and homing in salmon. Springer, Berlin Heidelberg New YorkGoogle Scholar
  29. Hauser L, Carvalho GR, Pitcher TJ (1998) Genetic population structure in the Lake Tanganyika sardine Limnothrissa miodon. J Fish Biol 53(Suppl A):413–429Google Scholar
  30. Helfman GS (1984) School fidelity in fishes: the yellow perch pattern. Anim Behav 32:663–672CrossRefGoogle Scholar
  31. Höglund LB (1961) The reaction of fish in concentration gradients. Rep Inst Freshw Res Drottningholm 43:1–147Google Scholar
  32. Höjesjö J, Johnsson JI, Petersson E, Järvi T (1998) The importance of being familiar: individual recognition and social behavior in sea trout (Salmo trutta). Behav Ecol 9:445–451CrossRefGoogle Scholar
  33. Irwin DE, Bensch S, Price TD (2001) Speciation in a ring. Nature 409:333–337PubMedCrossRefGoogle Scholar
  34. Krause J, Butlin RK, Peuhkuri N, Pritchard VL (2000a) The social organization of fish shoals: a test of the predictive power of laboratory experiments for the field. Biol Rev Camb Philos Soc 75:477–501PubMedGoogle Scholar
  35. Krause J, Hoare DJ, Croft D, Lawrence J, Ward A, Ruxton GD, Godin JG, James R (2000b) Fish shoal composition: mechanisms and constraints. Proc R Soc Lond B Biol Sci 267:2011–2017CrossRefGoogle Scholar
  36. Leclerc D, Wirth T, Bernatchez L (2000) Isolation and characterization of microsatellite loci in the yellow perch (Perca flavescens), and cross-species amplification within the family Percidae. Mol Ecol 9:993–1011CrossRefGoogle Scholar
  37. Lynch M (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45:622–629CrossRefGoogle Scholar
  38. Mann KD, Turnell ER, Atema J, Gerlach G (2003) Kin recognition in juvenile zebrafish (Danio rerio) based on olfactory cues. Biol Bull 205:224–225PubMedCrossRefGoogle Scholar
  39. Mathieu E, Roux AM, Bonhomme F (1990) Épreuves de validation dans l'analyse de structures génétiques multivariées: comment tester l'équilibre panmitique? Rev Stat Appl 38:47–66Google Scholar
  40. Mayr E (1963) Animal species and evolution. Harvard University Press, CambridgeGoogle Scholar
  41. Milinski M (1987) Tit-for tat in sticklebacks and the evolution of cooperation. Nature 325:433–437PubMedCrossRefGoogle Scholar
  42. Naish KA, Carvalho GR, Pitcher TJ (1993) The genetic structure and microdistribution of shoals of Phoxinus phoxinus, the European minnow. J Fish Biol 43(Suppl A):75–89Google Scholar
  43. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  44. Olsén KH (1986) Chemoattraction between juveniles of two sympatric stocks of Arctic charr (Salvelinus alpinus (L.)) and their gene frequency of serum esterases. J Fish Biol 28:221–231CrossRefGoogle Scholar
  45. Olsén KH (1989) Sibling recognition in juvenile Arctic charr, Salvelinus alpinus (L.). J Fish Biol 34:571–581CrossRefGoogle Scholar
  46. Olsén KH (1992) Kin recognition in fish mediated by chemical cues. In: Hara TJ (ed) Fish chemoreception. Chapman & Hall, London, pp 229–248Google Scholar
  47. Olsén KH, Grahn M, Lohm J, Langefors A (1998) MHC and kin discrimination in juvenile Arctic charr, Salvelinus alpinus (L.). Anim Behav 56:319–327PubMedCrossRefGoogle Scholar
  48. Olsén KH, Grahn M, Lohm J (2002) Influence of MHC on sibling discrimination in Arctic charr, Salvelinus alpinus (L.). J Chem Ecol 28:21–40Google Scholar
  49. Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility complex genes. Am Nat 153:145–164CrossRefGoogle Scholar
  50. Peuhkuri N, Seppae P (1998) Do three-spined sticklebacks group with kin? Ann Zool Fenn 35:21–27Google Scholar
  51. Pouyaud L, Desmarais E, Chenuil A, Agnese JF, Bonhomme F (1999) Kin cohesiveness and possible inbreeding in the mouthbrooding tilapia Sarotherodon melanotheron (Pisces Cichlidae). Mol Ecol 8:803–812CrossRefGoogle Scholar
  52. Quinn TP, Busack CA (1985) Chemosensory recognition of siblings in juvenile coho salmon (Oncorhynchus kisutch). Anim Behav 33:51–56CrossRefGoogle Scholar
  53. Quinn TP, Hara TJ (1986) Sibling recognition and olfactory sensitivity in juvenile coho salmon. Can J Zool 64:921–925CrossRefGoogle Scholar
  54. Reusch TBH, Häberli MA, Aeschlimann PB, Milinski M (2001) Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414:300–302PubMedCrossRefGoogle Scholar
  55. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  56. Shaw KL, Herlihy DP (2000) Acoustic preference functions and song variability in the Hawaiian cricket Laupala cerasina. Proc R Soc Lond B Biol Sci 267:577–584CrossRefGoogle Scholar
  57. Sherman PW, Reeve HK, Pfennig DW (1997) Recognition systems. In: Krebs JR, Davies NB (eds) Behavioral ecology: an evolutionary approach. Blackwell, Oxford, pp 69–96Google Scholar
  58. Shields WM (1982) Philopatry, inbreeding and the evolution of sex. State University of New York Press, AlbanyGoogle Scholar
  59. Stabell OB (1982) Detection of natural odorants by Atlantic salmon parr using positive rheotaxis olfactometry. In: Brannon EL, Salo EO (eds) Proceedings of the salmon and trout migratory behavior symposium. University of Washington Press, Seattle, pp 71–78Google Scholar
  60. Stabell OB (1987) Intraspecific pheromone discrimination and substrate marking by Atlantic salmon parr. J Chem Ecol 13:1625–1643CrossRefGoogle Scholar
  61. Steck N, Wedekind C, Milinski M (1999) No sibling odour preference in juvenile threespined sticklebacks. Behav Ecol 10:493–497CrossRefGoogle Scholar
  62. Tang-Martinez Z (2001) The mechanisms of kin discrimination and the evolution of kin recognition in vertebrates: a critical re-evaluation. Behav Processes 53:21–40PubMedCrossRefGoogle Scholar
  63. Van Havre N, Fitzgerald GJ (1988) Shoaling and kin recognition in the threespine stickleback (Gasterosteus aculeatus L.). Biol Behav 13:190–201Google Scholar
  64. Wang N, Appenzeller A (1998) Abundance, depth distribution, diet composition and growth of perch (Perca fluviatilis) and burbot (Lota lota) larvae and juveniles in the pelagic zone of Lake Constance. Ecol Freshw Fish 7:176–183CrossRefGoogle Scholar
  65. Wang N, Eckmann R (1994) Distribution of perch (Perca fluviatilis L.) during their first year of life in Lake Constance. Hydrobiologia 277:135–143Google Scholar
  66. Warburton K, Lees N (1996) Species discrimination in guppies: learned responses to visual cues. Anim Behav 52:371–378CrossRefGoogle Scholar
  67. Ward AJ, Krause J (2004) The effects of habitat- and diet-based cues on association preferences in three-spined sticklebacks. Behav Ecol 15:925–929CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Jasminca Behrmann-Godel
    • 1
  • Gabriele Gerlach
    • 2
  • Reiner Eckmann
    • 1
  1. 1.Limnological InstituteUniversity of KonstanzKonstanzGermany
  2. 2.Marine Biological LaboratoryWoods HoleUSA

Personalised recommendations