The Science of Nature

, 105:53 | Cite as

Phenotypic assortment by body shape in wild-caught fish shoals

  • Jennifer L. KelleyEmail author
  • Jonathan P. Evans
Original Paper


Phenotypic variation plays a critical role in determining the structural organisation and ecological function of wild populations. Animal groups are often structured according to factors such as species, sex, body size and parasite load, but it is unclear whether body shape also influences patterns of social organisation, and thus contributes to population phenotypic structure. Here, we use geometric morphometric analyses to determine whether wild-caught shoals of a freshwater fish, the western rainbowfish (Melanotaenia australis), are structured according to body size and shape. Using randomisation analyses, we show that the level of variation in size and shape observed in natural group assemblages is lower than that expected under a null model of random shoal composition. In addition, we found evidence of further phenotypic structuring along an upstream-downstream environmental gradient. The putative benefits of morphological assortment include a reduction in predation risk (due to prey oddity and predator confusion effects) and increased hydrodynamic or foraging efficiency. We suggest that morphological variation is a neglected component of population social organisation that can affect population processes, such as patterns of gene flow, and ecological interactions, such as predator-prey dynamics.


Group structure Group living Oddity effect Confusion effect Social organisation 



We would like to thank Damien Farine for excellent feedback on a previous version of this manuscript and Christos Ioannou, Joel Trexler, and two anonymous reviewers for comments that improved our work. We would also like to thank Monica Gagliano for field assistance, Steven Correia for help with the image analyses and Andrew Storey (Wetland Research and Management) and Nicole Gregory (Rio Tinto) for coordinating field site access. We are grateful to Rio Tinto for facilitating the fieldwork and for providing accommodation in the field.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

All procedures were approved by the University of Western Australia Animal Ethics Committee (approval number RA/3/100/691).

Supplementary material

114_2018_1581_MOESM1_ESM.docx (74 kb)
ESM 1 (DOCX 73 kb)


  1. Allen GR, Midgley SH, Allen M (2002) Field guide to the freshwater fishes of Australia. Western Australian Museum, PerthGoogle Scholar
  2. Arnold KE (2000) Kin recognition in rainbowfish (Melanotaenia eachamensis): sex, sibs and shoaling. Behav Ecol Sociobiol 48:385–391CrossRefGoogle Scholar
  3. Barlow GW (1961) Causes and significance of morphological variation in fishes. Syst Zool 10(3):105–117. CrossRefGoogle Scholar
  4. 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(4):461–468. CrossRefGoogle Scholar
  5. Berwaerts K, Matthysen E, Van Dyck H (2008) Take-off flight performance in the butterfly Pararge aegeria relative to sex and morphology: a quantitative genetic assessment. Evolution 62(10):2525–2533. CrossRefPubMedGoogle Scholar
  6. Bolnick DI, Snowberg LK, Patenia C, Stutz WE, Ingram T, Lau OL (2009) Phenotype-dependent native habitat preference facilitates divergence between parapatric lake and stream stickleback. Evolution 63(8):2004–2016CrossRefGoogle Scholar
  7. Bonduriansky R, Rowe L, Tregenza T (2005) Sexual selection, genetic architecture, and the condition dependence of body shape in the sexually dimorphic fly Prochyliza xanthostoma (Piophilidae). Evolution 59(1):138–151CrossRefGoogle Scholar
  8. Bronmark C, Miner JG (1992) Predator-induced phenotypical change in body morphology in crucian carp. Science 258:1348–1350CrossRefGoogle Scholar
  9. Brown C (2002) Do female rainbowfish (Melanotaenia spp.) prefer to shoal with familiar individuals under predation pressure? Ethology 20:89–94CrossRefGoogle Scholar
  10. Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, ChicagoGoogle Scholar
  11. Croft DP, Arrowsmith BJ, Bielby J, Skinner K, White E, Couzin ID, Magurran AE, Ramnarine I, Krause J (2003) Mechanisms underlying shoal composition in the Trinidadian guppy, Poecilia reticulata. Oikos 100:429–438CrossRefGoogle Scholar
  12. Dayton Gage H, Saenz D, Baum Kristen A, Langerhans RB, DeWitt Thomas J (2005) Body shape, burst speed and escape behavior of larval anurans. Oikos 111(3):582–591. CrossRefGoogle Scholar
  13. Edelaar P, Siepielski AM, Clobert J (2008) Matching habitat choice causes directed gene flow: a neglected dimension in evolution and ecology. Evolution 62(10):2462–2472. CrossRefPubMedGoogle Scholar
  14. Ehlinger TJ, Wilson DS (1988) Complex foraging polymorphism in bluegill sunfish. Proc Natl Acad Sci 85(6):1878–1882CrossRefGoogle Scholar
  15. Farine DR, Montiglio P-O, Spiegel O (2015) From individuals to groups and back: the evolutionary implications of group phenotypic composition. TREE 30(10):609–621. CrossRefPubMedGoogle Scholar
  16. Farine DR, Freckleton R, Rands S (2017) A guide to null models for animal social network analysis. Methods Ecol Evol 8(10):1309–1320. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gerlach G, Schardt U, Eckmann R, Meyer A (2001) Kin-structured subpopulations in Eurasian perch (Perca fluviatilis L.). Heredity 86:213–221. CrossRefPubMedGoogle Scholar
  18. Hoare DJ, Ruxton GD, Godin JGJ, Krause J (2000) The social organization of free-ranging fish shoals. Oikos 89(3):546–554. CrossRefGoogle Scholar
  19. Hoare DJ, Krause J, Peukuri N, Godin JGJ (2005) Body size and shoaling in fish. J Fish Biol 57:1351–1366CrossRefGoogle Scholar
  20. Ioannou CC, Ramnarine IW, Torney CJ (2017) High-predation habitats affect the social dynamics of collective exploration in a shoaling fish. Sci Adv 3:e1602682. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Kanno Y, Vokoun JC, Letcher BH (2011) Fine-scale population structure and riverscape genetics of brook trout (Salvelinus fontinalis) distributed continuously along headwater channel networks. Mol Ecol 20(18):3711–3729. CrossRefPubMedGoogle Scholar
  22. Karpestam E, Wennersten L, Forsman A (2012) Matching habitat choice by experimentally mismatched phenotypes. Evol Ecol 26(4):893–907. CrossRefGoogle Scholar
  23. Kelley JL, Rodgers GM, Morrell LJ (2016) Conflict between background matching and social signalling in a colour-changing freshwater fish. Roy Soc Open Sci 3:160040. CrossRefGoogle Scholar
  24. Kelley JL, Davies PM, Collin SP, Grierson PF (2017) Morphological plasticity in a native freshwater fish from semi-arid Australia in response to variable water flows. Ecol Evol 7:6595–6605. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Killen SS, Marras S, Nadler L, Domenici P (2017) The role of physiological traits in assortment among and within fish shoals. Philos Trans R Soc Lond B Biol Sci 372(1727):20160233. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Klingenberg CP, Barluenga M, Meyer A (2003) Body shape variation in cichlid fishes of the Amphilophus citrinellus species complex. Biol J Linn Soc 80:397–408. CrossRefGoogle Scholar
  27. Klingenberg CP (2016) Size, shape, and form: concepts of allometry in geometric morphometrics. Dev Genes Evol 226:113–137. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Krause J, Butlin RK, Peuhkuri N, Pritchard VL (2000) The social organization of fish shoals: a test of the predictive power of laboratory experiments for the field. Biol Rev 75:477–501CrossRefGoogle Scholar
  29. 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 98:128–136CrossRefGoogle Scholar
  30. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, OxfordGoogle Scholar
  31. Krause J, Ruxton GD, Godin JG-J (2002) Distribution of Crassiphiala bulboglossa, a parastic worm, in shoaling fish. J Anim Ecol 68:27–33. CrossRefGoogle Scholar
  32. Krause J, Ward AJW, Jackson AL, Ruxton GD, James R, Currie S (2005) The influence of differential swimming speeds on composition of multi-species fish shoals. J Fish Biol 67:866–872. CrossRefGoogle Scholar
  33. Landeau L, Terborgh J (1986) Oddity and the ‘confusion effect’ in predation. Anim Behav 34:1372–1380CrossRefGoogle Scholar
  34. Langerhans RB, Reznick DN (2010) Ecology and evolution of swimming performance in fishes: predicting evolution with biomechanics. In: Domencini P, Kapoor BG (eds) Fish locomotion: an eco-ethological perspective. Science Publishers, Enfield, pp 200–248CrossRefGoogle Scholar
  35. Lostrom S, Evans JP, Grierson PF, Collin SP, Davies PM, Kelley JL (2015) Linking stream ecology with morphological variability in a native freshwater fish from semi-arid Australia. Ecol Evol 5:3272–3287. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Malhotra A, Thorpe RS (1997) Size and shape variation in a lesser Antillean anole, Anolis oculatus (Sauria: Iguanidae) in relation to habitat. Biol J Linn Soc 60:53–72. Google Scholar
  37. Marras S, Killen SS, Lindström J, McKenzie DJ, Steffensen JF, Domenici P (2015) Fish swimming in schools save energy regardless of their spatial position. Behav Ecol Sociobiol 69:219–226. CrossRefPubMedGoogle Scholar
  38. Marras S, Porfiri M (2012) Fish and robots swimming together. J Roy Soc Interface 9:1856–1868. CrossRefGoogle Scholar
  39. Mathis A, Chivers DP (2003) Overriding the oddity effect in mixed-species aggregations: group choice by armored and nonarmored prey. Behav Ecol 14(3):334–339. CrossRefGoogle Scholar
  40. McRobert SP, Bradner J (1998) The influence of body coloration on shoaling preferences in fish. Anim Behav 56:611–615CrossRefGoogle Scholar
  41. Milinski M (1987) TIT FOR TAT in sticklebacks and the evolution of co-operation. Nature 325:433–435CrossRefGoogle Scholar
  42. Morrell LJ, Croft DP, Dyer JRG, Chapman BB, Kelley JL, Laland KN, Krause J (2008) Association patterns and foraging behaviour in natural and artificial guppy shoals. Anim Behav 76:855–864. CrossRefGoogle Scholar
  43. Ohguchi O (1978) Experiments on the selection against colour oddity of water fleas by three-spined sticklebacks. Ethology 47:254–267Google Scholar
  44. Olsson J, Svanback R, Eklov P (2007) Effects of resource level and habitat type on behavioral and morphological plasticity in Eurasian perch. Oecologia 152(1):48–56. CrossRefPubMedGoogle Scholar
  45. Pakkasmaa S, Piironen J (2000) Water velocity shapes juvenile salmonids. Evol Ecol 14(8):721–730. CrossRefGoogle Scholar
  46. Persson L, Andersson J, Wahlstrom E, Eklov P (1996) Size-specific interactions in lake systems: predator gape limitation and prey growth rate and mortality. Ecology 77:900–911CrossRefGoogle Scholar
  47. Petrie M (1988) Intraspecific variation in structures that display competitive ability: large animals invest relatively more. Anim Behav 36(4):1174–1179. CrossRefGoogle Scholar
  48. Piyapong C, Butlin RK, Faria JJ, Scruton KJ, Wang J, Krause J (2011) Kin assortment in juvenile shoals in wild guppy populations. Heredity 106(5):749–756. CrossRefPubMedGoogle Scholar
  49. Pusey BJ, Kennard MJ, Arthington AH (2004) Freshwater fishes of north-eastern Australia. CSIRO Publishing, CollingwoodGoogle Scholar
  50. R Development Core Team (2016) A language and environment for statistical computing R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  51. Relyea RA (2004) Fine-tuned phenotypes: tadpole plasticity under 16 combinations of predators and competitors. Ecology 85(1):172–179. CrossRefGoogle Scholar
  52. Ranta E, Lindstrom K, Peuhkuri N (1992) Size matters when three-spined sticklebacks go to school. Anim Behav 43:160–162CrossRefGoogle Scholar
  53. Robinson BW, Parsons KJ (2002) Changing times, spaces, and faces: tests and implications of adaptive morphological plasticity in the fishes of northern postglacial lakes. Can J Fish Aquat Sci 59(11):1819–1833CrossRefGoogle Scholar
  54. Rodgers GM, Downing B, Morrell LJ (2015) Prey body size mediates the predation risk associated with being “odd”. Behav Ecol 26(1):242–246. CrossRefGoogle Scholar
  55. Rodgers GM, Kelley JL, Morrell LJ (2010) Colour change and assortment in the western rainbowfish. Anim Behav 79:1025–1030CrossRefGoogle Scholar
  56. Rohlf FJ (2004) tpsUtil, version 1.33 Department of Ecology and Evolution, State University of New YorkGoogle Scholar
  57. Rohlf FJ (2005a) TPSDIG2, digitize landmarks and outlines Department of Ecology and Evolution, State University, New YorkGoogle Scholar
  58. Rohlf FJ (2005b) tpsRelw, relative warp anlaysis, version 1.45. Stony Brook University, New YorkGoogle Scholar
  59. Russell ST, Kelley JL, Graves JA, Magurran AE (2004) Kin structure and shoal composition dynamics in the guppy, Poecilia reticulata. Oikos 106:520–526CrossRefGoogle Scholar
  60. Seebacher F, Webster MM, James RS, Tallis J, Ward AJ (2016) Morphological differences between habitats are associated with physiological and behavioural trade-offs in stickleback (Gasterosteus aculeatus). Roy Soc Open Sci 3:160316CrossRefGoogle Scholar
  61. Skulason S, Smith TB (1995) Resource polymorphisms in vertebrates. Trends Ecol Evol 10(9):366–370. CrossRefPubMedGoogle Scholar
  62. Theodorakis CW (1989) Size segregation and the effects of oddity on predation risk in minnow schools. Anim Behav 38:496–502CrossRefGoogle Scholar
  63. Walker JA (1997) Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L. (Gasterosteidae) body shape. Biol J Linn Soc 61:3–50. Google Scholar
  64. Ward AJ, Axford S, Krause J (2002) Mixed-species shoaling in fish: the sensory mechanisms and costs of shoal choice. Behav Ecol Sociobiol 52(3):182–187CrossRefGoogle Scholar
  65. Ward AJW, Hart PJB (2003) The effects of kin and familiarity on interactions between fish. Fish Fish 4:348–358CrossRefGoogle Scholar
  66. Young MJ, Simmons LW, Evans JP (2011) Predation is associated with variation in colour pattern, but not body shape or colour reflectance, in a rainbowfish (Melanotaenia australis). J Anim Ecol 80(1):183–191. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Centre for Evolutonary Biology, School of Biological Sciences (M092)The University of Western AustraliaPerthAustralia

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