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Sympatric species of threespine stickleback differ in their performance in a spatial learning task

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Abstract

Increasing evidence suggests that cognitive function is under selection in diverse taxa and that this results in different cognitive abilities in taxa experiencing different selective environments. For example, species inhabiting spatially complex environments might be expected to have good spatial learning ability. We investigated whether local habitat conditions influence learning by comparing the performance of two recently diverged species of threespine stickleback (Gasterosteus aculeatus complex) in a spatial learning task. The two species reside sympatrically in several lakes. Benthics occupy the spatially structured vegetated littoral zone, whereas limnetics occupy the spatially homogenous open-water pelagic zone. We trained fish to locate a hidden reward in a T-maze and asked whether they did so by learning a body-centred pattern of movement (turn left or right) or by using plant landmarks. Both benthics and limnetics used turn and landmark cues, but benthics learnt the task almost twice as quickly as limnetics. This difference is consistent with the hypothesis that benthic and limnetic sticklebacks are equipped with spatial learning abilities well suited to the spatial complexity of their littoral and pelagic habitats. Our findings add to the understanding of the evolution of learning.

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References

  • Able KP (1993) Orientation cues used by migratory birds: a review of cue-conflict experiments. Trends Ecol Evol 8:367–371

    Article  Google Scholar 

  • Ancel LW (1999) A quantitative model of the Simpson–Baldwin effect. J Theor Biol 196:197–209

    Article  PubMed  CAS  Google Scholar 

  • Anderson RW (1995) Learning and evolution: a quantitative genetics approach. J Theor Biol 175:89–101

    Article  PubMed  CAS  Google Scholar 

  • Balda RP, Pepperberg IM, Kamil AC (1998) Animal cognition in nature: the convergence of psychology and biology in laboratory and field. Academic, London

    Google Scholar 

  • Bentzen P, McPhail JD (1984) Ecology and evolution of sympatric sticklebacks (Gasterosteus)—specialization for alternative trophic niches in the Enos Lake species pair. Can J Zool 62:2280–2286

    Article  Google Scholar 

  • Bentzen P, Ridgway MS, McPhail JD (1984) Ecology and evolution of sympatric sticklebacks (Gasterosteus)—spatial segregation and seasonal habitat shifts in the Enos Lake species pair. Can J Zool 62:2436–2439

    Google Scholar 

  • Bolhuis JJ, Macphail EM (2001) A critique of the neuroecology of learning and memory. Trends Cog Sci 5:426–433

    Article  Google Scholar 

  • Braithwaite VA, Girvan JR (2003) Use of water flow direction to provide spatial information in a small-scale orientation task. J Fish Biol 63:74–83

    Article  Google Scholar 

  • Brick O, Jakobsson S (2002) Individual variation in risk-taking: the effect of a predatory threat on fighting behavior in Nannacara anomala. Behav Ecol 13:439–442

    Article  Google Scholar 

  • Brodbeck DR (1994) Memory for spatial and local cues: a comparison of a storing and a nonstoring species. Anim Learn Behav 22:119–133

    Google Scholar 

  • Brown C, Warburton K (1999) Differences in timidity and escape responses between predator-naive and predator-sympatric rainbowfish populations. Ethology 105:491–502

    Article  Google Scholar 

  • Clayton NS, Krebs JR (1994) Memory for spatial and object-specific cues in food-storing and non-storing birds. J Comp Phys A 174:371–379

    Google Scholar 

  • Cole S, Hainsworth FR, Kamil AC, Mercier T, Wolf LL (1982) Spatial learning as an adaptation in hummingbirds. Science 217:655–657

    Article  PubMed  Google Scholar 

  • Collett TS, Zeil J (1998) Places and landmarks: an arthropod perspective. In: Healy S (ed) Spatial representation in animals. Oxford University Press, Oxford, pp 18–53

    Google Scholar 

  • Chivers DP, Mirza RS, Johnston JG (2002) Learned recognition of heterospecific alarm cues enhances survival during encounters with predators. Behaviour 139:929–938

    Article  Google Scholar 

  • Dukas R (1998) Cognitive ecology: the evolutionary ecology of information processing and decision making. The University of Chicago Press, Chicago

    Google Scholar 

  • Dukas R (1999) Costs of memory: ideas and predictions. J Theor Biol 197:41–50

    Article  PubMed  CAS  Google Scholar 

  • Etienne AS, Teroni E, Hurni C, Portenier V (1990) The effect of a single light cue on homing behaviour of the golden hamster. Anim Behav 39:17–41

    Article  Google Scholar 

  • Fraser DF, Gilliam JF, Daley MJ, Le AN, Skalski GT (2001) Explaining leptokurtic movement distributions: intrapopulation variation in boldness and exploration. Am Nat 158:124–135

    Article  PubMed  CAS  Google Scholar 

  • Frommen JG, Luz C, Bakker TCM (2007) Kin discrimination in sticklebacks is mediated by social learning rather than innate recognition. Ethology 113:276–282

    Article  Google Scholar 

  • Girvan JR, Braithwaite VA (1998) Population differences in spatial learning in three-spined sticklebacks. Proc R Soc Lond, B 265:913–918

    Article  Google Scholar 

  • Godin JGJ (1995) Predation risk and alternative mating tactics in male Trinidadian guppies (Poecilia reticulata). Oecologia 103:224–229

    Article  Google Scholar 

  • Gow JL, Peichel CL, Taylor EB (2007) Selection against hybrids in natural populations of sympatric threespine sticklebacks. J Evol Biol 20:2173–2180

    Article  PubMed  CAS  Google Scholar 

  • Hatfield T, Schluter D (1999) Ecological speciation in sticklebacks: environment-dependent hybrid fitness. Evolution 53:866–873

    Article  Google Scholar 

  • Healy S, Braithwaite VA (2000) Cognitive ecology: a field of substance? Trends Ecol Evol 15:22–26

    Article  PubMed  Google Scholar 

  • Healy SD, Krebs JR (1993) Development of hippocampal specialisation in a food-storing bird. Behav Brain Res 53:127–131

    Article  PubMed  CAS  Google Scholar 

  • Healy SD, Clayton NS, Krebs JR (1994) Development of hippocampal specialisation in two species of tit (Parus spp.). Behav Brain Res 61:23–28

    Article  PubMed  CAS  Google Scholar 

  • Hughes RN, Blight CM (1999) Algorithmic behaviour and spatial memory are used by two intertidal fish species to solve the radial maze. Anim Behav 58:601–613

    Article  PubMed  Google Scholar 

  • Hughes RN, Blight CM (2000) Two intertidal fish species use visual association learning to track the status of food patches in a radial maze. Anim Behav 59:613–621 109:46–57

    Article  PubMed  Google Scholar 

  • Irwin DE, Price T (1999) Sexual imprinting, learning and speciation. Heredity 82:347–354

    Article  PubMed  Google Scholar 

  • Jablonka E, Lamb MJ (2005) Evolution in four dimensions. Genetic, epigenetic, behavioral and symbolic variation in the history of life. MIT Press, Cambridge

    Google Scholar 

  • Jacobs LF, Gaulin SJC, Sherry DF, Hoffman GE (1990) Evolution of spatial cognition: sex-specific patterns of spatial behavior predict hippocampal size. Proc Nat Acad Sci 87:6349–6352

    Article  PubMed  CAS  Google Scholar 

  • Jenkins J (1997) Pavlovian conditioning of sexual behavior in male threespine stickleback (Gasterosteus aculeatus). Behav Proc 41:133–137

    Article  Google Scholar 

  • Jenkins JR, Rowland WJ (1996) Pavlovian conditioning of agonistic behavior in male threespine stickleback (Gasterosteus aculeatus). J Comp Psychol 110:396–401

    Article  PubMed  CAS  Google Scholar 

  • Juraska JM, Henderson C, Muller J (1984) Differential rearing experience, gender, and radial maze performance. Dev Psychobiol 17:209–215

    Article  PubMed  CAS  Google Scholar 

  • Kamil AC (1998) On the proper definition of cognitive ethology. In: Pepperberg IM, Kamil AC (eds) Animal cognition in nature: the convergence of psychology and biology in laboratory and field. Academic, London, pp 1–28

    Google Scholar 

  • Kozak GM, Boughman JW (2008) Experience influences shoal member preference in a species pair of sticklebacks. Behav Ecol 19:667–676

    Article  Google Scholar 

  • Krebs JR, Healy SD, Shettleworth SJ (1990) Spatial memory of Paridae: comparison of a storing and a non-storing species, the coal tit, Parus ater, and the great tit, P. major. Anim Behav 39:1127–1137

    Article  Google Scholar 

  • Krebs JR, Clayton NS, Healy SD, Cristol DA, Patel SN, Jolliffe AR (1996) The ecology of the avian brain: food-storing memory and the hippocampus. Ibis 138:34–46

    Google Scholar 

  • Lefebvre L (1996) Ecological correlates of social learning: problems and solutions for the comparative method. Behav Proc 35:163–171

    Article  Google Scholar 

  • Losey GS, Sevenster P (1995) Can three-spined sticklebacks learn when to display—rewarded displays. Anim Behav 49:137–150

    Article  Google Scholar 

  • Mackney PA, Hughes RN (1995) Foraging behaviour and memory window in sticklebacks. Behaviour 132:1241–1253

    Article  Google Scholar 

  • Markel RW (1994) An adaptive value of spatial learning and memory in the blackeye goby, Coryphoterus nicholsi. Anim Behav 47:1462–1464

    Article  Google Scholar 

  • McPhail JD (1984) Ecology and evolution of sympatric sticklebacks (Gasterosteus)—morphological and genetic evidence for a species pair in Enos Lake, British Columbia. Can J Zool 62:1402–1408

    Article  Google Scholar 

  • McPhail JD (1992) Ecology and evolution of sympatric sticklebacks (Gasterosteus)—evidence for a species-pair in Paxton Lake, Texada Island, British Columbia. Can J Zool 70:361–369

    Article  Google Scholar 

  • McPhail JD (1993) Ecology and evolution of sympatric sticklebacks (Gasterosteus)—origin of the species pairs. Can J Zool 71:515–523

    Article  Google Scholar 

  • McPhail JD (1994) Speciation and the evolution of reproductive isolation in the sticklebacks (Gasterosteus) of south-western British Columbia. In: Bell MA, Foster SA (eds) The evolutionary biology of the threespine stickleback. Oxford University Press, Oxford, pp 399–437

    Google Scholar 

  • Mery F, Kawecki TJ (2003) A fitness cost of learning ability in Drosophila melanogaster. Proc R Soc Lond, B 270:2465–2469

    Article  Google Scholar 

  • Mery F, Kawecki TJ (2004) An operating cost of learning in Drosophila melanogaster. Anim Behav 68:589–598

    Article  Google Scholar 

  • Mery F, Kawecki TJ (2005) A cost of long-term memory in Drosophila. Science 308:1148

    Article  PubMed  CAS  Google Scholar 

  • Micheli F (1997) Effects of experience on crab foraging in a mobile and a sedentary species. Anim Behav 53:1149–1159

    Article  PubMed  Google Scholar 

  • Milinski M, Bakker TCM (1992) Costs influence sequential mate choice in sticklebacks, Gasterosteus aculeatus. Proc R Soc Lond, B 250:229–233

    Article  Google Scholar 

  • Noda M, Gushima K, Kakuda S (1994) Local prey search based on spatial memory and expectation in the planktivorous reef fish, Chromis chrysurus (Pomacentridae). Anim Behav 47:1413–1422

    Article  Google Scholar 

  • Odling-Smee LC, Braithwaite VA (2003) The influence of habitat stability on landmark use during spatial learning in the three-spined stickleback. Anim Behav 65:701–707

    Article  Google Scholar 

  • Olton DS (1979) Mazes, maps and memory. Am Psychol 34:583–596

    Article  PubMed  CAS  Google Scholar 

  • Owens IPF, Rowe C, Thomas ALR (1999) Sexual selection, speciation and imprinting: separating the sheep from the goats. Trends Ecol Evol 14:131–132

    Article  PubMed  Google Scholar 

  • Reboreda JC, Clayton NS, Kacelnik A (1996) Species and sex differences in hippocampus size in parasitic and non-parasitic cowbirds. NeuroReport 7:505–508

    Article  PubMed  CAS  Google Scholar 

  • Robinson BW, Dukas R (1999) The influence of phenotypic modifications on evolution: the Baldwin effect and modern perspectives. Oikos 85:582–589

    Article  Google Scholar 

  • Rodríguez F, Durán E, Vargas JP, Torres B, Salas C (1994) Performance of goldfish trained in allocentric and egocentric maze procedures suggest the presence of a cognitive mapping system in fishes. Anim Learn Behav 22:409–420

    Google Scholar 

  • Rundle HD, Nagel LM, Boughman JW, Schluter D (2000) Natural selection and parallel speciation in sympatric sticklebacks. Science 287:306–308

    Article  PubMed  CAS  Google Scholar 

  • Schlichting CD, Pigliucci M (1998) Phenotypic evolution: a reaction norm perspective. Sinauer Associates, Sunderland

    Google Scholar 

  • Schluter D (1996) Ecological causes of adaptive radiation. Am Nat 148:S40–S64

    Article  Google Scholar 

  • Schluter D, McPhail JD (1992) Ecological character displacement and speciation in sticklebacks. Am Nat 140:85–108

    Article  CAS  PubMed  Google Scholar 

  • Seymoure P, Dou H, Juraska JM (1996) Sex differences in radial maze performance: influence of rearing environment and room cues. Psychobiol 24:33–37

    Google Scholar 

  • Shettleworth SJ (1993) Where is the comparison in comparative cognition? Am Psychol Soc 4:179–184

    Google Scholar 

  • Shettleworth SJ (1998) Cognition, evolution and the study of behavior. In: Shettleworth SJ (ed) Cognition, evolution and behavior. Oxford University Press, New York, pp 3–48

    Google Scholar 

  • Shettleworth SJ, Westwood RP (2002) Divided attention, memory, and spatial discrimination in food-storing and nonstoring birds, black-capped chickadees (Poecile atricapilla) and dark-eyed juncos (Junco hyemalis). J Exp Psych - Anim Behav Proc 28:227–241

    Article  Google Scholar 

  • Stamps J (2003) Behavioural processes affecting development: Tinbergen’s fourth question comes of age. Anim Behav 66:1–13

    Article  Google Scholar 

  • Taylor EB, McPhail JD (2000) Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus. Proc R Soc Lond, B 267:2375–2384

    Article  CAS  Google Scholar 

  • Vamosi SM (2002) Predation sharpens the adaptive peaks: survival trade-offs in sympatric sticklebacks. Ann Zool Fenn 39:237–248

    Google Scholar 

  • Warburton K (2003) Learning of foraging skills by fish. Fish Fish 4:203–215

    Google Scholar 

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Acknowledgments

We thank D. Schluter for his assistance and generous provision of facilities. We thank S. Vamosi, D. Taylor and H. Rundle for technical assistance; T. Vines for statistical advice; and C. Brown and S. West for valuable comments on earlier drafts of the manuscript. This research was supported by the Biotechnology and Biological Sciences Research Council, the Fisheries Society of the British Isles and The University of Edinburgh Student Travel Fund and Development and Alumni Services. This research was conducted in accordance with animal care guidelines of the University of British Columbia and University of Edinburgh.

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Correspondence to Janette W. Boughman.

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Communicated by T. Bakker

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Odling-Smee, L.C., Boughman, J.W. & Braithwaite, V.A. Sympatric species of threespine stickleback differ in their performance in a spatial learning task. Behav Ecol Sociobiol 62, 1935–1945 (2008). https://doi.org/10.1007/s00265-008-0625-1

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