Skip to main content
SpringerLink
Log in

Sex differences in discrimination reversal learning in the guppy

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

Abstract

In several mammalian and avian species, females show a higher performance than males in tasks requiring cognitive flexibility such as the discrimination reversal learning. A recent study showed that female guppies are twice as efficient as males in a reversal learning task involving yellow–red discrimination, suggesting a higher cognitive flexibility in female guppies. However, the possibility exists that the superior performance exhibited by females does not reflect a general sex difference in cognitive abilities, but instead, is confined to colour discrimination tasks. To address this issue, we compared male and female guppies in two different discrimination reversal learning tasks and we performed a meta-analysis of these experiments and the previous one involving colour discrimination. In the first experiment of this study, guppies were tested in a task requiring them to learn to select the correct arm of a T-maze in order to rejoin a group of conspecifics. In experiment 2, guppies were observed in a numerical task requiring them to discriminate between 5 and 10 dots in order to obtain a food reward. Although females outperformed males in one condition of the T-maze, we did not find any clear evidence of females’ greater reversal learning performance in either experiment. However, the meta-analysis of the three experiments supported the hypothesis of females’ greater reversal learning ability. Our data do not completely exclude the idea that female guppies have a generally higher cognitive flexibility than males; however, they suggest that the size of this sex difference might depend on the task.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agrillo C, Bisazza A (2014) Spontaneous versus trained numerical abilities. A comparison between the two main tools to study numerical competence in non-human animals. J Neurosci Met 234:82–91

    Article  Google Scholar 

  • Agrillo C, Miletto Petrazzini ME, Bisazza A (2017) Numerical abilities in fish: a methodological review. Behav Process 141:161–171

    Article  Google Scholar 

  • Barchard KA (2015) Null hypothesis significance testing does not show equivalence. Anal Soc Issues Public Policy 15:418–421

    Article  Google Scholar 

  • Bisazza A, Brown C (2011) Lateralization of cognitive functions in fish. In: Brown C, Krause J, Laland KN (eds) Fish cognition and behavior. Wiley, Oxford, pp 298–324

    Chapter  Google Scholar 

  • Bisazza A, Facchin L, Pignatti R, Vallortigara G (1998) Lateralization of detour behaviour in poeciliid fish: the effect of species, gender and sexual motivation. Behav Brain Res 91:157–164

    Article  CAS  PubMed  Google Scholar 

  • Brust V, Wuerz Y, Krüger O (2013) Behavioural flexibility and personality in zebra finches. Ethology 119:559–569

    Article  Google Scholar 

  • Burghardt GM, Hess EH (1966) Food imprinting in the snapping turtle, Chelydra serpentina. Science 151:108–109

    Article  CAS  PubMed  Google Scholar 

  • Crawley MJ (2012) The R book. Wiley, Chichester

    Book  Google Scholar 

  • Croze H (1970) Searching image in carrion crows. Paul Parey, Berlin

    Google Scholar 

  • Dugatkin LA, Godin JGJ (1992) Reversal of female mate choice by copying in the guppy (Poecilia reticulata). Proc R Soc Lond Ser B Biol Sci 249:179–184

    Article  CAS  Google Scholar 

  • Eakley AL, Houde AE (2004) Possible role of female discrimination against ‘redundant’ males in the evolution of colour pattern polymorphism in guppies. Proc R Soc Lond Ser B Biol Sci 271:S299–S301

    Article  Google Scholar 

  • Elias MF, Dupree M, Eleftheriou BE (1973) Differences in spatial discrimination reversal learning between two inbred mouse strains following specific amygdaloid lesions. J Comp Physiol Psychol 83:149–156

    Article  CAS  PubMed  Google Scholar 

  • Feigenson L, Carey S, Spelke E (2002) Infants’ discrimination of number vs. continuous extent. Cogn Psychol 44:33–66

    Article  PubMed  Google Scholar 

  • Gasparini C, Serena G, Pilastro A (2013) Do unattractive friends make you look better? Context-dependent male mating preferences in the guppy. Proc R Soc Lond Ser B Biol Sci 280:20123072

    Article  Google Scholar 

  • Gaulin SJ, FitzGerald RW (1986) Sex differences in spatial ability: an evolutionary hypothesis and test. Am Nat 127:74–88

    Article  Google Scholar 

  • Gebuis T, Reynvoet B (2012) The interplay between nonsymbolic number and its continuous visual properties. J Exp Psychol Gen 141:642–648

    Article  PubMed  Google Scholar 

  • Godin JGJ, Herdman EJ, Dugatkin LA (2005) Social influences on female mate choice in the guppy, Poecilia reticulata: generalized and repeatable trait-copying behaviour. Anim Behav 69:999–1005

    Article  Google Scholar 

  • Gómez-Laplaza LM, Gerlai R (2010) Latent learning in zebrafish (Danio rerio). Behav Brain Res 208:509–515

    Article  PubMed  Google Scholar 

  • Gong A, Gibson RM (1996) Reversal of a female preference after visual exposure to a predator in the guppy, Poecilia reticulata. Anim Behav 52:1007–1015

    Article  Google Scholar 

  • Grether GF (2000) Carotenoid limitation and mate preference evolution: a test of the indicator hypothesis in guppies (Poecilia reticulata). Evolution 54:1712–1724

    Article  CAS  PubMed  Google Scholar 

  • Griffin AS, Guillette LM, Healy SD (2015) Cognition and personality: an analysis of an emerging field. Trends Ecol Evol 30:207–214

    Article  PubMed  Google Scholar 

  • Guillamón A, Valencia A, Calés J, Segovia S (1986) Effects of early postnatal gonadal steroids on the successive conditional discrimination reversal learning in the rat. Physiol Behav 38:845–849

    Article  PubMed  Google Scholar 

  • Ha JC, Mandell DJ, Gray J (2011) Two-item discrimination and Hamilton search learning in infant pigtailed macaque monkeys. Behav Process 86:1–6

    Article  Google Scholar 

  • Houde AE (1997) Sex, color, and mate choice in guppies. Princeton University Press, Princeton

    Google Scholar 

  • Hughes KA, Du L, Rodd FH, Reznick DN (1999) Familiarity leads to female mate preference for novel males in the guppy, Poecilia reticulata. Anim Behav 58:907–916

    Article  CAS  PubMed  Google Scholar 

  • Jeffreys H (1961) Theory of probability, 3rd edn. Oxford University Press, Oxford

    Google Scholar 

  • Kellogg WN, Gavin J (1960) Maze-learning in the guppy. Psychol Rep 6:445–446

    Article  Google Scholar 

  • Kodric-Brown A (1989) Dietary carotenoids and male mating success in the guppy: an environmental component to female choice. Behav Ecol Sociobiol 25:393–401

    Article  Google Scholar 

  • Lakens D, Evers ER (2014) Sailing from the seas of chaos into the corridor of stability: practical recommendations to increase the informational value of studies. Perspect Psychol Sci 9:278–292

    Article  PubMed  Google Scholar 

  • Laland KN, Reader SM (1999) Foraging innovation in the guppy. Anim Behav 57:331–340

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Burmeister SS (2017) Sex differences during place learning in the túngara frog. Anim Behav 128:61–67

    Article  Google Scholar 

  • Lucon-Xiccato T, Bisazza A (2014) Discrimination reversal learning reveals greater female behavioural flexibility in guppies. Biol Lett 10:20140206

    Article  PubMed Central  Google Scholar 

  • Lucon-Xiccato T, Bisazza A (2016) Male and female guppies differ in speed but not in accuracy in visual discrimination learning. Anim Cogn 19:733–744

    Article  PubMed  Google Scholar 

  • Lucon-Xiccato T, Bisazza A (2017a) Sex differences in spatial abilities and cognitive flexibility in the guppy. Anim Behav 123:53–60

    Article  Google Scholar 

  • Lucon-Xiccato T, Bisazza A (2017b) Complex maze learning by fish. Anim Behav 125:69–75

    Article  Google Scholar 

  • Lucon-Xiccato T, Bisazza A (2017c) Individual differences in cognition among teleost fishes. Behav Process 141:184–195

    Article  Google Scholar 

  • Lucon-Xiccato T, Miletto Petrazzini ME, Agrillo C, Bisazza A (2015) Guppies discriminate between two quantities of food items but prioritize item size over total amount. Anim Behav 107:183–191

    Article  Google Scholar 

  • Lucon-Xiccato T, Dadda M, Bisazza A (2016) Sex differences in discrimination of shoal size in the guppy (Poecilia reticulata). Ethology 122:481–491

    Article  Google Scholar 

  • Mackintosh NJ (1965) Overtraining, reversal, and extinction in rats and chicks. J Comp Physiol Psychol 59:31–36

    Article  CAS  PubMed  Google Scholar 

  • Mackintosh NJ, Mackintosh J, Safriel-Jorne O, Sutherland NS (1966) Overtraining, reversal and extinction in the goldfish. Anim Behav 14:314–318

    Article  CAS  PubMed  Google Scholar 

  • Mandler G, Shebo BJ (1982) Subitizing: an analysis of its component processes. J Exp Psychol Gen 111:1–22

    Article  CAS  PubMed  Google Scholar 

  • Miletto Petrazzini ME, Agrillo C, Izard V, Bisazza A (2015a) Relative versus absolute numerical representation in fish: can guppies represent “fourness”? Anim Cogn 18:1007–1017

    Article  PubMed  Google Scholar 

  • Miletto Petrazzini ME, Lucon-Xiccato T, Agrillo C, Bisazza A (2015b) Use of ordinal information by fish. Sci Rep 5:15497

    Article  Google Scholar 

  • Persons MH, Rypstra AL (2000) Preference for chemical cues associated with recent prey in the wolf spider Hogna helluo (Araneae: Lycosidae). Ethology 106:27–35

    Article  Google Scholar 

  • Pisa PE, Agrillo C (2009) Quantity discrimination in felines: a preliminary investigation of the domestic cat (Felis silvestris catus). J Ethol 27:289–293

    Article  Google Scholar 

  • Rabinowitch V (1969) The role of experience in the development and retention of seed preferences in zebra finches. Behaviour 33:222–235

    Article  Google Scholar 

  • Reddon AR, Hurd PL (2009) Sex differences in the cerebral lateralization of a cichlid fish when detouring to view emotionally conditioned stimuli. Behav Process 82:25–29

    Article  Google Scholar 

  • Rilea SL, Roskos-Ewoldsen B, Boles D (2004) Sex differences in spatial ability: a lateralization of function approach. Brain Cogn 56:332–343

    Article  PubMed  Google Scholar 

  • Rodd FH, Hughes KA, Grether GF, Baril CT (2002) A possible non-sexual origin of mate preference: are male guppies mimicking fruit? Proc R Soc Lond Ser B Biol Sci 269:475–481

    Article  Google Scholar 

  • Roelofs S, Nordquist RE, van der Staay FJ (2017) Female and male pigs’ performance in a spatial holeboard and judgment bias task. Appl Anim Behav Sci. doi:10.1016/j.applanim.2017.01.016

    Google Scholar 

  • Rogers LJ (1974) Persistence and search influenced by natural levels of androgens in young and adult chickens. Physiol Behav 12:197–204

    Article  CAS  PubMed  Google Scholar 

  • Rowe L, Cameron E, Day T (2005) Escalation, retreat, and female indifference as alternative outcomes of sexually antagonistic coevolution. Am Nat 165:S5–S18

    Article  PubMed  Google Scholar 

  • Shettleworth SJ (2010) Cognition, evolution, and behavior. Oxford University Press, Oxford

    Google Scholar 

  • Tinbergen L (1960) The natural control of insects in pinewoods. Arch Neerl Zool 13:265–343

    Article  Google Scholar 

  • Titulaer M, van Oers K, Naguib M (2012) Personality affects learning performance in difficult tasks in a sex-dependent way. Anim Behav 83:723–730

    Article  Google Scholar 

  • Tommasi L, Vallortigara G (2004) Hemispheric processing of landmark and geometric information in male and female domestic chicks (Gallus gallus). Behav Brain Res 155:85–96

    Article  PubMed  Google Scholar 

  • Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw 36:1–48

    Article  Google Scholar 

  • Wagenmakers EJ (2007) A practical solution to the pervasive problems of p values. Psychon Bull Rev 14:779–804

    Article  PubMed  Google Scholar 

  • Warren JM (1960) Reversal learning by paradise fish (Macropodus opercularis). J Comp Physiol Psychol 53:376–378

    Article  CAS  PubMed  Google Scholar 

  • Watson DJ, Stanton ME (2009) Intrahippocampal administration of an NMDA-receptor antagonist impairs spatial discrimination reversal learning in weanling rats. Neurobiol Learn Mem 92:89–98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank Immacolata Orrù and Jacqueline Giada Mazzon for their help in testing the animals. This study was founded by “PRIN 2015” (prot.: 2015FFATB7) from the University of Padova to Angelo Bisazza.

Author information

Authors and Affiliations

  1. Dipartimento di Psicologia Generale, Università di Padova, Via Venezia 8, 35131, Padua, Italy

    Maria Elena Miletto Petrazzini, Angelo Bisazza, Christian Agrillo & Tyrone Lucon-Xiccato

Authors
  1. Maria Elena Miletto Petrazzini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Angelo Bisazza
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christian Agrillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tyrone Lucon-Xiccato
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria Elena Miletto Petrazzini.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standard

Experiments were conducted in agreement with the law of our country (Italy, D.L. 4 Marzo 2014, n. 26). The Ethical Committee of the University of Padova reviewed and approved the experimental procedures (Protocol n. 33/2015 and n. 22/2016). None of the subjects showed sign of distress. At the end of the experiments, all subjects were released into the maintenance tanks.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miletto Petrazzini, M.E., Bisazza, A., Agrillo, C. et al. Sex differences in discrimination reversal learning in the guppy. Anim Cogn 20, 1081–1091 (2017). https://doi.org/10.1007/s10071-017-1124-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-017-1124-4

Keywords

Search

Navigation