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Guppies show sex and individual differences in the ability to inhibit behaviour

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Abstract

In humans, individual and sex differences have been long reported for several cognitive tasks and are at least in part due to variability in the function that inhibits behaviour (i.e. inhibitory control). Similar evidence of individual and sex differences in inhibitory abilities is also present in other vertebrates, but is scarce outside primates. Experiments on reversal learning, which requires inhibiting behaviours, suggest that this variability may exist in a teleost fish, the guppy, Poecilia reticulata. We tested this hypothesis by observing guppies in an inhibitory task. Guppies were exposed to unreachable prey inside a transparent tube for six trials. Guppies showed a marked reduction in the number of attempts to catch the prey within the first trial and also over repeated trials. We found a striking sex difference in the capacity to inhibit foraging behaviour. Males attempted to attack the prey twice as often as females and showed negligible improvement over trials. Irrespective of sex, individuals remarkably differed in their performance, with some guppies being systematically more skilled than others across the repeated trials. These results confirm that individual and sex differences in the ability to inhibit behaviour are not restricted to humans and other primates, suggesting that they might be widespread among vertebrates. Variability in inhibitory ability provides an explanation for emerging records of variability in other cognitive tasks in fish.

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References

  • Agin V, Dickel L, Chichery R, Chichery MP (1998) Evidence for a specific short-term memory in the cuttlefish, Sepia. Behav Process 43:329–334

    CAS  Google Scholar 

  • Amici F, Aureli F, Call J (2008) Fission-fusion dynamics, behavioral flexibility, and inhibitory control in primates. Curr Biol 18:1415–1419

    CAS  PubMed  Google Scholar 

  • Baler RD, Volkow ND (2006) Drug addiction: the neurobiology of disrupted self-control. Trend Mol Med 12:559–566

    CAS  Google Scholar 

  • Beran MJ (2015) The comparative science of “self-control”: what are we talking about? Front Psychol 6:51

    PubMed  PubMed Central  Google Scholar 

  • Beran MJ, Hopkins WD (2018) Self-control in chimpanzees relates to general intelligence. Curr Biol 28:574–579

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brandão ML, Braithwaite VA, Gonçalves-de-Freitas E (2015) Isolation impairs cognition in a social fish. Appl Anim Behav Sci 171:204–210

    Google Scholar 

  • Bshary R, Brown C (2014) Fish cognition. Curr Biol 24:R947–R950

    CAS  PubMed  Google Scholar 

  • Buechel SD, Boussard A, Kotrschal A, van der Bijl W, Kolm N (2018) Brain size affects performance in a reversal-learning test. Proc R Soc B 285:20172031

    PubMed  Google Scholar 

  • Cain K (2006) Individual differences in children's memory and reading comprehension: An investigation of semantic and inhibitory deficits. Memory 14:553–569

    PubMed  Google Scholar 

  • Carere C, Locurto C (2011) Interaction between animal personality and animal cognition. Curr Zool 57:491–498

    Google Scholar 

  • Cong L, Wang Z, Chai Y, Hang W, Shang C, Yang W et al (2017) Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (Danio rerio). Elife 6:e28158

    PubMed  PubMed Central  Google Scholar 

  • Dahlgren BT (1981) Impact of different dietary protein contents on fecundity and fertility in the female guppy, Poecilia reticulata (Peters). Biol Reprod 24:734–746

    CAS  PubMed  Google Scholar 

  • Diamond A (1990) Developmental time course in human infants and infant monkeys, and the neural bases of inhibitory control in reaching. Ann N Y Acad Sci 608:637–676

    CAS  PubMed  Google Scholar 

  • Diamond A (2013) Executive Functions. Ann Rev Psychol 64:135–168

    Google Scholar 

  • Enticott PG, Ogloff JR, Bradshaw JL, Fitzgerald PB (2008) Cognitive inhibitory control and self-reported impulsivity among violent offenders with schizophrenia. J Clin Exp Neuropsychol 30:157–162

    PubMed  Google Scholar 

  • Estep DQ, Nieuwenhuijsen K, Bruce KE, De Neef KJ, Walters PA III, Baker SC, Slob AK (1988) Inhibition of sexual behaviour among subordinate stumptail macaques, Macaca arctoides. Anim Behav 36:854–864

    Google Scholar 

  • Etheredge RI, Avenas C, Armstrong MJ, Cummings ME (2018) Sex-specific cognitive–behavioural profiles emerging from individual variation in numerosity discrimination in Gambusia affinis. Anim Cogn 21:37–53

    PubMed  Google Scholar 

  • Garavan H, Hester R, Murphy K, Fassbender C, Kelly C (2006) Individual differences in the functional neuroanatomy of inhibitory control. Brain Res 1105:130–142

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Genty E, Roeder JJ (2006) Self-control: why should sea lions, Zalophus californianus, perform better than primates? Anim Behav 72:1241–1247

    Google Scholar 

  • Gibbs RB, Johnson DA (2008) Sex-specific effects of gonadectomy and hormone treatment on acquisition of a 12-arm radial maze task by Sprague Dawley rats. Endocrinology 149:3176–3183

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gilmore C, Attridge N, Clayton S, Cragg L, Johnson S, Marlow N et al (2013) Individual differences in inhibitory control, not non-verbal number acuity, correlate with mathematics achievement. PLoS ONE 8:e67374

    CAS  PubMed  PubMed Central  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

    PubMed  Google Scholar 

  • Hausmann M, Slabbekoorn D, Van Goozen SH, Cohen-Kettenis PT, Güntürkün O (2000) Sex hormones affect spatial abilities during the menstrual cycle. Behav Neurosci 114:1245–1250

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Jones CM, Braithwaite VA, Healy SD (2003) The evolution of sex differences in spatial ability. Behav Neurosci 117:403–411

    PubMed  Google Scholar 

  • Kabadayi C, Taylor LA, von Bayern AM, Osvath M (2016) Ravens, New Caledonian crows and jackdaws parallel great apes in motor self-regulation despite smaller brains. Roy Soc Open Sci 3:160104

    Google Scholar 

  • Kabadayi C, Krasheninnikova A, O’neill L, van de Weijer J, Osvath M, von Bayern AM (2017) Are parrots poor at motor self-regulation or is the cylinder task poor at measuring it? Anim Cogn 20:1137–1146

    PubMed  PubMed Central  Google Scholar 

  • Kieffer JD, Colgan PW (1991) Individual variation in learning by foraging pumpkinseed sunfish, Lepomis gibbosus: the influence of habitat. Anim Behav 41:603–611

    Google Scholar 

  • Kralik JD, Hauser MD, Zimlicki R (2002) The relationship between problem solving and inhibitory control: Cotton-top tamarins (Saguinus oedipus) performance on a reversed contingency task. J Comp Psychol 116:39

    PubMed  Google Scholar 

  • Lindsay DR, Dunsmore DG, Williams JD, Syme GJ (1976) Audience effects on the mating behaviour of rams. Anim Behav 24:818–821

    Google Scholar 

  • Lucon-Xiccato T, Bertolucci C (2019) Guppies show rapid and lasting inhibition of foraging behaviour. Behav Process 164:91–99

    Google Scholar 

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

    PubMed Central  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Lucon-Xiccato T, Dadda M (2017) Individual guppies differ in quantity discrimination performance across antipredator and foraging contexts. Behav Ecol Sociobiol 71:13

    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

    Google Scholar 

  • Lucon-Xiccato T, Gatto E, Bisazza A (2017) Fish perform like mammals and birds in inhibitory motor control tasks. Sci Rep 7:13144

    PubMed  PubMed Central  Google Scholar 

  • Lucon-Xiccato T, Montalbano G, Bertolucci C (2019) Personality traits covary with individual differences in inhibitory abilities in 2 species of fish. Curr Zool. https://doi.org/10.1093/cz/zoz039

    Article  PubMed  PubMed Central  Google Scholar 

  • MacLean EL et al (2014) The evolution of self-control. Proc Nat Acad Sci 111:E2140–E2148

    CAS  PubMed  Google Scholar 

  • Magurran AE, Seghers BH (1994) A cost of sexual harassment in the guppy, Poecilia reticulata. Proc R Soc B 258:89–92

    Google Scholar 

  • Miletto Petrazzini ME, Bisazza A, Agrillo C, Lucon-Xiccato T (2017) Sex differences in discrimination reversal learning in the guppy. Anim Cogn 20:1081–1091

    PubMed  Google Scholar 

  • Müller CA, Riemer S, Virányi Z, Huber L, Range F (2016) Inhibitory control, but not prolonged object-related experience appears to affect physical problem-solving performance of pet dogs. PLoS ONE 11:e0147753

    PubMed  PubMed Central  Google Scholar 

  • Nigg JT (2001) Is ADHD a disinhibitory disorder? Psychol Bull 127:571–598

    CAS  PubMed  Google Scholar 

  • Rankin CH, Abrams T, Barry RJ, Bhatnagar S, Clayton DF, Colombo J et al (2009) Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. Neurobiol Learn Mem 92:135–138

    PubMed  Google Scholar 

  • Reader SM, Laland KN (2000) Diffusion of foraging innovations in the guppy. Anim Behav 60:175–180

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Rohr JR, Madison DM (2001) A chemically mediated trade-off between predation risk and mate search in newts. Anim Behav 62:863–869

    Google Scholar 

  • Rowe C, Healy SD (2014) Measuring variation in cognition. Behav Ecol 25:1287–1292

    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

    PubMed  Google Scholar 

  • Roy T, Bhat A (2018) Divergences in learning and memory among wild zebrafish: Do sex and body size play a role? Learn Behav 46:124–133

    PubMed  Google Scholar 

  • Ryer CH, Olla BL (1991) Information transfer and the facilitation and inhibition of feeding in a schooling fish. Environ Biol Fishes 30:317–323

    Google Scholar 

  • Santacà M, Busatta M, Lucon-Xiccato T, Bisazza A (2019) Sensory differences mediate species variation in detour task performance. Anim Behav 155:153–162

    Google Scholar 

  • Shamosh NA, DeYoung CG, Green AE, Reis DL, Johnson MR, Conway AR, Engle RW, Braver TS, Gray JR (2008) Individual differences in delay discounting: relation to intelligence, working memory, and anterior prefrontal cortex. Psychol Sci 19:904–911

    PubMed  Google Scholar 

  • Shettleworth SJ (2009) Cognition, evolution, and behavior. Oxford University Press, Oxford

    Google Scholar 

  • Studzinski ALM, Barros DM, Marins LF (2015) Growth hormone (GH) increases cognition and expression of ionotropic glutamate receptors (AMPA and NMDA) in transgenic zebrafish (Danio rerio). Behav Brain Res 294:36–42

    CAS  PubMed  Google Scholar 

  • Szabo B, Whiting MJ, Noble DW (2019) Sex-dependent discrimination learning in lizards: a meta-analysis. Behav Process. https://doi.org/10.1016/j.beproc.2019.04.002

    Article  Google Scholar 

  • Tapp PD, Siwak CT, Estrada J, Head E, Muggenburg BA, Cotman CW, Milgram NW (2003) Size and reversal learning in the beagle dog as a measure of executive function and inhibitory control in aging. Learn Mem 10:64–73

    PubMed  PubMed Central  Google Scholar 

  • Thornton A, Lukas D (2012) Individual variation in cognitive performance: developmental and evolutionary perspectives. Philos Trans R Soc B 367:2773–2783

    Google Scholar 

  • van Horik JO, Langley EJ, Whiteside MA, Laker PR, Beardsworth CE, Madden JR (2018) Do detour tasks provide accurate assays of inhibitory control? Proc R Soc B 285:20180150

    PubMed  Google Scholar 

  • Vlamings PH, Hare B, Call J (2010) Reaching around barriers: the performance of the great apes and 3–5-year-old children. Anim Cogn 13:273–285

    PubMed  Google Scholar 

  • Völter CJ, Tinklenberg B, Call J, Seed AM (2018) Comparative psychometrics: establishing what differs is central to understanding what evolves. Philos Trans R Soc B 373:20170283

    Google Scholar 

  • White SL, Wagner T, Gowan C, Braithwaite VA (2017) Can personality predict individual differences in brook trout spatial learning ability? Behav Process 141:220–228

    CAS  Google Scholar 

  • Widholm JJ, Clarkson GB, Strupp BJ, Crofton KM, Seegal RF, Schantz SL (2001) Spatial reversal learning in Aroclor 1254-exposed rats: sex-specific deficits in associative ability and inhibitory control. Toxicol Appl Pharmacol 174:188–198

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Andrea Margutti for his help in building the apparatuses and Giulia Trioschi for help in testing the subjects.

Funding

This work was supported by FAR 2018 and FIR 2018 Grant from University of Ferrara to TLX.

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Authors and Affiliations

  1. Department of Life Sciences and Biotechnology, University of Ferrara, Via Borsari 46, 44121, Ferrara, Italy

    Tyrone Lucon-Xiccato & Cristiano Bertolucci

  2. Department of General Psychology, University of Padova, Padova, Italy

    Angelo Bisazza

  3. Padova Neuroscience Center, University of Padova, Padova, Italy

    Angelo Bisazza

Authors
  1. Tyrone Lucon-Xiccato
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  2. Angelo Bisazza
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  3. Cristiano Bertolucci
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Correspondence to Tyrone Lucon-Xiccato.

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The authors declare that they have no conflict of interest.

Ethical approval

The experiment followed the law of the country in which they were performed (Italy, D.L. 4 Marzo 2014, n. 26). The Ethical Committee of the University of Ferrara reviewed and approved all the experimental procedures (TLX 2-2018-PR). No fish showed sign of distress during the experiments. We released all the fish into stock tanks after the study for future breeding purposes.

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Lucon-Xiccato, T., Bisazza, A. & Bertolucci, C. Guppies show sex and individual differences in the ability to inhibit behaviour. Anim Cogn 23, 535–543 (2020). https://doi.org/10.1007/s10071-020-01357-4

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