Abstract
The relationship between an individual’s cognitive abilities and other behavioural attributes is complex, yet critical to understanding how individual differences in cognition arise. Here we use western mosquitofish, Gambusia affinis, to investigate the relationship between individual associative learning performance in numerical discrimination tests and independent measures of activity, exploration, anxiety and sociability. We found extensive and highly repeatable inter-individual variation in learning performance (r = 0.89; ICC = 0.89). Males and females exhibited similar learning performance, yet differed in sociability, activity and their relationship between learning and anxiety/exploration tendencies. Sex-specific multivariate behaviour scores successfully predicted variation in individual learning performance, whereas combined sex analyses did not. Female multivariate behaviour scores significantly predict learning performance across females (ρ = 0.80, p = 0.005) with high-performing female learners differentiated from female non-learners and low-performing learners by significant contributions of activity and sociability measures. Meanwhile, males of different learning performance levels (high-, low- and non-learners) were distinguished from each other by unique behavioural loadings of sociability, activity and anxiety/exploration scores, respectively. Our data suggest that despite convergence on learning performance, the sexes diverge in cognitive–behavioural relationships that are likely products of different sexual selection pressures.
Similar content being viewed by others
References
Agrillo C, Dadda M, Bisazza A (2006) Sexual harassment influences group choice in female mosquitofish. Ethology 112:592–598. doi:10.1111/j.1439-0310.2006.01188.x
Agrillo C, Dadda M, Serena G, Bisazza A (2008) Do fish count? Spontaneous discrimination of quantity in female mosquitofish. Anim Cogn 11:495–503. doi:10.1007/s10071-008-0140-9
Agrillo C, Miletto Petrazzini ME, Piffer L, Dadda M, Bisazza A (2012a) A new training procedure for studying discrimination learning in fishes. Behav Brain Res 230:343–348
Agrillo C, Miletto Petrazzini ME, Tagliapietra C, Bisazza A (2012b) Inter-specific differences in numerical abilities among teleost fish. Front Psychol 3:483. doi:10.3389/fpsyg.2012.00483
Agrillo C, Miletto Petrazzini ME, Bisazza A (2017) Numerical abilities in fish: a methodological review. Behav Proc 141:161–171
Auge A-C, Auld HL, Sherratt TN, Godin J-GJ (2016) Do males form social associations based on sexual attractiveness in a fission-fusion fish society? PLoS ONE 11(3):e0151243. doi:10.1371/journal.pone.0151243
Bell A (2012) Randomized or fixed order for studies of behavioral syndromes? Behav Ecol 24:16–20. doi:10.1093/beheco/ars148
Bisazza A (1993) Male competition, female mate choice and sexual size dimorphism in poeciliid fishes. In: Huntingford F, Torricelli P (eds) The behavioural ecology of fishes. Harwood Academic Press, Amsterdam, pp 257–286
Bisazza A, Marin G (1995) Sexual selection and sexual size dimorphism in the eastern mosquitofish Gambusia holbrooki (Pisces Poeciliidae). Ethol Ecol Evol 7:169–183
Bisazza A, Agrillo C, Lucon-Xiccato T (2014) Extensive training extends numerical abilities of guppies. Anim Cogn 17:1413–1419
Brust V, Würz Y, Krüger O (2013) Behavioural flexibility and personality in zebra finches. Ethology 119:559–569. doi:10.1111/eth.12095
Buechel S, Booksmythe I, Kotrschal A, Jennions MD, Kolm N (2016) Artificial selection on male genitalia length alters female brain size. Proc R Soc Lond B 283:20161796. doi:10.1098/rspb.2016.1796
Carere C, Locurto C (2011) Interaction between animal personality and animal cognition. Curr Zool 57:491–498. doi:10.1093/czoolo/57.4.491
Carter AJ, Feeney WE, Marshall HH, Cowlishaw G, Heinsohn R (2013) Animal personality: what are behavioural ecologists measuring? Biol Rev 88:465–475
Chapman BB, Ward AJW, Krause J (2008) Schooling and learning: early social environment predicts social learning ability in the guppy, Poecilia reticulata. Anim Behav 76:923–929. doi:10.1016/j.anbehav.2008.03.022
Cote J, Dreiss A, Clobert J (2008) Social personality trait and fitness. Proc R Soc B 275:2851–2858. doi:10.1098/rspb.2008.0783
Cote J, Fogarty S, Weinersmith K, Brodin T, Sih A (2010) Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis). Proc R Soc B 277:1571–1579. doi:10.1098/rspb.2009.2128
Cote J, Fogarty S, Brodin T, Weinersmith K, Sih A (2011) Personality-dependent dispersal in the invasive mosquitofish: group composition matters. Proc R Soc B 278:1670–1678
Cote J, Fogerty S, Sih A (2012) Individual sociability and choosiness between shoal types. Anim Behav 83:1469–1476. doi:10.1016/j.anbehav.2012.03.019
Crespi BJ, Hurd PL (2014) Cognitive-Behavioral phenotypes of Williams syndrome are associated with genetic variation of the GTF2I gene, in a healthy population. BMC Neurosci 15:127. doi:10.1186/s12868-014-0127-1
Croft DP, Morrell LJ, Wade AS, Piyapong C, Ioannou CC, Dyer JRG, Champman BB, Yan W, Krause J (2006) Predation risk as a driving force for sexual segregation: a cross-population comparison. Am Nat 167:867–878
DePasquale C, Wagner T, Archard GA, Ferguson B, Braithwaite VA (2014) Learning rate and temperament in a high predation risk environment. Oecologia 176:661–667
Dickman SJ (1990) Functional and dysfunctional impulsivity: personality and cognitive correlates. J Pers Soc Psychol 58:95–102. doi:10.1037/0022-3514.58.1.95
Dingemanse NJ, Both C, Drent PJ, Tinbergen JM (2004) Fitness consequence of avian personalities in a fluctuating environment. Proc R Soc B 271:847–852. doi:10.1098/rspb.2004.2680
Dugatkin LA, Alfieri MS (2003) Boldness, behavioral inhibition and learning. Ethol Ecol Evol 15:43–49
Dukas R (2008) Evolutionary biology of insect learning. Annu Rev Entomol 53:145–160. doi:10.1146/annurev.ento.53.103106.093343
Dunbar RIM (1998) The social brain hypothesis. Evol Anthrol 6:178–190. doi:10.1002/(SICI)1520-6505(1998)6:5<178:AID-EVAN5>3.0.CO;2-8
Dunbar RIM, Shultz S (2007) Evolution in the social brain. Science 317:1344–1347
Dyer JRG, Croft DP, Morrell LJ, Krause J (2009) Shoal composition determines foraging success in the guppy. Behav Ecol 20:165–171. doi:10.1093/beheco/arn129
Fernald RD (2017) Cognitive skills and the evolution of social systems. J Exp Biol 220:103–113. doi:10.1242/jeb.142430
Friendly M, Fox J (2016) Candisc: visualizing generalized canonical discriminant and canonical correlation analysis. R package version 0.7-2. https://CRAN.R-project.org/package=candisc
Gaulin SJ, Fitzgerald RW (1986) Sex differences in spatial ability: an evolutionary hypothesis and test. Am Nat 127:74–88
Goldberg TE, Weinberger DR (2004) Genes and the parsing of cognitive processes. Trends Cogn Sci 8:325–335. doi:10.1016/j.tics.2004.05.011
Greggor AL, Thornton A, Clayton N (2015) Neophobia is not only avoidance: improving neophobia tests by combining cognition and ecology. Curr Opin Behav Sci 6:82–89
Griffin AS, Guillette LM, Healy SD (2015) Cognition and personality: an analysis of an emerging field. Trends Ecol Evol 30:207–214. doi:10.1016/j.tree.2015.01.012
Griffiths SW, Magurran AE (1998) Sex and schooling behaviour in the Trinidadian guppy. Anim Behav 56:689–693. doi:10.1006/anbe.1998.0767
Guigueno MF, Snow DA, MacDougall-Schackleton SA, Sherry DF (2014) Female cowbirds have more accurate spatial memory than males. Biol Let 10:1–4
Guillette LM, Reddon AR, Hurd PL, Sturdy CB (2009) Exploration of a novel space is associated with individual differences in learning speed in a novel space is associated with individual differences in learning speed in black-capped chickadees, Poecile atricapillus. Behav Proc 82:265–270. doi:10.1016/j.beproc.2009.07.005
Harris S, Ramnarine IW, Smith HG, Pettersson LB (2010) Picking personalities apart: estimating the influence of predation, sex and body size on boldness in the guppy Poecilia reticulata. Oikos 119:1711–1718. doi:10.1111/j.1600-0706.2010.18028.x
Heinen-Kay JL, Schmidt DA, Stafford AT, Costa MT, Peterson MN, Kern EMA, Langerhans RB (2016) Predicting multifarious behavioural divergence in the wild. Anim Behav 121:3–10. doi:10.1016/j.anbehav.2016.08.016
Jones CM, Braithwaite VA, Healy SD (2003) The evolution of sex differences in spatial ability. Behav Neurosci 117:403–411
Laland KN, Reader SM (1999) Foraging innovation is inversely related to competitive ability in male but not in female guppies. Behav Ecol 10:270–274. doi:10.1093/beheco/10.3.270
Laland KN, Williams K (1997) Shoaling generates social learning of foraging information in guppies. Anim Behav 53:1161–1169. doi:10.1006/anbe.1996.0318
Langerhans RB, Layman CA, DeWitt TJ (2005) Male genital size reflects a tradeoff between attracting mates and avoiding predators in two live-bearing fish species. Proc Natl Acad Sci 102:7618–7623. doi:10.1073/pnas.0500935102
Liu Y, Burmeister SS (2017) Sex differences during place learning in the túngara frog. Anim Behav 128:61–67
Lucon-Xiccato T, Bisazza A (2014) Discrimination reversal learning reveals greater female behavioural flexibility in guppies. Biol Lett 10:20140206. doi:10.1098/rsbl.2014.0206
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
Lucon-Xiccato T, Bisazza A (2017a) Individual differences in cognition among teleost fishes. Behav Proc 141:184–195
Lucon-Xiccato T, Bisazza A (2017b) Sex differences in spatial abilities and cognitive flexibility in the guppy. Anim Behav 123:53–60
Lucon-Xiccato T, Dadda M (2016) Guppies show behavioural but not cognitive sex differences in a novel object recognition test. PLoS ONE 11(6):e0156589. doi:10.1371/journal.pone.0156589
Lucon-Xiccato T, Dadda M (2017) Personality and cognition: sociability negatively predicts shoal size discrimination performance in guppies. Front Psychol 8:1118
Lynch KS, Ramsey ME, Cummings ME (2012) The mate choice brain: comparing gene profiles between female choice and male coercive poeciliids. Genes Brain Behav 11:222–229. doi:10.1111/j.1601-183X.2011.00742.x
Magurran AE, Garcia CM (2000) Sex differences in behaviour as an indirect consequence of mating system. J Fish Biol 57:839–857. doi:10.1111/j.1095-8649.2000.tb02196.x
Magurran AE, Nowak MA (1991) Another battle of the sexes: the consequences of sexual asymmetry in mating costs and predation risk in the guppy, Poecilia reticulata. Proc R Soc B 246:31–38. doi:10.1098/rspb.1991.0121
Magurran AE, Seghers BH (1994) Sexual conflict as a consequence of ecology: evidence from guppy, Poecilia reticulata, populations in Trinidad. Proc R Soc B 255:31–36. doi:10.1098/rspb.1994.0005
Mamuneas D, Spence AJ, Manica A, King AJ (2015) Bolder stickleback fish make faster decisions, but they are not less accurate. Behav Ecol 26:91–96. doi:10.1093/beheco/aru160
Maximino C, Marques de Brito T, da Silva Waneza, Batista A, Herculano AM, Morato S, Gouveia A Jr (2010a) Measuring anxiety in zebrafish: a critical review. Behav Brain Res 214:157–171
Maximino C, Marques de Brito T, de Dias CAM, Gouveia A JR, Morato S (2010b) Scototaxis as anxiety-like behavior in fish. Nat Protoc 5:209–216. doi:10.1038/nprot.2009.225
Miletto Petrazzini ME, Bisazza A, Agrillo C, Lucon-Xiccato T (2017) Sex differences in discrimination reversal learning in the guppy. Anim Cogn. doi:10.1007/s/10071-017-1124-4
Morley KI, Montgomery GW (2001) The genetics of cognitive processes: candidate genes in humans and animals. Behav Genet 31:511–531. doi:10.1023/A:1013337209957
Perals D, Griffin AS, Bartomeus I, Sol D (2017) Revisiting the open-field test: what does it really tell us about animal personality. Anim Behav 123:69–79
Pérez-Escudero A, Vicente-Page J, Hinz RC, Arganda S, de Polavieja GG (2014) idTracker: tracking individuals in a group by automatic identification of unmarked animals. Nat Methods 11:743–748. doi:10.1038/nmeth.2994
Pilastro A, Benetton S, Bisazza A (2003) Female aggregation and male competition reduce costs of sexual harassment in the mosquitofish Gambusia holbrooki. Anim Behav 65:1161–1167. doi:10.1006/anbe.2003.2118
Piyapong C, Krause J, Chapman BB, Ramnarine IW, Louca V, Croft DP (2010) Sex matters: a social context to boldness in guppies (Poecilia reticulata). Behav Ecol 21:3–8. doi:10.1093/beheco/arp142
Pruitt JN, Riechert SE (2009) Sex matters: sexually dimorphic fitness consequences of behavioural syndrome. Anim Behav 78:175–181. doi:10.1016/j.anbehav.2009.04.016
Ramsey ME, Vu W, Cummings ME (2014) Testing synaptic plasticity in dynamic mate choice decisions: N-methyl d-aspartate receptor blockade disrupts female preference. Proc Biol Sci 281:20140047. doi:10.1098/rspb.2014.0047
Range F, Bugnyar T, Schlögl C, Kotrschal K (2006) Individual and sex difference in learning ability of ravens. Behav Proc 73:100–106. doi:10.1016/j.beproc.2006.04.002
Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318. doi:10.1111/j.1469-185X.2007.00010.x
Rodriguez CA, Torres A, Mackintosh NJ, Chamizo VD (2010) Sex differences in the strategies bused by rats to solve a navigation task. J Exp Psychol Anim Behav Proc 36:395–401. doi:10.1037/a0017297
Schuett W, Dall SRX (2009) Sex differences, social context and personality in Zebra Finches, Taeniopygia guttata. Anim Behav 77:1041–1050. doi:10.1016/j.anbehav.2008.12.024
Seed A, Seddon E, Greene B, Call J (2012) Chimpanzee ‘folk physics’: bringing failures into focus. Philos Trans R Soc B 367:2743–2752
Seyfarth RM, Cheney DL (2003) The structure of social knowledge in monkeys. In: de Waal F, Tyack P (eds) Animal social complexity: intelligence, culture, and individualized societies. Harvard University Press, Cambridge, MA, pp 207–229
Sih A, Giudice MD (2012) Linking behavioural syndromes and cognition: a behavioural ecology perspective. Philos Trans R Soc B 367:2762–2772. doi:10.1098/rstb.2012.0216
Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378. doi:10.1016/j.tree.2004.04.009
Spence R, Magurran AE, Smith C (2011) Spatial cognition in zebrafish: the role of strain and rearing environment. Anim Cogn 14:607–612. doi:10.1007/s10071-011-0391-8
Stevens JR, Wood JN, Hauser MD (2007) When quantity trumps number: discrimination experiments in cotton-top tamarins (Saguinus oedipus) and common marmosets (Callithrix jacchus). Anim Cogn 10:429–437. doi:10.1007/s10071-007-0081-8
Thornton A, Lukas D (2012) Individual variation in cognitive performance: developmental and evolutionary perspectives. Philos Trans R Soc B 367:2773–2783. doi:10.1098/rstb.2012.0214
Titulaer M, Van Oers K, Haguib M (2012) Personality affects learning performance in difficult tasks in a sex-dependent way. Anim Behav 83:723–730. doi:10.1016/j.anbehav.2011.12.020
Walsh RN, Cummins RA (1976) The open-field test: a critical review. Psychol Bull 83(3):482–504
Wang SM, Ramsey ME, Cummings ME (2014) Plasticity of the mate choice mind: courtship evokes choice-like brain responses in females from a coercive mating system. Genes Brain Behav 13:365–375. doi:10.1111/gbb.12124
Acknowledgements
The authors would like to thank the many undergraduates who assisted in this project including Rachel Ellerd, Patricia Phillips, Omar Mohammad, Chris Monty, Matt Milam, and Ashton Berger; and the very helpful comments and assistance from all Cummings’ laboratory members.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
This research was conducted without any external financial support.
Conflict of interest
The authors declare that they have no conflict of interests.
Ethical approval
The authors certify that this work followed ethical treatment of animals outlined in their IACUC protocol (AUP-2016-00246).
Electronic supplementary material
Below is the link to the electronic supplementary material.
Figure S1
Behavioural consistency measured as correlations across (a) learning assays, (b) activity, (c), anxiety behaviour—thigmoatixs black and latency to enter white side, (d) sociality, (e) thigmotaxis behaviour, (f) exploritory behaviour—thigmotaxis white and scototaxis (PDF 2584 kb)
Figure S2
Generalised canonical discrimination plot for all behavioural assays. Entries into white (DFA1: r = 0.27, p = 0.27), scototaxis (DFA1: r = 0.03, p = 0.91), thigmotaxis numerosity (DFA1: r = 0.17, p = 0.48), thigmotaxis black(DFA1: r = 0.35, p = 0.13), thigmotaxis white (DFA1: r = 0.15, p = 0.53), latency to enter white side (DFA1: r = 0.32, p = 0.18), sociality (DFA1: r = 0.86, p = 2.03e−06), activity (DFA1: r = 0.17, p = 0.47). DFA1 axis showed a nonsignificant correlation with learning performance (r = 0.26, p = 0.28) (PDF 2212 kb)
Rights and permissions
About this article
Cite this article
Etheredge, R.I., Avenas, C., Armstrong, M.J. et al. Sex-specific cognitive–behavioural profiles emerging from individual variation in numerosity discrimination in Gambusia affinis . Anim Cogn 21, 37–53 (2018). https://doi.org/10.1007/s10071-017-1134-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-017-1134-2