Spatial learning in captive and wild-born lizards: heritability and environmental effects

Abstract

Animals raised in captivity go through drastically different life experiences compared with those raised in the wild. The captive environment is usually characterised by highly stable conditions and limited social interactions. Such early developmental environment, alone and interacting with genes, can have long-lasting effects on cognitive performance. By testing pairs of mothers and offspring delicate skinks, Lampropholis delicata, we investigated how being raised in a captive environment shapes spatial learning. Additionally, with this design, we were able to evaluate the additive genetic component and strength of genetic effects in this lizard species. Using a Y-maze task, we compared the spatial learning abilities of wild-caught adult female (mothers) delicate skinks, to their captive-born and raised sexually mature offspring. We found that more mothers completed the task and showed shorter latencies compared with offspring who took longer to complete the maze. The offspring performance did not appear to correlate with their mothers’ performance, indicating little narrow-sense heritability. Furthermore, offspring performance was neither affected nor predicted by their mothers’ performance, indicating a limited overall genetic effect. Our results suggest that early life experiences in a captive environment may have a hindering effect on cognitive performance.

Significance statement

How important are environmental effects compared with genetics on the development of learning abilities in non-human animals? Studying mother-offspring skink pairs, we show that wild-born mothers outperformed their captive-born offspring in a spatial learning task. We further show that offspring performance in the task was neither explained nor predicted by their mothers’ performance. We suggest that conditions during early-life stages shape spatial learning more than genetics, and stable captive conditions may have a negative effect on the development of spatial learning.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Amiel JJ, Shine R (2012) Hotter nests produce smarter young lizards. Biol Lett 8:372–374. https://doi.org/10.1098/rsbl.2011.1161

    Article  PubMed  PubMed Central  Google Scholar 

  2. Batabyal A, Thaker M (2019) Lizards from suburban areas learn faster to stay safe. Biol Lett 15:20190009. https://doi.org/10.1098/rsbl.2019.0009

    Article  PubMed  PubMed Central  Google Scholar 

  3. Berger-Tal O, Nathan J, Meron E, Saltz D (2014) The exploration-exploitation dilemma: a multidisciplinary framework. PLoS One 9:e95693. https://doi.org/10.1371/journal.pone.0095693

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. Boogert NJ, Fawcett TW, Lefebvre L (2011) Mate choice for cognitive traits: a review of the evidence in nonhuman vertebrates. Behav Ecol 22:447–459. https://doi.org/10.1093/beheco/arq173

    Article  Google Scholar 

  5. Boogert NJ, Madden JR, Morand-Ferron J, Thornton A (2018) Measuring and understanding individual differences in cognition. Philos Trans R Soc B 373:20170280. https://doi.org/10.1098/rstb.2017.0280

    Article  Google Scholar 

  6. Bronson G (1965) The hierarchical organization of TAME categories. Behav Sci 10:7–25

    CAS  Article  Google Scholar 

  7. Buchanan KL, Grindstaff JL, Pravosudov VV (2013) Condition dependence, developmental plasticity, and cognition: implications for ecology and evolution. Trends Ecol Evol 28:290–296. https://doi.org/10.1016/j.tree.2013.02.004

    Article  PubMed  PubMed Central  Google Scholar 

  8. Burghardt GM (1977) Learning processes in reptiles. In: Gans C, Tinkle DW (ed) Biology of the Reptilia: ecology and behaviour A (Vol 7), Academic Press

  9. Cacioppo JT, Hawkley LC (2009) Perceived social isolation and cognition. Trends Cogn Sci 13:447–454. https://doi.org/10.1016/j.tics.2009.06.005

    Article  PubMed  PubMed Central  Google Scholar 

  10. Carazo P, Noble DWA, Chandrasoma D, Whiting MJ (2014) Sex and boldness explain individual differences in spatial learning in a lizard sex and boldness explain individual differences in spatial learning in a lizard. Proc R Soc B 281:20133275. https://doi.org/10.1098/rspb.2013.3275

    Article  PubMed  Google Scholar 

  11. Carere C, Locurto C (2011) Interaction between animal personality and animal cognition. Curr Zool 57:491–498. https://doi.org/10.1093/czoolo/57.4.491

    Article  Google Scholar 

  12. Cauchoix M, Hermer E, Chaine AS, Morand-Ferron J (2017) Cognition in the field: comparison of reversal learning performance in captive and wild passerines. Sci Rep 7:12945. https://doi.org/10.1038/s41598-017-13179-5

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Chapple DG, Simmonds SM, Wong BBM (2011) Know when to run, know when to hide: can behavioral differences explain the divergent invasion success of two sympatric lizards? Ecol Evol 1:278–289. https://doi.org/10.1002/ece3.22

    Article  PubMed  PubMed Central  Google Scholar 

  14. Chapple DG, Miller KA, Kraus F, Thompson MB (2013) Divergent introduction histories among invasive populations of the delicate skink (Lampropholis delicata): has the importance of genetic admixture in the success of biological invasions been overemphasized? Divers Distrib 19:134–146. https://doi.org/10.1111/j.1472-4642.2012.00919.x

    Article  Google Scholar 

  15. Chung M, Goulet CT, Michelangeli M, Melki-Wegner B, Wong BB, Chapple DG (2017) Does personality influence learning? A case study in an invasive lizard. Oecologia 185:641–651. https://doi.org/10.1007/s00442-017-3975-4

    Article  PubMed  Google Scholar 

  16. Coss RG (1991) Context and animal behavior III: the relationship between early development and evolutionary persistence of ground squirrel antisnake behavior. J Ecol Psychol 3:277–315

    Article  Google Scholar 

  17. Croston R, Branch CL, Kozlovsky DY, Dukas R, Pravosudov VV (2015) Heritability and the evolution of cognitive traits. Behav Ecol 26:1447–1459. https://doi.org/10.1093/beheco/arv088

    Article  Google Scholar 

  18. Davis EP, Stout SA, Molet J, Vegetabile B, Glynn LM, Sandman CA, Heins K, Stern H, Baram TZ (2017) Exposure to unpredictable maternal sensory signals influences cognitive development across species. Proc Natl Acad Sci U S A 114:10390–10395. https://doi.org/10.1073/pnas.1703444114

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. Dayananda B, Webb JK (2017) Incubation under climate warming affects learning ability and survival in hatchling lizards. Biol Lett 13:20170002. https://doi.org/10.1098/rsbl.2017.0002

    Article  PubMed  PubMed Central  Google Scholar 

  20. Deary IJ, Johnson W, Houlihan LM (2009) Genetic foundations of human intelligence. Hum Genet 126:215–232. https://doi.org/10.1007/s00439-009-0655-4

    Article  PubMed  Google Scholar 

  21. Dukas R (2004) Evolutionary biology of animal cognition. Annu Rev Ecol Evol 35:347–374. https://doi.org/10.1146/annurev.ecolsys.35.112202.130152

    Article  Google Scholar 

  22. Dukas R (2008) Evolutionary biology of insect learning. Annu Rev Entomol 53:145–160. https://doi.org/10.1146/annurev.ento.53.103106.093343

    CAS  Article  PubMed  Google Scholar 

  23. Feldman R, Eidelman AI (2009) Biological and environmental initial conditions shape the trajectories of cognitive and social-emotional development across the first years of life. Dev Sci 12:194–200. https://doi.org/10.1111/j.1467-7687.2008.00761.x

    Article  PubMed  Google Scholar 

  24. Forsman A, Shine R (1995a) Parallel geographic variation in body shape and reproductive life history within the Australian scincid lizard Lampropholis delicata. Funct Ecol 9:818–828

    Article  Google Scholar 

  25. Forsman A, Shine R (1995b) The adaptative significance of colour pattern polymophism in the Australian scincid lizard Lampropholis delicata. Biol J Linn Soc 55:291–373

    Article  Google Scholar 

  26. Freas CA, LaDage LD, Roth TC, Pravosudov VV (2012) Elevation-related differences in memory and the hippocampus in mountain chickadees, Poecile gambeli. Anim Behav 84:121–127. https://doi.org/10.1016/j.anbehav.2012.04.018

    Article  Google Scholar 

  27. Fumagalli F, Molteni R, Racagni G, Riva MA (2007) Stress during development: impact on neuroplasticity and relevance to psychopathology. Prog Neurobiol 81:197–217. https://doi.org/10.1016/j.pneurobio.2007.01.002

    Article  PubMed  Google Scholar 

  28. Geary DC (1995) Sexual selection and sex differences in spatial cognition. Learn Individ Differ 7:289–301. https://doi.org/10.1016/1041-6080(95)90003-9

    Article  Google Scholar 

  29. Goulet CT, Michelangeli M, Chung M, Riley JL, Wong BB, Thompson MB, Chapple DG (2018) Evaluating cognition and thermal physiology as components of the pace-of-life syndrome. Evol Ecol 32:469–488. https://doi.org/10.1007/s10682-018-9948-1

    Article  Google Scholar 

  30. Hedges DW, Woon FL (2011) Early-life stress and cognitive outcome. Psychopharmacology 214:121–130. https://doi.org/10.1007/s00213-010-2090-6

    CAS  Article  PubMed  Google Scholar 

  31. Holding ML, Frazier JA, Taylor EN, Strand CR (2012) Experimentally altered navigational demands induce changes in the cortical forebrain of free-ranging northern pacific rattlesnakes (Crotalus o. oreganus). Brain Behav Evol 79:144–154. https://doi.org/10.1159/000335034

    Article  PubMed  Google Scholar 

  32. Holtzman DA, Harris TW, Aranguren G, Bostock E (1999) Spatial learning of an escape task by young corn snakes, Elaphe guttata guttata. Anim Behav 57:51–60. https://doi.org/10.1006/anbe.1998.0971

    CAS  Article  PubMed  Google Scholar 

  33. Hopkins WD, Russell JL, Schaeffer J (2014) Chimpanzee intelligence is heritable. Curr Biol 24:1649–1652. https://doi.org/10.1016/j.cub.2014.05.076

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Jones CM, Braithwaite VA, Healy SD (2003) The evolution of sex differences in spatial ability. Behav Neurosci 117:403–411. https://doi.org/10.1037/0735-7044.117.3.403

    Article  PubMed  Google Scholar 

  35. Joss JMP, Minard JA (1985) On the reproductive cycles of Lampropholis guichenoti and L. delicata (Squamata:Scincidae) in the Sydney region. Aust J Zool 33:625–640. https://doi.org/10.1071/ZO9850699

    Article  Google Scholar 

  36. Kang F, Goulet CT, Chapple DG (2018) The impact of urbanization on learning ability in an invasive lizard. Biol J Linn Soc 123:55–62. https://doi.org/10.1093/biolinnean/blx131

    Article  Google Scholar 

  37. Kotrschal A, Taborsky B (2010) Environmental change enhances cognitive abilities in fish. PLoS Biol 8:e1000351. https://doi.org/10.1371/journal.pbio.1000351

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. Light KR, Kolata S, Wass C, Denman-Brice A, Zagalsky R, Matzel LD (2010) Working memory training promotes general cognitive abilities in genetically heterogeneous mice. Curr Biol 20:777–782. https://doi.org/10.1016/j.cub.2010.02.034

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. MacDougall-Shackleton SA, Spencer KA (2012) Developmental stress and birdsong: current evidence and future directions. J Ornithol 153:105–117. https://doi.org/10.1007/s10336-011-0807-x

    Article  Google Scholar 

  40. Matsubara S, Deeming DC, Wilkinson A (2017) Cold-blooded cognition: new directions in reptile cognition. Curr Opin Behav Sci 16:126–130. https://doi.org/10.1016/j.cobeha.2017.06.006

    Article  Google Scholar 

  41. McCune KB, Jablonski P, Lee S, Ha RR (2019) Captive jays exhibit reduced problem-solving performance compared to wild conspecifics. R Soc Open Sci 6:181311. https://doi.org/10.1098/rsos.181311

    Article  PubMed  PubMed Central  Google Scholar 

  42. Michelangeli M, Chapple DG, Wong BBM (2016) Are behavioural syndromes sex specific? Personality in a widespread lizard species. Behav Ecol Sociobiol 70:1911–1919. https://doi.org/10.1007/s00265-016-2197-9

    Article  Google Scholar 

  43. Miller KA, Duran A, Melville J, Thompson MB, Chapple DG (2017) Sex-specific shifts in morphology and colour pattern polymorphism during range expansion of an invasive lizard. J Biogeogr 44:2778–2788. https://doi.org/10.1111/jbi.13075

    Article  Google Scholar 

  44. Morand-Ferron J, Cole EF, Quinn JL (2016) Studying the evolutionary ecology of cognition in the wild: a review of practical and conceptual challenges. Biol Rev 91:367–389. https://doi.org/10.1111/brv.12174

    Article  PubMed  Google Scholar 

  45. Moule H, Michelangeli M, Thompson MB, Chapple DG (2016) The influence of urbanization on the behaviour of an Australian lizard and the presence of an activity-exploratory behavioural syndrome. J Zool 298:103–111. https://doi.org/10.1111/jzo.12288

    Article  Google Scholar 

  46. Noble DWA, Byrne RW, Whiting MJ (2014) Age-dependent social learning in a lizard. Biol Lett 10:420140430. https://doi.org/10.1098/rsbl.2014.0430

    Article  Google Scholar 

  47. Orr MV, Hittel K, Lukowiak K (2008) Comparing memory-forming capabilities between laboratory-reared and wild Lymnaea: learning in the wild, a heritable component of snail memory. J Exp Biol 211:2807–2816. https://doi.org/10.1242/jeb.020172

    Article  PubMed  Google Scholar 

  48. Parker KJ, Buckmaster CL, Justus KR, Schatzberg AF, Lyons DM (2005) Mild early life stress enhances prefrontal-dependent response inhibition in monkeys. Biol Psychiatry 57:848–855. https://doi.org/10.1016/j.biopsych.2004.12.024

    Article  PubMed  Google Scholar 

  49. Paulissen MA (2008) Spatial learning in the little brown skink, Scincella lateralis: the importance of experience. Anim Behav 76:135–141. https://doi.org/10.1016/j.anbehav.2007.12.017

    Article  Google Scholar 

  50. Pollen AA, Dobberfuhl AP, Scace J, Igulu MM, Renn SC, Shumway CA, Hofmann HA (2007) Environmental complexity and social organization sculpt the brain in Lake Tanganyikan cichlid fish. Brain Behav Evol 70:21–39. https://doi.org/10.1159/000101067

    Article  PubMed  Google Scholar 

  51. Pravosudov VV (2003) Long-term moderate elevation of corticosterone facilitates avian food-caching behaviour and enhances spatial memory. Proc R Soc Lond B 270:2599–2604. https://doi.org/10.1098/rspb.2003.2551

    CAS  Article  Google Scholar 

  52. Riley JL, Noble DWA, Byrne RW, Whiting MJ (2017) Does social environment influence learning ability in a family-living lizard? Anim Cogn 20:449–458. https://doi.org/10.1007/s10071-016-1068-0

    Article  PubMed  Google Scholar 

  53. Roth TC, Krochmal AR (2015) The role of age-specific learning and experience for turtles navigating a changing landscape. Curr Biol 25:333–337. https://doi.org/10.1016/j.cub.2014.11.048

    CAS  Article  PubMed  Google Scholar 

  54. Roth TC, LaDage LD, Pravosudov VV (2010) Learning capabilities enhanced in harsh environments: a common garden approach. Proc R Soc Lond B 277:3187–3193. https://doi.org/10.1098/rspb.2010.0630

    Article  Google Scholar 

  55. Sale A, Berardi N, Maffei L (2009) Enrich the environment to empower the brain. Trends Neurosci 32:233–239. https://doi.org/10.1016/j.tins.2008.12.004

    CAS  Article  PubMed  Google Scholar 

  56. Salvanes AG, Moberg O, Ebbesson LO, Nilsen TO, Jensen KH, Braithwaite VA (2013) Environmental enrichment promotes neural plasticity and cognitive ability in fish. Proc R Soc B 280:20131331. https://doi.org/10.1098/rspb.2013.1331

    Article  PubMed  Google Scholar 

  57. Sameroff A (2010) A unified theory of development: a dialectic integration of nature and nurture. Child Dev 81:6–22

    Article  Google Scholar 

  58. Shaw RC (2017) Testing cognition in the wild: factors affecting performance and individual consistency in two measures of avian cognition. Behav Process 134:31–36. https://doi.org/10.1016/j.beproc.2016.06.004

    Article  Google Scholar 

  59. Shettleworth SJ (2010) Cognition, evolution, and behavior. Oxford university press

  60. Smith C, Philips A, Reichard M (2015) Cognitive ability is heritable and predicts the success of an alternative mating tactic. Proc R Soc B 282:20151046. https://doi.org/10.1098/rspb.2015.1046

    Article  PubMed  Google Scholar 

  61. Sorato E, Zidar J, Garnham L, Wilson A, Løvlie H (2018) Heritabilities and co-variation among cognitive traits in red junglefowl. Philos Trans R Soc B 373:20170285. https://doi.org/10.1098/rstb.2017.0285

    Article  Google Scholar 

  62. Szabo B, Noble DW, Byrne RW, Tait DS, Whiting MJ (2019) Precocial juvenile lizards show adult level learning and behavioural flexibility. Anim Behav 154:75–84. https://doi.org/10.1016/j.anbehav.2019.06.003

    Article  Google Scholar 

  63. Tebbich S, Stereln K, Teschke I (2010) The tale of the finch: adaptive radiation and behavioural flexibility. Philos Trans R Soc B 365:1099–1109. https://doi.org/10.1098/rstb.2009.0291

    Article  Google Scholar 

  64. Thornton A, Lukas D (2012) Individual variation in cognitive performance: developmental and evolutionary perspectives. Philos Trans R Soc B 367:2773–2783. https://doi.org/10.1098/rstb.2012.0214

    Article  Google Scholar 

  65. Tierney AL, Nelson III CA (2009) Brain development and the role of experience in the early years. Zero three 30(2):9–13

  66. Tromborg CT, Coss RG (2015) Isolation rearing reveals latent antisnake behavior in California ground squirrels (Otospermophilus becheeyi) searching for predatory threats. Anim Cogn 18:855–865. https://doi.org/10.1007/s10071-015-0853-5

    Article  PubMed  Google Scholar 

  67. Valenzuela N, Lance V (2004) Temperature-dependent sex determination in vertebrates. Washington, DC: Smithsonian Institution

  68. Volkers KM, Scherder EJA (2011) Impoverished environment, cognition, aging and dementia. Rev Neurosci 22:259–266. https://doi.org/10.1515/RNS.2011.026

    Article  PubMed  Google Scholar 

  69. Wiggins WD, Bounds S, Wilder SM (2018) Laboratory-reared and field-collected predators respond differently to same experimental treatments. Behav Ecol Sociobiol. 72:19. https://doi.org/10.1007/s00265-017-2437-7

  70. Wilkinson A, Huber L (2012) Cold-blooded cognition: reptilian cognitive abilities. In: Shackelford TK, Vonk J (eds) Oxford handbook of comparative evolutionary psychology. Oxford University Press, Oxford, pp 129–143. https://doi.org/10.1093/oxfordhb/9780199738182.013.0008

    Google Scholar 

  71. Wilson S, Swan G (2010) A complete guide to reptiles of Australia. 3rd ed. Reed New Holland, Sydney

  72. Wongwitdecha N, Marsden CA (1996) Effects of social isolation rearing on learning in the Morris water maze. Brain Res 715:119–124. https://doi.org/10.1016/0006-8993(95)01578-7

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Felix Zajitschek for help in the field. We would like to thank Alison L. Greggor for insightful comments on the manuscript and Uri Roll for fruitful discussion and assistance in the analysis. We would also like to thank two anonymous reviewers whose comments greatly improved the manuscript.

Funding

This work was supported by a Ben-Gurion University-Monash University seed grant. This is publication number 1057 of the Mitrani Department of Desert Ecology.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Reut Vardi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All animal care and experimental procedures were approved by the Monash University Animal Ethics Committee (BSCI/2016/17, BSCI/2017/33). All applicable international, national, and/or institutional guidelines for the use of animals were followed.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by S. Joy Downes

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Vardi, R., Goulet, C.T., Matthews, G. et al. Spatial learning in captive and wild-born lizards: heritability and environmental effects. Behav Ecol Sociobiol 74, 23 (2020). https://doi.org/10.1007/s00265-020-2805-6

Download citation

Keywords

  • Cognition
  • Delicate skink
  • Genetic effects
  • Nature-nurture
  • Rearing environment
  • Y-maze