Animal Cognition

, Volume 20, Issue 1, pp 117–125 | Cite as

The effects of incubation temperature on the development of the cortical forebrain in a lizard

Original Paper
Part of the following topical collections:
  1. Animal cognition in a human-dominated world

Abstract

The embryos of egg-laying species are exposed to variable thermal regimes, which can influence not only the resultant hatchling’s morphology (e.g., size, sex) and performance (e.g., locomotor speed), but also its cognitive performance (learning ability). To clarify the proximate basis for this latter effect, we incubated eggs of the scincid lizard Bassiana duperreyi under simulated ‘hot’ and ‘cold’ natural nest temperatures to examine the effect of incubation temperature on the structure of the telencephalon region of the forebrain. Hatchlings from low-temperature incubation had larger telencephalons (both in absolute terms and relative to body size) and larger neurons in their medial cortices, whereas the medial cortices of hatchlings from high-temperature incubation had fewer neurons overall, but greater neuronal density, and more neurons in certain areas. These temperature-induced differences in B. duperreyi forebrain development are consistent with (and may explain) the disparities in learning ability between hatchlings from our two incubation treatments. The phenotypic plasticity of lizard telencephalon anatomy in response to incubation temperature presents exciting opportunities for studies on the evolutionary and developmental determinants of intelligence in vertebrates, but also offers a cautionary tale. Global climate changes, wrought by anthropogenic activities, may directly modify brain structure in reptiles.

Keywords

Cognition Brain anatomy Functional anatomy Learning ability Squamate reptile 

References

  1. Amiel JJ, Shine R (2012) Hotter nests produce smarter young lizards. Biol Lett 8:372–374CrossRefPubMedPubMedCentralGoogle Scholar
  2. Amiel JJ, Tingley R, Shine R (2011) Smart moves: effects of relative brain size on establishment success of invasive amphibians and reptiles. PLoS One 6:e18277CrossRefPubMedPubMedCentralGoogle Scholar
  3. Amiel JJ, Lindström T, Shine R (2014) Egg-incubation effects generate positive correlations between size, speed and learning ability in young lizards. Anim Cogn 17:337–347CrossRefPubMedGoogle Scholar
  4. Butler AB (1980) Cytoarchitectonic and connectional organization of the lacertilian telencephalon with comments on vertebrate forebrain evolution. In: Ebbesson SOE (ed) Comparative neurology of the telencephalon. Plenum Press, New York, pp 297–329CrossRefGoogle Scholar
  5. Chittka L, Niven J (2009) Are bigger brains better? Curr Biol 19:R995–R1008CrossRefPubMedGoogle Scholar
  6. Clark BF, Noble DWA, Whiting MJ, Amiel JJ, Shine R (2014) Colour discrimination and associative learning in hatchling lizards incubated at ‘hot’ and ‘cold’ temperatures. Behav Ecol Sociobiol 68:239–247CrossRefGoogle Scholar
  7. Coomber P, Crews D, Gonzalez-Lima F (1997) Independent effects of incubation temperature and gonadal sex on the volume and metabolic capacity of brain nuclei in the leopard gecko (Eublepharis macularius), a lizard with temperature-dependent sex determination. J Comp Neurol 380:409–421CrossRefPubMedGoogle Scholar
  8. Crews D, Coomber P, Gonzalez-Lima F (1997) Effects of age and sociosexual experience on the morphology and metabolic capacity of brain nuclei in the leopard gecko (Eublepharis macularius), a lizard with temperature-dependent sex determination. Brain Res 758:169–179CrossRefPubMedGoogle Scholar
  9. Day LB, Crews D, Wilczynski W (1999a) Relative medial and dorsal cortex volume in relation to foraging ecology in congeneric lizards. Brain Behav Evol 54:314–322Google Scholar
  10. Day LB, Crews D, Wilczynski W (1999b) Spatial and reversal learning in congeneric lizards with different foraging strategies. Anim Behav 57:393–407CrossRefPubMedGoogle Scholar
  11. Day LB, Crews D, Wilczynski W (2001) Effects of medial and dorsal cortex lesions on spatial memory in lizards. Behav Brain Res 118:27–42CrossRefPubMedGoogle Scholar
  12. Deeming D (2004) Post-hatching phenotypic effects of incubation in reptiles. In: Deeming D (ed) Reptilian incubation: environment, evolution and behaviour. Nottingham University Press, Nottingham, pp 229–251Google Scholar
  13. Elphick MJ, Shine R (1998) Longterm effects of incubation temperatures on the morphology and locomotor performance of hatchling lizards (Bassiana duperreyi, Scincidae). Biol J Linn Soc 63:429–447CrossRefGoogle Scholar
  14. Harlow PS (1996) A harmless technique for sexing hatchling lizards. Herpetol Rev 27:71–72Google Scholar
  15. Hayashi A, Nagaoka M, Yamada K, Ichitani Y, Miake Y, Okado N (1998) Maternal stress induces synaptic loss and developmental disabilities of offspring. Int J Dev Neurosci 16:209–216CrossRefPubMedGoogle Scholar
  16. Healy SD, Rowe C (2007) A critique of comparative studies of brain size. Proc Roy Soc London B 274:453–464CrossRefGoogle Scholar
  17. Herculano-Houzel S, Manger PR, Kaas JH (2014) Brain scaling in mammalian evolution as a consequence of concerted and mosaic changes in numbers of neurons and average neuronal cell size. Front Neuroanat 8:1–28Google Scholar
  18. 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 79:144–154CrossRefPubMedGoogle Scholar
  19. Jerison HJ, Barlow HB (1985) Animal intelligence as encephalization. Philos Trans R Soc B 308:21–35CrossRefGoogle Scholar
  20. Lefebvre L, Reader SM, Sol D (2004) Brains, innovations and evolution in birds and primates. Brain Behav Evol 63:233–246CrossRefPubMedGoogle Scholar
  21. Lemaire V, Koehl M, Le Moal M, Abrous D (2000) Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 97:11032–11037CrossRefPubMedPubMedCentralGoogle Scholar
  22. López J, Vargas J, Gómez Y, Salas C (2003) Spatial and non-spatial learning in turtles: the role of medial cortex. Behav Brain Res 143:109–120CrossRefPubMedGoogle Scholar
  23. Luders E, Narr KL, Thompson PM, Toga AW (2009) Neuroanatomical correlates of intelligence. Intelligence 37:156–163CrossRefPubMedPubMedCentralGoogle Scholar
  24. Mader D (2006) Euthanasia. In: Mader D (ed) Reptile medicine and surgery, 2nd edn. Saunders Elsevier, St Louis, pp 564–568CrossRefGoogle Scholar
  25. Morgane PJ, Mokler DJ, Galler JR (2002) Effects of prenatal protein malnutrition on the hippocampal formation. Neurosci Biobehav Rev 26:471–483CrossRefPubMedGoogle Scholar
  26. Mouton PR (2011) Unbiased stereology: a concise guide. Johns Hopkins University Press, BaltimoreGoogle Scholar
  27. Northcutt RG (1978) Forebrain and midbrain organization in lizards and its phylogenetic significance. In: Greenberg N, MacLean PD (eds) Behaviour and neurology of lizards: an interdisciplinary colloquium. National Institute of Mental Health, Maryland, pp 11–64Google Scholar
  28. Pfefferbaum A, Mathalon DH, Sullivan EV, Rawles JM, Zipursky RB, Lim KO (1994) A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. Arch Neurol 51:874–887CrossRefPubMedGoogle Scholar
  29. Purves D, Lichtman JW (1985) Principles of neural development. Sinauer, SunderlandGoogle Scholar
  30. Roth ED, Lutterschmidt WI, Wilson DA (2006) Relative medial and dorsal cortex volume in relation to sex differences in spatial ecology of a snake population. Brain Behav Evol 67:103–110CrossRefPubMedGoogle Scholar
  31. Sakata JT, Coomber P, Gonzalez-Lima F, Crews D (2000) Functional connectivity among limbic brain areas: differential effects of incubation temperature and gonadal sex in the leopard gecko, Eublepharis macularius. Brain Behav Evol 55:139–151CrossRefPubMedGoogle Scholar
  32. Shine R, Harlow PS (1996) Maternal manipulation of offspring phenotypes via nest-site selection in an oviparous lizard. Ecology 77:1808–1817CrossRefGoogle Scholar
  33. Telemeco RS, Elphick MJ, Shine R (2009) Nesting lizards (Bassiana duperreyi) compensate partly, but not completely, for climate change. Ecology 90:17–22CrossRefPubMedGoogle Scholar
  34. West MJ (2012) Basic stereology for biologists and neuroscientists. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  35. White S, O’Reilly H, Frith U (2009) Big heads, small details and autism. Neuropsychologia 47:1274–1281CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.School of Life and Environmental SciencesUniversity of SydneySydneyAustralia
  2. 2.Discipline of Pathology, Bosch InstituteUniversity of SydneySydneyAustralia

Personalised recommendations