Brain, Behavior and Evolution
Jude M.B.a,b· Strand C.R. aaDepartment of Biological Sciences, California Polytechnic State University, San Luis Obispo, CA, USA
bSchool of Medicine, University of California Davis Medical Center, Sacramento, CA, USA
Log in to MyKarger to check if you already have access to this content.
Buy FullText & PDF Unlimited re-access via MyKarger Unrestricted printing, no saving restrictions for personal use read more
CHF 38.00 *
EUR 35.00 *
USD 39.00 *
Buy a Karger Article Bundle (KAB) and profit from a discount!
If you would like to redeem your KAB credit, please log in.
Save over 20% compared to the individual article price. Rent via DeepDyve Unlimited fulltext viewing of this article Organize, annotate and mark up articles Printing and downloading restrictions apply Subscribe Access to all articles of the subscribed year(s) guaranteed for 5 years Unlimited re-access via Subscriber Login or MyKarger Unrestricted printing, no saving restrictions for personal use read more Select* The final prices may differ from the prices shown due to specifics of VAT rules.
Article / Publication Details
Received: March 23, 2022
Accepted: February 06, 2023
Published online: February 16, 2023
Number of Print Pages: 10
Number of Figures: 2
Number of Tables: 0
ISSN: 0006-8977 (Print)
eISSN: 1421-9743 (Online)
For additional information: https://www.karger.com/BBE
AbstractThe hippocampus plays an important role in spatial navigation and spatial learning across a variety of vertebrate species. Sex and seasonal differences in space use and behavior are known to affect hippocampal volume. Similarly, territoriality and differences in home range size are known to affect the volume of the reptile hippocampal homologues, the medial and dorsal cortices (MC, DC). However, studies have almost exclusively investigated males and little is known about sex or seasonal differences in MC and/or DC volumes in lizards. Here, we are the first to simultaneously examine sex and seasonal differences in MC and DC volumes in a wild lizard population. In Sceloporus occidentalis, males display territorial behaviors that are more pronounced during the breeding season. Given this sex difference in behavioral ecology, we expected males to have larger MC and/or DC volumes than females and for this difference to be most pronounced during the breeding season when territorial behavior is increased. Male and female S. occidentalis were captured from the wild during the breeding season and the post-breeding season and were sacrificed within 2 days of capture. Brains were collected and processed for histology. Cresyl-violet-stained sections were used to quantify brain region volumes. In these lizards, breeding females had larger DC volumes than breeding males and nonbreeding females. There was no sex or seasonal difference in MC volumes. Differences in spatial navigation in these lizards may involve aspects of spatial memory related to breeding other than territoriality that affect plasticity of the DC. This study highlights the importance of investigating sex differences and including females in studies of spatial ecology and neuroplasticity.
© 2023 S. Karger AG, Basel
References Angilletta MJ, Jr, Sears MW, Pringle RM. Spatial dynamics of nesting behavior: lizards shift microhabitats to construct nests with beneficial thermal properties. Ecology. 2009;90(10):2933–9. Araya-Salas M, Gonzalez-Gomez P, Wojczulanis-Jakubas K, López V3rd, Wright TF. Spatial memory is as important as weapon and body size for territorial ownership in a lekking hummingbird. Sci Rep. 2018 Jan 31;8(1):2001. Avigan MR, Powers AS. The effects of MK-801 injections and dorsal cortex lesions on maze learning in turtles (Chrysemys picta). Psychobiology. 1995 Mar;23(1):63–8. Beuchat CA. Temperature effects during gestation in a viviparous lizard. J Therm Biol. 1988;13(3):135–42. Biegler R, McGregor A, Krebs JR, Healy SD. A larger hippocampus is associated with longer-lasting spatial memory. Proc Natl Acad Sci U S A. 2001;98(12):6941–4. Bruce LL, Butler AB. Telencephalic connections in lizards. I. Projections to cortex. J Comp Neurol. 1984;229(4):585–601. Burger J, Zappalorti RT. Effects of incubation temperature on sex ratios in pine snakes: differential vulnerability of males and females. Am Naturalist. 1988;132(4):492–505. Burger J, Zappalorti RT, Gochfeld M. Developmental effects of incubation temperature on hatchling pine snakes Pituophis melanoleucus. Comp Biochem Physiol. 1987;87(3):727–32. Butler AB, Hodos W. Comparative vertebrate neuroanatomy: evolution and adaptationJohn Wiley & Sons; 2005. Calisi RM, Chintamen S, Ennin E, Kriegsfeld L, Rosenblum EB. Neuroanatomical changes related to a changing environment in lesser earless lizards. J Herpetology. 2017;51(2):258–62. Carazo P, Noble DW, Chandrasoma D, Whiting MJ. Sex and boldness explain individual differences in spatial learning in a lizard. Proc R Soc B. 2014 May 7;281(1782):20133275. Clayton NS, Reboreda JC, Kacelnik A. Seasonal changes of hippocampus volume in parasitic cowbirds. Behav Process. 1997;41(3):237–43. Clint EK, Sober E, Garland TJr, Rhodes JS. Male superiority in spatial navigation: adaptation or side effect?Q Rev Biol. 2012;87(4):289–313. Crusio WE, Schwegler H. Hippocampal mossy fiber distribution covaries with open-field habituation in the mouse. Behav Brain Res. 1987;26(2-3):153–8. Davis J. The times of mating and oviposition of the Western fence lizard, Sceloporus occidentalis occidentalis. J Herpetology. 1980;14(1):102–2. Davis J, Ford RG. Home range in the Western fence lizard (Sceloporus occidentalis occidentalis). Copeia. 1983;1983(4):933–40. Baird Day L, Crews D, Wilczynski W. Relative medial and dorsal cortex volume in relation to foraging ecology in congeneric lizards. Brain Behav Evol. 1999;54(6):314–22. Day LB, Crews D, Wilczynski W. Effects of medial and dorsal cortex lesions on spatial memory in lizards. Behav Brain Res. 2001;118(1):27–42. Day LB, Guerra M, Schlinger BA, Rothstein SI. Sex differences in the effects of captivity on hippocampus size in brown-headed cowbirds (Molothrus ater obscurus). Behav Neurosci. 2008;122(3):527–34. Deeming DC, Ferguson M. Physiological effects of incubation temperature on embryonic development in reptiles and birds. In: Deeming DC, Ferguson MW, editors. Egg incubation: Its effects on embryonic development in birds and reptilesCambridge University Press; 1991. p. 147–71. Delgado-González FJ, Alonso-Fuentes A, Delgado-Fumero A, García-Verdugo JM, Gonzalez-Granero S, Trujillo-Trujillo CM, et al. Seasonal differences in ventricular proliferation of adult Gallotia galloti lizards. Brain Res. 2008;1191:39–46. den Heijer T, Geerlings MI, Hofman A, de Jong FH, Launer LJ, Pols HAP, et al. Higher estrogen levels are not associated with larger hippocampi and better memory performance. Arch Neurol. 2003 Feb;60(2):213–20. Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza PV, Abrous DN. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci U S A. 2003;100(24):14385–90. Du WG, Shine R, Ma L, Sun BJ. Adaptive responses of the embryos of birds and reptiles to spatial and temporal variations in nest temperatures. Proc Biol Sci. 2019 Nov;286(1915):20192078. Ferner JW. Home-range size and overlap in Sceloporus undulatus erythrocheilus (Reptilia: iguanidae). Copeia. 1974;1974(2):332–7. Fitch HS. A field study of the growth and behavior of the fence lizardUniversity of California Publications in Zoology; 1940. Font E, García-Roa R, Pincheira-Donoso D, Carazo P. Rethinking the effects of body size on the study of brain size evolution. Brain Behav Evol. 2019;93(4):182–95. Galea LA, Perrot-Sinal TS, Kavaliers M, Ossenkopp KP. Relations of hippocampal volume and dentate gyrus width to gonadal hormone levels in male and female meadow voles. Brain Res. 1999;821(2):383–91. Gaulin SJ. Evolution of sex difference in spatial ability. Am J Phys Anthropol. 1992;35(S15):125–51. FitzGerald RW, FitzGerald RW. Sex differences in spatial ability: an evolutionary hypothesis and test. Am Naturalist. 1986;127(1):74–88. Gaulin SJ, Fitzgerald RW. Sexual selection for spatial-learning ability. Anim Behav. 1989;37:322–31. Geary DC. Sexual selection and sex differences in spatial cognition. Learn Individual Differences. 1995;7(4):289–301. Grisham W, Powers AS. Function of the dorsal and medial cortex of turtles in learning. Behav Neurosci. 1989 Oct;103(5):991–7. Grisham W, Powers AS. Effects of dorsal and medial cortex lesions on reversals in turtles. Physiol Behav. 1990 Jan;47(1):43–9. Guigueno MF, MacDougall-Shackleton SA, Sherry DF. Sex and seasonal differences in hippocampal volume and neurogenesis in brood-parasitic brown-headed cowbirds (Molothrus ater). Dev Neurobiol. 2016;76(11):1275–90. Guigueno MF, Snow DA, MacDougall-Shackleton SA, Sherry DF. Female cowbirds have more accurate spatial memory than males. Biol Lett. 2014;10(2):20140026. Gundersen HJ, Jensen EB. The efficiency of systematic sampling in stereology and its prediction. J Microsc. 1987 Sep;147(Pt 3):229–63. Hampton RR, Sherry DF, Shettleworth SJ, Khurgel M, Ivy G. Hippocampal volume and food-storing behavior are related in parids. Brain Behav Evol. 1995;45(1):54–61. Hampton RR, Shettleworth SJ. Hippocampus and memory in a food-storing and in a nonstoring bird species. Behav Neurosci. 1996;110(5):946–64. Healy SD, Krebs JR. Food storing and the hippocampus in corvids: amount and volume are correlated. Proc R Soc Lond Ser B. 1992;248(1323):241–5. Holding ML, Frazier JA, Taylor EN, Strand CR. Experimentally altered navigational demands induce changes in the cortical forebrain of free-ranging Northern Pacific Rattlesnakes (Crotalus o. oreganus). Brain Behav Evol. 2012;79(3):144–54. Jacobs LF, Gaulin SJ, Sherry DF, Hoffman GE. Evolution of spatial cognition: sex-specific patterns of spatial behavior predict hippocampal size. Proc Natl Acad Sci U S A. 1990;87(16):6349–52. Jarrard LE. On the role of the hippocampus in learning and memory in the rat. Behav Neural Biol. 1993;60(1):9–26. Jašarević E, Williams SA, Roberts RM, Geary DC, Rosenfeld CS. Spatial navigation strategies in Peromyscus: a comparative study. Anim Behav. 2012 Nov 1;84(5):1141–9. Jones CM, Braithwaite VA, Healy SD. The evolution of sex differences in spatial ability. Behav Neurosci. 2003 Jun;117(3):403–11. Jones SM, Droge DL. Home range size and spatial distributions of two sympatric lizard species (Sceloporus undulatus, Holbrookia maculata) in the sand hills of Nebraska. Herpetologica. 1980:127–32. Krebs JR, Sherry DF, Healy SD, Perry VH, Vaccarino AL. Hippocampal specialization of food-storing birds. Proc Natl Acad Sci U S A. 1989;86(4):1388–92. LaDage LD, Maged RM, Forney MV, Roth TCII, Sinervo B, Pravosudov VV. Interaction between territoriality, spatial environment, and hippocampal neurogenesis in male side-blotched lizards. Behav Neurosci. 2013;127(4):555–65. LaDage LD, Riggs BJ, Sinervo B, Pravosudov VV. Dorsal cortex volume in male side-blotched lizards, Uta stansburiana, is associated with different space use strategies. Anim Behav. 2009;78(1):91–6. LaDage LD, Roth TCII, Sinervo B, Pravosudov VV. Environmental experiences influence cortical volume in territorial and nonterritorial side-blotched lizards, Uta stansburiana. Anim Behav. 2016;115:11–8. LaDage LD, Roth TC, Downs CJ, Sinervo B, Pravosudov VV. Increased testosterone decreases medial cortical volume and neurogenesis in territorial side-blotched lizards (Uta stansburiana). Front Neurosci. 2017;11:97. Leuner B, Gould E. Structural plasticity and hippocampal function. Annu Rev Psychol. 2010;61:111–40. Licht P, Moberly WR. Thermal requirements for embryonic development in the tropical lizard Iguana iguana. Copeia. 1965;1965(4):515–7. Liu Y, Burmeister SS. Sex differences during place learning in the túngara frog. Anim Behav. 2017;128:61–7. López JC, Vargas JP, Gómez Y, Salas C. Spatial and non-spatial learning in turtles: the role of medial cortex. Behav Brain Res. 2003;143(2):109–20. López-García C, Molowny A, Martínez-Guijarro FJ, Blasco-Ibáñez JM, Luis de la Iglesia JA, Bernabeu A, et al. Lesion and regeneration in the medial cerebral cortex of lizards. Histol Histopathol. 1992;7(4):725–46. Lourdais O, Heulin B, Denardo DF. Thermoregulation during gravidity in the children’s python (Antaresia childreni): a test of the preadaptation hypothesis for maternal thermophily in snakes. Biol J Linn Soc. 2008;93(3):499–508. Lüddecke H. Space use, cave choice, and spatial learning in the dendrobatid frog Colostethus palmatus. Amphib Reptil. 2003;24(1):37–46. Lutterschmidt DI, Lucas AR, Karam RA, Nguyen VT, Rasmussen MR. Sexually dimorphic patterns of cell proliferation in the brain are linked to seasonal life-history transitions in red-sided garter snakes. Front Neurosci. 2018;12:364. Madularu D, Kulkarni P, Ferris CF, Brake WG. Changes in brain volume in response to estradiol levels, amphetamine sensitization and haloperidol treatment in awake female rats. Brain Res. 2015;1618:100–10. Maguire EA, Gadian DG, Johnsrude IS, Good CD, Ashburner J, Frackowiak RS, et al. Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci U S A. 2000;97(8):4398–403. Maguire EA, Woollett K, Spiers HJ. London taxi drivers and bus drivers: a structural MRI and neuropsychological analysis. Hippocampus. 2006;16(12):1091–101. Medina L, Abellán A, Desfilis E. Contribution of genoarchitecture to understanding hippocampal evolution and development. Brain Behav Evol. 2017;90(1):25–40. Moran A, Wojcik L, Cangiane L, Powers AS. Dorsal cortex lesions impair habituation in turtles (Chrysemys picta). Brain Behav Evol. 1998;51(1):40–7. Morris RG, Garrud P, Rawlins JN, O’Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature. 1982;297(5868):681–3. Moser E, Moser M-B, Andersen P. Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J Neurosci. 1993;13(9):3916–25. Muth A. Physiological ecology of desert iguana (Dipsosaurus dorsalis) eggs: temperature and water relations. Ecology. 1980;61(6):1335–43. Ochinskaia EI, Rubtsova NB. [Extrapolation reactions following destruction of the dorsal cortex of the turtle forebrain]. Zh Vyssh Nerv Deiat Im I P Pavlova. 1976;26(3):626–32. Pollock NB, Vredevoe LK, Taylor EN. The effect of exogenous testosterone on ectoparasite loads in free-ranging western fence lizards. J Exp Zool A Ecol Genet Physiol. 2012 Aug;317(7):447–54. Pravosudov VV, Clayton NS. A test of the adaptive specialization hypothesis: population differences in caching, memory, and the hippocampus in black-capped chickadees (Poecile atricapilla). Behav Neurosci. 2002 Aug;116(4):515–22. Reboreda JC, Clayton NS, Kacelnik A. Species and sex differences in hippocampus size in parasitic and non-parasitic cowbirds. Neuroreport. 1996 Jan;7(2):505–8. Reiter S, Liaw HP, Yamawaki TM, Naumann RK, Laurent G. On the value of reptilian brains to map the evolution of the hippocampal formation. Brain Behav Evol. 2017;90(1):41–52. Rodríguez F, López JC, Vargas JP, Gómez Y, Broglio C, Salas C. Conservation of spatial memory function in the pallial forebrain of reptiles and ray-finned fishes. J Neurosci. 2002 Apr 22;22(7):2894–903. Roof RL, Havens MD. Testosterone improves maze performance and induces development of a male hippocampus in females. Brain Res. 1992 Feb 572;572(1-2):310–3. Roth ED, Lutterschmidt WI, Wilson DA. Relative medial and dorsal cortex volume in relation to sex differences in spatial ecology of a snake population. Brain Behav Evol. 2006;67(2):103–10. Roth TC, 2nd, Krochmal AR, LaDage LD. Reptilian cognition: a more complex picture via integration of neurological mechanisms, behavioral constraints, and evolutionary context. Bioessays. 2019 Aug;41(8):e1900033. Ruby DE. Seasonal changes in the territorial behavior of the iguanid lizard Sceloporus jarrovi. Copeia. 1978;1978(3):430–8. Sabo JL. Hot rocks or no hot rocks: overnight retreat availability and selection by a diurnal lizard. Oecologia. 2003 Aug;136(3):329–35. Sexton OJ, Marion KR. Duration of incubation of Sceloporus undulatus eggs at constant temperature. Physiol Zoolog. 1974;47(2):91–8. Sheldahl LA, Martins EP. The territorial behavior of the western fence lizard, Sceloporus occidentalis. Herpetologica. 2000;56(4):469–79. Sherry DF. The ecology and neurobiology of spatial memory. Cognitive ecology: the evolutionary ecology of information processing and decision makin. 1998. p. 261–96. Sherry DF, Forbes MR, Khurgel M, Ivy GO. Females have a larger hippocampus than males in the brood-parasitic brown-headed cowbird. Proc Natl Acad Sci U S A. 1993;90(16):7839–43. Sherry DF, Jacobs LF, Gaulin SJ. Spatial memory and adaptive specialization of the hippocampus. Trends Neurosci. 1992;15(8):298–303. Shine R. Is increased maternal basking an adaptation or a pre-adaptation to viviparity in lizards?J Exp Zool A Comp Exp Biol. 2006;305(6):524–35. Shine R, Elphick MJ, Harlow PS. The influence of natural incubation environments on the phenotypic traits of hatchling lizards. Ecology. 1997;78(8):2559–68. Stebbins RC. Amphibians and reptiles of Western North America. New York: McGraw-Hill; 1954. Striedter GF. Evolution of the hippocampus in reptiles and birds. J Comp Neurol. 2016 Feb;524(3):496–517. Sutherland RJ, Whishaw IQ, Kolb B. A behavioural analysis of spatial localization following electrolytic, kainate-or colchicine-induced damage to the hippocampal formation in the rat. Behav Brain Res. 1983;7(2):133–53. Turner FB, Jennrich RI, Weintraub JD. Home ranges and body size of lizards. Ecology. 1969;50(6):1076–81. Willmer P. Microclimate and the environmental physiology of insects. Adv Insect Physiol. 1982;16:1–57. Yang C, Wang L, Xing X, Gao Y, Guo L. Seasonal variation in telencephalon cell proliferation in adult female tsinling dwarf skinks (Scincella tsinlingensis). Brain Res. 2017 May;1662:7–15. Article / Publication Details
Received: March 23, 2022
Accepted: February 06, 2023
Published online: February 16, 2023
Number of Print Pages: 10
Number of Figures: 2
Number of Tables: 0
ISSN: 0006-8977 (Print)
eISSN: 1421-9743 (Online)
For additional information: https://www.karger.com/BBE
Copyright / Drug Dosage / Disclaimer Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
留言 (0)