Variation in environmental conditions associated with differential selection on spatial memory has been hypothesized to result in evolutionary changes in the morphology of the hippocampus, a brain region involved in spatial memory. At the same time, it is well known that the morphology of the hippocampus might also be directly affected by environmental conditions. Understanding the role of environment-based plasticity is therefore critical when investigating potential adaptive evolutionary changes in the hippocampus associated with environmental variation. We previously demonstrated large elevation-related variation in hippocampus morphology in mountain chickadees over an extremely small spatial scale. We hypothesized that this variation is related to differential selection pressures associated with differences in winter climate severity along an elevation gradient, which make different demands on spatial memory used for food cache retrieval. Here, we tested whether such variation is experience based, generated by potential differences in the environment, by comparing the hippocampus morphology of chickadees from different elevations maintained in a uniform captive environment in a laboratory with those sampled directly from the wild. In addition, we compared hippocampal neuron soma size in chickadees sampled directly from the wild with those maintained in laboratory conditions with restricted and unrestricted spatial memory use via manipulation of food-caching experiences to test whether memory use can affect neuron soma size. There were significant elevation-related differences in hippocampus volume and the total number of hippocampal neurons, but not in neuron soma size, in captive birds. Captive environmental conditions were associated with a large reduction in hippocampus volume and neuron soma size, but not in the total number of neurons or in neuron soma size in other telencephalic regions. Restriction of memory use while in laboratory conditions produced no significant effects on hippocampal neuron soma size. Overall our results showed that captivity has a strong effect on hippocampus volume, which could be due, at least partly, to a reduction in neuron soma size specifically in the hippocampus, but it did not override elevation-related differences in hippocampus volume or in the total number of hippocampal neurons. These data are consistent with the idea of the adaptive nature of the elevation-related differences associated with selection on spatial memory, while at the same time demonstrating additional environment-based plasticity in hippocampus volume, but not in neuron numbers. Our results, however, cannot rule out that the differences between elevations might still be driven by some developmental or early posthatching conditions/experiences.

Keywords:
Hippocampus, Memory, Chickadee, Environment, Evolution, Neuron, Neuron soma
1.
Bolhuis JJ, Wynne CDL (2009): Can evolution explain how minds work? Nature 458:832-833.
2.
Clayton NS (1996): Development of food-storing and the hippocampus in juvenile marsh tits (Parus palustris). Behav Brain Res 74:153-159.
3.
Clayton NS (2001): Hippocampal growth and maintenance depend on food-caching experience in juvenile mountain chickadees (Poecile gambeli). Behav Neurosci 115:614-625.
4.
Clayton NS, Krebs JR (1994): Hippocampal growth and attrition in birds affected by experience. Proc Natl Acad Sci USA 91:7410-7414.
5.
Cole EF, Morrand-Ferron J, Hinks A, Quinn JL (2012): Cognitive ability influences reproductive life history variation in the wild. Curr Biol 22:1808-1812.
6.
Crispo E, Chapman LJ (2010): Geographic variation in phenotypic plasticity in response to dissolved oxygen in African cichlid fish. J Evol Biol 23:2091-2103.
7.
DeVoogd T, Nottebohm F (1981): Gonadal hormones induce dendritic growth in the adult avian brain. Science 214:202-204.
8.
Freas CA, LaDage LD, Roth TC 2nd, Pravosudov VV (2012): Elevation-related differences in memory and the hippocampus in mountain chickadees (Poecile gambeli). Anim Behav 84:121-127.
9.
Freas CA, Roth TC 2nd, LaDage LD, Pravosudov VV (2013): Hippocampal neuron soma size is associated with population differences in winter climate severity in food-caching chickadees. Funct Ecol, in press.
10.
Garroway CJ, Radersma R, Sepil I, Santure AW, De Cauwer I, Slate J, Sheldon BC (2013): Fine-scale genetic structure in a wild bird population: the role of limited dispersal and environmentally based selection as causal factors. Evolution, E-pub ahead of print.
11.
Gonda A, Herczeg G, Merila J (2009): Habitat-dependent and -independent plastic responses to social environment in the none-spined stickleback (Pungitius pungitius) brain. Proc Biol Sci 276:2085-2092.
12.
Gonda A, Herczeg G, Merila J (2011): Population variation in brain size of none-spined sticklebacks (Pungitius pungitius) - local adaptation or environmentally induced variation? BMC Evol Biol 11:75.
13.
Herculano-Houzel S (2011): Brains matter, bodies maybe not: the case for examining neuron numbers irrespective of body size. Ann NY Acad Sci 1225:191-199.
14.
Herculano-Houzel S (2012): The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated costs. Proc Natl Acad Sci USA 109(suppl 1):10661-10668.
15.
Kolb B, Whishaw IQ (1998): Brain plasticity and behavior. Annu Rev Psychol 49:43-64.
16.
Krebs JR, Sherry DF, Healy SD, Perry VH, Vaccarino AL (1989): Hippocampal specialization of food-storing birds. Proc Natl Acad Sci USA 86:1388-1392.
17.
LaDage LD, Roth TC 2nd, Fox RA, Pravosudov VV (2009): Effects of captivity and memory-based experiences on the hippocampus in mountain chickadees. Behav Neurosci 123:284-291.
18.
LaDage LD, Roth TC 2nd, Fox RA, Pravosudov VV (2010): Ecologically-relevant spatial memory use modulates hippocampal neurogenesis. Proc Biol Sci 365:859-867.
19.
Leuner B, Gould E (2010): Structural plasticity and hippocampal function. Annu Rev Psychol 61:111-140.
20.
Oberlander JG, Schlinger BA, Clayton NS, Saldanha CJ (2004): Neural aromatization accelerates the acquisition of spatial memory via an influence on the song bird hippocampus. Horm Behav 45:250-258.
21.
Pravosudov VV, Clayton NS (2002): A test of the adaptive specialization hypothesis: population differences in caching, memory and the hippocampus in black-capped chickadees (Poecile atricapilla). Behav Neurosci 116:515-522.
22.
Pravosudov VV, Roth TC 2nd (2013): Cognitive ecology of food-hoarding: the evolution of spatial memory and the hippocampus. Ann Rev Ecol Evol Syst, in press.
23.
Pravosudov VV, Roth TC 2nd, Forister M, LaDage LD, Burg T, Braun M, Davidson B (2012): Population genetic structure and its implications for adaptive variation in memory and the hippocampus on a continental scale in food-caching black-capped chickadees. Molec Ecol 21:4486-4497.
24.
Pravosudov VV, Smulders TV (2010): Integrating ecology, psychology, and neurobiology within a food-hoarding paradigm. Philos Trans R Soc Lond B Biol Sci 365:859-867.
25.
Roth TC 2nd, Brodin A, LaDage LD, Smulders TV, Pravosudov VV (2010): Is bigger always better? A critical appraisal of the issue of volumetric analysis in the study of the hippocampus. Philos Trans R Soc Lond B Biol Sci 365:915-931.
26.
Roth TC 2nd, LaDage LD, Freas FA, Pravosudov VV (2012): Variation in memory and the hippocampus across populations with different climates: a common garden approach. Proc Biol Sci 279:402-410.
27.
Roth TC 2nd, LaDage LD, Pravosudov VV (2011): Variation in hippocampal morphology along an environmental gradient: controlling for the effect of day length. Proc Biol Sci 278:2662-2667.
28.
Roth TC 2nd, Pravosudov VV (2009): Hippocampal volume and neuron numbers increase along a gradient of environmental harshness: a large-scale comparison. Proc Biol Sci 276:401-405.
29.
Sherry DF, Vaccarino AL, Buckenham K, Herz RS (1989): The hippocampus complex of food-storing birds. Brain Behav Evol 34:308 -317.
30.
Sherwood CC, Stimpson CD, Raghanti MA, Wildman DE, Uddin M, Grossman LI, Goodman M, Redmond JC, Bonar CJ, Erwin JM, Hof PR (2006): Evolution of increased glia-neuron rations in the human frontal cortex. Proc Natl Acad Sci USA 103:13606-13611.
31.
Smulders TV, Casto JM, Nolan V Jr, Ketterson ED, DeVoogd TJ (2000): Effects of captivity and testosterone on the volumes of four brain regions in the dark-eyed junco (Junco hyemalis). J Neurobiol 43:244-253.
32.
Smulders TV, Sasson AD, DeVoogd TJ (1995): Seasonal variation in hippocampal volume in a food-storing bird, the black-capped chickadee. J Neurobiol 27:15-25.
33.
Tarr B, Rabinowitz J, Ali Imtiaz M, DeVoogd TJ (2009): Captivity reduces hippocampal volume but not survival of new cells in a food-storing bird. Dev Neurobiol 69:972-981.
34.
Van Schaik CP, Isler K, Burkart JM (2012): Explaining brain size variation: from social to cultural brain. Trends Cogn Sci 16:277-284.
35.
Woollett K, Maguire EA (2011): Acquiring ‘the knowledge' of London's layout drives structural brain changes. Curr Biol 21:2109-2114.
© 2013 S. Karger AG, Basel
2013
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.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.