Navigational and social challenges due to habitat conditions and sociality are known to influence dentate gyrus (DG) morphology, yet the relative importance of these factors remains unclear. Thus, we studied three natural populations of O. lunatus (Los Molles) and Octodon degus (El Salitre and Rinconada), two caviomorph species that differ in the extent of sociality and with contrasting vegetation cover of habitat used. The brains and DG of male and female breeding degus with simultaneous information on their physical and social environments were examined. The extent of sociality was quantified from total group size and range area overlap. O. degus at El Salitre was more social than at Rinconada and than O. lunatus from Los Molles. The use of transects to quantify cover of vegetation (and other physical objects in the habitat) and measures of the spatial behavior of animals indicated animal navigation based on unique cues or global landmarks is more cognitively challenging to O. lunatus. During lactation, female O. lunatus had larger brains than males. Relative DG volume was similar across sexes and populations. The right hemisphere of male and female O. lunatus had more cells than the left hemisphere, with DG directional asymmetry not found in O. degus. Degu population differences in brain size and DG cell number seemed more responsive to differences in habitat than to differences in sociality. Yet, large-sized O. degus (but not O. lunatus) that ranged over larger areas and were members of larger social groups had more DG cells per hemisphere. Thus, within-population variation in DG cell number by hemisphere was consistent with a joint influence of habitat and sociality in O. degus at El Salitre.

1.
Amrein I, Becker AS, Engler S, Huang S, Müller J, Slomianka L, Oosthuizen MK (2014): Adult neurogenesis and its anatomical context in the hippocampus of three mole-rat species. Front Neuroanat 8:39.
[PubMed]
2.
Barkley CL, Jacobs LF (1998): Visual environment and delay affect cache retrieval accuracy in a food-storing rodent. Anim Learn Behav 26:439-447.
3.
Barkley CL, Jacobs LF (2007): Sex and species differences in spatial memory in food storing kangaroo rats. Anim Behav 73:321-329.
4.
Bauer CM, Hayes LD, Ebensperger LA, Romero LM (2014): Seasonal variation in the degu (Octodon degus) endocrine stress response. Gen Comp Endocrinol 197:26-32.
[PubMed]
5.
Beery A, Kamal Y, Sobrero R, Hayes LD (2016): Comparative neurobiology and genetics of mammalian social behavior; in Ebensperger LA, Hayes LD (eds): Sociobiology of Caviomorph Rodents. Hoboken, Wiley.
6.
Beery AK, Kaufer D (2015): Stress, social behavior, and resilience: insights from rodents. Neurobiol Stress 1:116-127.
[PubMed]
7.
Biegler R, Morris RG (1996): Landmark stability: further studies pointing to a role in spatial learning. QJ Exp Psychol B 49:307-345.
[PubMed]
8.
Bruck JN, Mateo JM (2010): How habitat features shape ground squirrel (Urocitellus beldingi) navigation. J Comp Psychol 124:176-186.
[PubMed]
9.
Bruel-Jungerman E, Laroche S, Rampon C (2005): New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur J Neurosci 21:513-521.
[PubMed]
10.
Burger DK, Gulbrandsen T, Saucier DM, Iwaniuk AN (2014): The effects of season and sex on dentate gyrus size and neurogenesis in a wild rodent, Richardson's ground squirrel (Urocitellus richardsonii). Neuroscience 272:240-251.
[PubMed]
11.
Burger DK, Saucier JM, Iwaniuk AN, Saucier DM (2013): Seasonal and sex differences in the hippocampus of a wild rodent. Behav Brain Res 1:131-138.
[PubMed]
12.
Burnham KP, Anderson DR (2002): Model Selection and Multimodel Inference, ed 2. New York, Springer.
13.
Champagne FA, Curley JP (2009): The trans-generational influence of maternal care on offspring gene expression and behavior in rodents; in Maestripieri D, Mateo JM (eds): Maternal Effects in Mammals. Chicago, University of Chicago Press, pp 182-202.
14.
Cimadevilla JM (2001): Transient sex differences in the between-sessions but not in the within-session memory underlying an active place avoidance task in weanling rats. Behav Neurosci 115:695-703.
[PubMed]
15.
Cirulli F, Berry A, Bonsignore LT, Capone F, D'Andrea I, Aloe L, Branchi I, Alleva E (2010): Early life influences on emotional reactivity: evidence that social enrichment has greater effects than handling on anxiety-like behaviors, neuroendocrine responses to stress and central BDNF levels. Neurosci Biobehav Rev 34:808-820.
[PubMed]
16.
Clayton NS, Krebs JR (1994): Memory for spatial and object-specific cues in food-storing and non-storing birds. J Comp Physiol A 174:371-379.
17.
Clutton-Brock TH, Harvey PH (1980): Primates, brains and ecology. J Zool Lond 190:309-323.
18.
Dukas R (1998): Cognitive Ecology: The Evolutionary Ecology of Information Processing and Decision Making. Chicago, University of Chicago Press.
19.
Dunbar RIM (1998): The social brain hypothesis. Evol Anthropol 6:178-190.
20.
Ebensperger LA, Blumstein DT (2006): Sociality in New World hystricognath rodents is linked to predators and burrow digging. Behav Ecol 17:410-418.
21.
Ebensperger LA, Bozinovic F (2000): Communal burrowing in the hystricognath rodent, Octodon degus: a benefit of sociality? Behav Ecol Sociobiol 47:365-369.
22.
Ebensperger LA, Chesh AS, Castro RA, Ortiz Tolhuysen L, Quirici Q, Burger JR, Hayes LD (2009): Instability rules social groups in the communal breeder rodent Octodon degus. Ethology 115:540-554.
23.
Ebensperger LA, Cofré H (2001): On the evolution of group-living in the New World cursorial hystricognath rodents. Behav Ecol 12:227-236.
24.
Ebensperger LA, Hurtado MJ, Soto-Gamboa M, Lacey EA, Chang AT (2004): Communal nesting and kinship in degus (Octodon degus). Naturwissenschaften 91:391-395.
[PubMed]
25.
Ebensperger LA, Sobrero R, Quirici V, Castro RA, Ortiz Tolhuysen L, Vargas F, Burger JR, Quispe R, Villavicencio C, Vásquez R, Hayes LD (2012): Ecological drivers of group living in two populations of the communally rearing rodent, Octodon degus. Behav Ecol Sociobiol 66:261-274.
[PubMed]
26.
Ebensperger LA, Tamarin RH (1997): Use of fluorescent powder to infer mating activity of male rodents. J Mammal 78:888-893.
27.
Eichenbaum H (2015): The hippocampus as a cognitive map of social space. Neuron 87:9-11.
[PubMed]
28.
Fowler CD, Liu Y, Ouimet C, Wang Z (2002): The effects of social environment on adult neurogenesis in the female prairie vole. J Neurobiol 51:115-128.
[PubMed]
29.
Fulk GW (1976): Notes on the activity, reproduction, and social behavior of Octodon degus. J Mammal 57:495-505.
30.
Galea LA, McEwen BS (1999): Sex and seasonal differences in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles. Microtus pennsylvannicus. Neuroscience 89:955-964.
[PubMed]
31.
Galea LA, Ormerod BK, Sampath S, Kostaras X, Wilkie DM, Phelps MT (2000): Spatial working memory and hippocampal size across pregnancy in rats. Horm Behav 37:86-95.
[PubMed]
32.
Gheusi G, Ortega-Perez I, Murray K, Lledo PM (2009): A niche for adult neurogenesis in social behaviour. Behav Brain Res 200:315-322.
[PubMed]
33.
Gundersen HJG, Jensen EB (1987): The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229 -263.
[PubMed]
34.
Hamilton WL, Diamond MC, Johnson RE, Ingham CA (1977): Effects of pregnancy and differential environments on rat cerebral cortical depth. Behav Biol 19:333-340.
[PubMed]
35.
Hayes LD, Chesh AS, Castro RA, Ortiz Tolhuysen L, Burger JR, Bhattacharjee J, Ebensperger LA (2009): Fitness consequences of group living in the degu Octodon degus, a plural breeder rodent with communal care. Anim Behav 78:131-139.
36.
Herculano-Houzel S, Collins CE, Wong P, Kaas H (2007): Cellular scaling rules for primate brains. Proc Natl Acad Sci USA 104:3562-3567.
[PubMed]
37.
Herculano-Houzel S, Messeder DJ, Fonseca-Azevedo K, Pantoja NA (2015): When larger brains do not have more neurons: increased numbers of cells are compensated by decreased average cell size across mouse individuals. Front Neuroanat 9:64.
[PubMed]
38.
Herculano-Houzel S, Mota B, Lent R (2006): Cellular scaling rules for rodent brains. Proc Natl Acad Sci USA 103:12138-12143.
[PubMed]
39.
Hoshaw BA, Evans JC, Mueller B, Valentino RJ, Lucki I (2006): Social competition in rats: cell proliferation and behaviour. Behav Brain Res 175:343-351.
[PubMed]
40.
Jacobs LF (1995): The ecology of spatial cognition: adaptive patterns of hippocampal size and space use in wild rodents; in Alleva E, Fasolo A, Lipp H-P, Nadel L (eds): Studies of the Brain in Naturalistic Settings. Dordrecht, Kluwer, pp 301-322.
41.
Jacobs LF (1996): The economy of winter: phenotypic plasticity in behaviour and brain structure. Biol Bull 191:92-100.
[PubMed]
42.
Jacobs LF (2003): The evolution of the cognitive map. Brain Behav Evol 62:128-139.
[PubMed]
43.
Jacobs LF (2006): From movement to transitivity: the role of hippocampal parallel maps in configural learning. Rev Neurosci 17:99-109.
[PubMed]
44.
Jacobs LF, Schenk F (2003): Unpacking the cognitive map: the parallel map theory of hippocampal function. Psychol Rev 110:285-315.
[PubMed]
45.
Jesseau SA (2004): Kin Discrimination and Social Behaviour in Communally Nesting Degus (Octodon degus); PhD dissertation, Univeristy of Michigan.
46.
Jones CM, Braithwaite VA, Healy SD (2003): The evolution of sex differences in spatial ability. Behav Neurosci 117:403-411.
[PubMed]
47.
Kalcounis-Ruppell MC, Patrick A, Millar JS (2001): Effect of fluorescent powder marking of females on mate choice by male white-footed mice (Peromyscus leucopus). Am Midl Nat 146:429-433.
48.
Kempermann G, Kuhn HG, Gage FH (1997): More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495.
[PubMed]
49.
Kenward RE (1987): Wildlife Radio Tagging: Equipment, Field Techniques and Data Analysis. London, Academic Press.
50.
Kenward RE (2001): A Manual for Wildlife Radio Tagging. San Diego, Academic Press.
51.
Kenward RE, South AB, Walls SS (2003): Ranges 6, Version 1.2: For the Analysis of Tracking and Location Data. Wareham, Anatrack Ltd.
52.
Kozorovitskiy Y, Gould E (2004): Dominance hierarchy influences adult neurogenesis in the dentate gyrus. J Neurosci 24:6755-6759.
[PubMed]
53.
Kumazawa-Manita N, Katayama M, Hashikawa T, Iriki A (2013): Three-dimensional reconstruction of brain structures of the rodent Octodon degus: a brain atlas constructed by combining histological and magnetic resonance images. Exp Brain Res 231:65-74.
[PubMed]
54.
Lagos VO, Contreras LC, Meserve PL, Gutiérrez JR, Jaksic, FM (1995): Effects of predation risk on space use by small mammals: a field experiment with a neotropical rodent. Oikos 74:259-264.
55.
LaMendola NP, Bever TG (1997): Peripheral and cerebral asymmetries in the rat. Science 278:483-486.
[PubMed]
56.
Langley CM (1994): Spatial memory in the desert kangaroo rat (Dipodomys deserti). J Comp Psychol 108:3-14.
[PubMed]
57.
Lemen CA, Freeman PW (1985): Tracking mammals with fluorescent pigments: a new technique. J Mammal 66:134-136.
58.
Lu L, Bao G, Chen H, Xia P, Fan X, Zhang J, Pei G, Ma L (2003): Modification of hippocampal neurogenesis and neuroplasticity by social environments. Exp Neurol 183:600-609.
[PubMed]
59.
MacFadden A, Elias L, Saucier D (2003): Males and females scan maps similarly, but give directions differently. Brain Cogn 53:297-300.
[PubMed]
60.
Maguire EA, Woollett K, Spiers HJ (2006): London taxi drivers and bus drivers: a structural MRI and neuropsychological analysis. Hippocampus 16:1091-1101.
[PubMed]
61.
McEwen B (2002): Estrogen actions throughout the brain. Recent Prog Horm Res 57:357-384.
[PubMed]
62.
Nams VO (1990): Locate II User's Guide. Tatamagouche, Pacer Computer Software.
63.
Nesterova AP (2007): Age-dependent use of local and global landmarks during escape: experiments using Columbian ground squirrels. Behav Processes 75:276-282.
[PubMed]
64.
Nilsson M, Perfilieva E, Johansson U, Orwar O, Eriksson PS (1999): Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J Neurobiol 39:569-578.
[PubMed]
65.
O'Keefe J, Nadel J (1978): The Hippocampus as a Cognitive Map. Oxford, Clarendon Press.
66.
Popović N, Madrid JA, Rol MA, Caballero-Bleda M, Popović M (2010): Barnes maze performance of Octodon degus is gender dependent. Behav Brain Res 212:159-167.
[PubMed]
67.
Pucek M (1965): Water contents and seasonal changes of the brain weight in shrews. Acta Theriol 10:353-367.
68.
Pyter LM (2005): Short photoperiods impair spatial learning and alter hippocampal dendritic morphology in adult male white-footed mice (Peromyscus leucopus). J Neurosci 25:4521-4526.
[PubMed]
69.
Quispe R, Villavicencio CP, Cortés A, Vásquez RA (2009): Interpopulation variation in hoarding behaviour in degus, Octodon degus. Ethology 115:465-474.
70.
Roes M, Galea LAM (2016): The maternal brain: short- and long-term effects of reproductive experience on hippocampus structure and function in adulthood; in Shansky RM (ed): Sex Differences in the Central Nervous System. Amsterdam, Elsevier, pp 197-221.
71.
Rogers LJ, Vallortigara G (2015): When and why did brains break symmetry? Symmetry 7:2181-2194.
72.
Rogers LJ, Vallortigara G, Andrew RJ (2013): Divided Brains: The Biology and Behaviour of Brain Asymmetries. New York, Cambridge University Press.
73.
Roth TC II, Pravosudov VV (2009): Hippocampal volume and neuron numbers increase along a gradient of environmental harshness: a large-scale comparison. Proc R Soc B 276:401-405.
[PubMed]
74.
Rubenstein DR (2011): Spatiotemporal environmental variation, risk aversion, and the evolution of cooperative breeding as a bet-hedging strategy. Proc Natl Acad Sci USA 108:10816-10822.
[PubMed]
75.
Sandstrom NJ, Kaufman J, Huettel SA (1998): Males and females use different distal cues in a virtual environment navigation task. Brain Res Cogn Brain Res 6:351-360.
[PubMed]
76.
Sherry DF, Jacobs LF, Gaulin SJ (1992): Spatial memory and adaptive specialization of the hippocampus. Trends Neurosci 15:298-302.
[PubMed]
77.
Shettleworth SJ (1998): Cognition, Evolution and Behaviour. New York, Oxford University Press.
78.
Sikes RS, Gannon WL, The Animal Care and Use Committee of the American Society of Mammalogists (2011): Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92:235-253.
79.
Silk JB (2007): The adaptive value of sociality in mammalian groups. Phil Trans R Soc B 362:539-559.
[PubMed]
80.
Sobrero R, Ly Prieto A, Ebensperger LE (2014): Activity, overlap of range areas, and sharing of resting locations in the moon-toothed degu, Octodon lunatus. J Mammal 95:91-98.
81.
Sokal RR, Rohlf FJ (1995): Biometry: The Principles and Practice of Statistics in Biological Research, ed 3. New York, Freeman.
82.
Swihart RK, Slade NA (1985): Testing for independence of observations in animal movements. Ecology 66:1176-1184.
83.
Symonds MRE, Moussalli A (2011): A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike's information criterion. Behav Ecol Sociobiol 65:13-21.
84.
Tavares RM, Mendelsohn A, Grossman Y, Williams CH, Shapiro M, Trope Y, Schiller D (2015): A map for social navigation in the human brain. Neuron 87:231-243.
[PubMed]
85.
Vallortigara G, Pagni P, Sovrano VA (2004): Separate geometric and non-geometric modules for spatial reorientation: evidence from a lopsided animal brain. J Cogn Neurosci 16:390-400.
[PubMed]
86.
Vallortigara G, Rogers LJ (2005): Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:574-633.
[PubMed]
87.
van Praag H, Kempermann G, Gage FH (1999): Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266-270.
[PubMed]
88.
Vásquez RA, Ebensperger LA, Bozinovic F (2002): The influence of habitat on travel speed, intermittent locomotion, and vigilance in a diurnal rodent. Behav Ecol 13:182-187.
89.
Vega-Zuniga T, Medina FS, Fredes F, Zuniga C, Severín D, Palacios AG, Karten HJ, Mpodozis J (2013): Does nocturnality drive binocular vision? Octodontine rodents as a case study. PLoS One 8:e84199.
[PubMed]
90.
Vlasak AN (2006): Global and local spatial landmarks: their role during foraging by Columbian ground squirrels (Spermophilus columbianus). Anim Cogn 9:71-80.
[PubMed]
91.
West MJ, Slomianka L, Gundersen HJ (1991): Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
[PubMed]
92.
Whitehead H (2008): Analyzing Animal Societies: Quantitative Methods for Vertebrate Social Analysis. Chicago, University of Chicago Press.
93.
Whitehead H (2009): SOCPROG programs: analysing animal social structures. Behav Ecol Sociobiol 63:765-778.
94.
Workman JL, Bowers SL, Nelson RJ (2009): Enrichment and photoperiod interact to affect spatial learning and hippocampal dendritic morphology in white-footed mice (Peromyscus leucopus). Eur J Neurosci 29:161-170.
[PubMed]
95.
Wright JW, Kern MD (1992): Stereotaxic atlas of the brain of Octodon degus. J Morphol 214:299-320.
[PubMed]
96.
Zar JH (1999): Biostatistical Analysis, ed 4. Englewood Cliffs, Prentice Hall.
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