Research reportSociability, but not spatial memory, is correlated with regional brain volume variation in the striped mouse Rhabdomys spp.
Introduction
Taxa occurring in different parts of a geographic range usually experience different local conditions and selection pressures, leading to geographic variation in phenotypes [1]. For instance, black-capped chickadees Poecile atricapillus from colder climates had more accurate memory recall and efficient cache retrieval compared to conspecifics in a milder climate [2], since any unnecessary activity is more energetically costly [3]. Differences in behavioural phenotypes are frequently accompanied by neural differences in the brain, such as the hippocampus and the amygdala, which are involved in, amongst other things, spatial navigation [4], [5] and social recognition [6]. Cryptic taxa, while morphologically similar, may differ in behaviour and neural capacity [7]. For example, cryptic species of Old World leaf warblers (Phylloscopus inornatus and P. humei) are morphologically indistinct but differ in vocalisations [8]. Similarly, the cursor grass mouse Akodon cursor and the montane grass mouse A. montensis are indistinguishable based on external identification but differ in skull size and shape [9]. Within the cryptic striped mouse genus Rhabdomys, taxa differ in social organisation [10], [11], spatial-cue preference in navigation [12], and in personality [13], [14]. In this study, we investigated the correlation between behaviour and brain volume in this cryptic small rodent genus that occurs in a variety of habitats.
Brain areas work together in large-scale functional networks to carry out specific cognitive functions [15]. Behaviours that have specific target regions in the brain (e.g., spatial navigation and the hippocampus, and sociality and the amygdala) may thus result in these brain regions becoming larger where new information is stored in extensive neuronal networks as short-term memory and later consolidated into long-term memory [16]. Individuals with a greater memory capacity may be better able to retrieve memories and display greater capacities for related behaviours [17], [18]. This is evident with food-storing which requires a greater memory capacity in order to locate previously cached food [17]. For example, marsh tits Parus palustris allowed to store and retrieve caches have larger hippocampal volumes than control individuals that were prevented from caching food [19]. Similarly, animals with larger home ranges have better spatial memories, as occurs in male bank voles Clethrionomys glareolus, where home ranges shrink seasonally, with voles showing a corresponding reduction in hippocampus size and spatial activity [20].
Brain areas specialised for higher cognitive function, like the hippocampus for spatial navigation, tend to be larger in species that have greater spatial requirements, and thus have higher energetic requirements to maintain large neural networks (i.e., the Expensive-Tissue Hypothesis [21]). As a result of this higher energetic requirement, cognitive ability can be adaptive only as long as the evolutionary trade-off between the fitness that results as a consequence of the behaviour outweighs the cost of maintaining the larger brain size that is needed (reviewed in [22]). Thus, the environment will select for cognitive traits and brain sizes that result in greater reproductive fitness. For example, black-capped chickadees with denser hippocampal neural-networks and better spatial memories are more likely to survive to reproduce than chickadees with less dense neural networks [23]. This selection pressure may act to a lesser degree in chickadee populations where the climate is less harsh since food is often more abundant and so would not necessarily affect survival [23].
The hippocampus has been linked to working memory in both spatial and non-spatial tasks [24], using sensory cues to form a cognitive map of the environment during exploration [25]. Animals from more challenging environments have larger hippocampal volumes and better spatial memory [17], [26]. For example, zebrafish Danio rerio housed in more structurally complex environments had larger telencephalon volumes (a hippocampus analogue involved in spatial memory in fish) as well as better performances in a spatial task [27]. There is no evidence of a relationship between environmental homogeneity and navigation capability in the literature. Instead, in cichlids, species from a rocky habitat (Asprotilapia leptura) were quicker and made fewer errors in a spatial maze than species from a sandy habitat (Xenotilapia flavipinnis) [28]. In addition, males often display better spatial navigation abilities than females (e.g., meadow voles Microtus pennsylvanicus, [29]; deer mice Peromyscus maniculatus [30]), correlated with increased dispersal or larger home ranges as a result of mate-seeking [29], and have larger hippocampal volumes than females (e.g., meadow voles Microtus pennsylvanicus [31]). In guppies Poecilia reticulata, males usually occupy more complex habitats, disperse more often than females and are able to learn to navigate a complex maze more easily than females [32]. There are some exceptions where sex differences are absent, such as in Cape mole-rats Georychus capensis and Damaraland mole-rats Fukomys damarensis [33] and pine voles Microtus pinetorum [31]. Likewise, Healy et al. [34] found no consistent sex effects in Lister hooded rats Rattus norvegicus – males and females took a similar amount of time to complete the Morris Water Maze task. Thus, structurally complex environments appear to require greater spatial memory and therefore influence hippocampus size between taxa [23], and sexes [31].
The hippocampus has also been linked to sociability through social learning and social memory (reviewed in [35]). Group-living animals must be able to recognise and remember individuals that form part of their group in order to display appropriate behaviours, i.e., affiliative behaviours mainly toward group members but not strangers (reviewed in [36]). Hippocampal-lesioned C57BL/6J lab mice were unable to recognise familiar juvenile mice [37]. Similarly, Uekita & Okanoya [38] found that hippocampal-lesioned common degus Octodon degus did not show any differences in social behaviour toward familiar and novel conspecifics, whereas control degus were more aggressive toward novel degus but exhibited more affiliative behaviours toward familiar conspecifics. Therefore, social organisation may influence both the propensity for amicability and hippocampus volume [39].
The amygdala is one of the brain regions regulating social behaviour (reviewed in [40]) and social investigation [41]. C57BL/6J male lab mice that have undergone amygdala lesioning do not demonstrate intermale aggression [42], while rats with amygdala lesions demonstrate reduced social investigation [41]. Studies of oxytocin knock-out mice (which naturally have impaired social recognition abilities) have found that treatments of oxytocin into the medial amygdala prior to social encounters facilitate social recognition during the initial encounter [43]. Likewise, amygdala volume correlates positively with social network size in humans [44]. Thus, group-living taxa may exhibit larger amygdala volumes than solitary taxa as a result of increased social recognition requirements [43].
To assess the relationship between regional brain volume and behaviour requires a study model that differs in sociality and habitat types. The genus Rhabdomys is such an appropriate model because taxa within the genus occur in different habitats (from mesic grasslands to arid semi-desert), differ in sociality (solitary-living vs. group-living), and possibly experience different selection pressures [1]. The striped mouse Rhabdomys is a small (weighing approximately 40–50 g), diurnal murid rodent, with a widespread geographic distribution across southern Africa and the montane regions of East Africa [45]. Four sister species (R. pumilio, R. bechuanae, R. intermedius and R. dilectus) have been proposed within the genus based on genetic studies [46], [47], [48]. There are two cytotypes within R. dilectus, R. dilectus dilectus (2 n = 46) and R. dilectus chakae (2 n = 48) [46], [49], [50]. However, these distinctions are putative, with taxonomic revision still ongoing. Rhabdomys pumilio has a western distribution, occurring along the arid west coast of South Africa, and R. dilectus occurs in the more mesic eastern part of South Africa. Rhabdomys is omnivorous, although its diet composition varies seasonally and according to geographic location. For instance, R. pumilio in the semi-desert Succulent Karoo consumes largely shrubs and succulents for most of the year, but in spring, prefers protein-rich foods such as insects, the new-growth of plants and wildflowers [51]. The mesic grassland/savanna R. dilectus consumes berries, seeds, and herbs, with its diet in the spring/summer consisting of seeds and insects [51].
For R. pumilio, food is more clumped in the Succulent Karoo than it is for R. dilectus in the grasslands [51], and hence home ranges of R. dilectus are six times larger for females and 10 times larger for males than for R. pumilio [52]. Rhabdomys pumilio in the Succulent Karoo is facultatively group-living, related to changes in population densities and the availability of limited nesting sites [53]. Groups consist of a single reproductive male, 2–4 breeding females, and their juvenile and non-breeding subadult offspring [52]. When population density decreases, groups can disband and both sexes can live alone [53]. However, this is not the case for R. dilectus, which is solitary and territorial in the mesic grasslands, with territories of males overlapping with those of several females [10]. Previous studies of spatial cognition in striped mice using a Barnes maze have shown that males from a semi-desert population responded faster and made fewer mistakes in winter than in summer [54], whereas a comparative study found no differences in spatial memory between sister taxa or the sexes (R. pumilio, R. bechuanae and R. d. dilectus) [12]. Given differences in the environments in which these taxa occur, spatial memory performance may be expected to differ within these taxa when the memory load is greater.
We investigated spatial navigation, memory and sociability in 36 individuals each of three taxa: the semi-desert occurring R. pumilio and the mesic occurring R. d. dilectus and R. d. chakae. We then correlated amygdala and hippocampus volume and the spatial cognitive memory and sociability in the taxa. We made 5 predictions. 1) Compared to R. pumilio, R. d. dilectus and R. d. chakae would make fewer navigation errors and locate the exit tunnel faster in a Barnes maze because of their larger home range sizes and the more complex environment they occupy. 2) The group-living R. pumilio would be more sociable than both R. dilectus subspecies which are solitary. 3) R. pumilio would have larger amygdala volumes than both R. dilectus subspecies because of being group-living, whereas both R. d. dilectus and R. d. chakae would have larger hippocampus volumes than R. pumilio due to the greater memory requirements associated with larger home ranges and more complex environments. 4) Hippocampus volume would be related to spatial memory with individuals with larger hippocampal volumes making fewer errors and having shorter latencies. 5) There would be a positive relationship between region volume (both amygdala and hippocampus) and amicability, particularly in the group-living R. pumilio.
Section snippets
Study animals
We used R. dilectus chakae (from Suikerbosrand Nature Reserve in Gauteng, 26°29’1” S, 28°13’45” E), R. dilectus dilectus (from Irene in Gauteng, 25°53’59” S, 28°12’51” E), and R. pumilio (from Goegap Nature Reserve in the Northern Cape, 29°40’53” S, 17°58’9” E; Fig. 1). Wild-caught individuals from each locality were bred in the laboratory and six adult males and six adult females from the F2 and F3 generations of each taxon were used to investigate the relationship between behaviour and brain
Amygdala and hippocampus volume
Taxon (F2,31 = 25.21, p < 0.001) and sex (F1,31 = 3.41, p = 0.022) were significant predictors of amygdala volume. R. pumilio had a significantly larger amygdala volume than R. d. dilectus and R. d. chakae (Fig. 2A) and males had larger amygdala volumes than females (Fig. 2B). The taxon*sex interaction (F2,31 = 0.60, p = 0.557) and total brain volume (F1,31 = 1.21, p = 0.071) were not significant predictors of amygdala volume.
Taxon (F2,31 = 13.20, p < 0.001) was a significant predictor of
Discussion
We investigated spatial memory and sociability in three Rhabdomys taxa originating from different environments, and the correlates of hippocampus and amygdala volume with spatial memory and sociability. We found that the arid-occurring R. pumilio made fewer errors and had shorter latencies before encountering the escape hole in the Barnes maze than both grassland-occurring R. d. dilectus and R. d. chakae. In addition, R. pumilio was more amicable, and had larger amygdala and hippocampus volumes
Funding
Funding was obtained from the National Research Foundation, South Africa (grant number 117920) and the University of the Witwatersrand, South Africa on the basis of publication.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
The authors wish to thank Dr Megan Mackay for commenting on an earlier version of the manuscript.
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