Abstract
Daily life of wild mammals is characterized by a multitude of attractive and aversive stimuli. The hippocampus processes complex polymodal information associated with such stimuli and mediates adequate behavioral responses. How newly generated hippocampal neurons in wild animals contribute to hippocampal function is still a subject of debate. Here, we test the relationship between adult hippocampal neurogenesis (AHN) and habitat types. To this end, we compare wild Muridae species of southern Africa [Namaqua rock mouse (Micaelamys namaquensis), red veld rat (Aethomys chrysophilus), highveld gerbil (Tatera brantsii), and spiny mouse (Acomys spinosissimus)] with data from wild European Muridae [long-tailed wood mice (Apodemus sylvaticus), pygmy field mice (Apodemus microps), yellow-necked wood mice (Apodemus flavicollis), and house mice (Mus musculus domesticus)] from previous studies. The pattern of neurogenesis, expressed in normalized numbers of Ki67- and Doublecortin(DCX)-positive cells to total granule cells (GCs), is similar for the species from a southern African habitat. However, we found low proliferation, but high neuronal differentiation in rodents from the southern African habitat compared to rodents from the European environment. Within the African rodents, we observe additional regulatory and morphological traits in the hippocampus. Namaqua rock mice with previous pregnancies showed lower AHN compared to males and nulliparous females. The phylogenetically closely related species (Namaqua rock mouse and red veld rat) show a CA4, which is not usually observed in murine rodents. The specific features of the southern environment that may be associated with the high number of young neurons in African rodents still remain to be elucidated. This study provides the first evidence that a habitat can shape adult neurogenesis in rodents across phylogenetic groups.
Highlights
Adult hippocampal neurogenesis (AHN) in wild living mammals shows large species-specific variation
This unexpected high number of granule cells (GCs) was verified by an independent second investigator, yielding results within 10% of the original estimate, i.e., within the margin of error defined by the Coefficient of Error (CE) estimates
AHN in laboratory rodents is affected by a multitude of factors, and it is surprisingly easy to increase or decrease the number of dividing or differentiating cells in laboratory rodents
Summary
Adult hippocampal neurogenesis (AHN) in wild living mammals shows large species-specific variation. It can either be absent as in bats (Amrein et al, 2007), or exceptionally high as in red foxes (Amrein and Slomianka, 2010). All wild rodents that have been studied show AHN to various degrees [for a review see Amrein et al (2011)], but no common behavioral, ecological, or taxonomic feature has been identified that can explain the variation between species. Spatial orientation requirements have been suggested to depend on AHN, as territory size in wild rodents correlates with proliferation (Amrein et al, 2004b). The idea that behavioral flexibility may depend on and express itself in the form of AHN (Garthe et al, 2009; Amrein et al, 2011) has been interpreted as a means for the ontogenetic and phylogenetic adaption to changing habitats (Kempermann, 2012)
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