Habitat-specific shaping of proliferation and neuronal differentiation in adult hippocampal neurogenesis of wild rodents

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.

Adult Hippocampal Neurogenesis in Natural Populations of Mammals

“…Within the surface-dwelling rodents, the South African species from an environmental challenging habitat form their own cluster. (Data from Amrein et al 2011Amrein et al , 2014Cavegn et al 2013. ) …”

“…Epp et al (2009) have used eye lens weights, assessed in both wild rats and laboratory conspecifics of known age, for age estimation. Barker et al (2003) and Cavegn et al (2013) combined lens weight with age-dependent structural changes in the number of adhesion lines in the circumferential lamellae of the femur. Even if it may not be possible to arrive at an exact absolute age that would allow direct comparison with laboratory-raised animals, it is at least possible to age wild animals relative to each other in a rather precise manner.…”

Adult neurogenesis in the mammalian hippocampus: Why the dentate gyrus?

“…Despite this ubiquity, however, neurogenesis in the adult hippocampus varies widely across species, with differences apparent in the rate of proliferation, survival, and neuronal maturation (for example, Cavegn et al 2013). The process appears absent in certain bat species (Amrein et al 2007), whereas especially high levels are found in rodents, especially rats (Amrein et al 2011).…”

Trading new neurons for status: Adult hippocampal neurogenesis in eusocial Damaraland mole-rats

“…For example in chickadees, the results indicate that populations that live in harsher environmental conditions show increased neurogenesis (Chancellor et al, 2011). In rodents, a different approach has been followed where various species from diverse habitats were compared, and once again rodents species resident in more challenging environments show higher neurogenesis (Cavegn et al, 2013). Compared to these surface dwelling rodents, mole-rats have the lowest level of neurogenesis (Amrein et al, 2014, Penz et al, 2015.…”

“…These differences appear to be largely dependent on hormonal variations (Marques et al, 2016). The precise functional significance of adult hippocampal neurogenesis is still a matter of debate, however evidence suggests that newly born neurons may have a more general function by contributing to behavioural flexibility in both wild and laboratory rodents (Garthe et al, 2009, Cavegn et al, 2013 by modulating the animal's reaction to novelty (van Dijk et al, 2015).…”