Evolutionary Shaping of Adult Hippocampal Neurogenesis in Mammals-Cognitive Gain or Developmental Priming of Personality Traits?

Adult hippocampal neurogenesis (AHN) in mammals peaks in early postnatal/juvenile periods and is strongly down-regulated thereafter. Depending on species, it may disappear rapidly in adult individuals, or persist at very low levels for a lifetime. Commonly, higher levels of AHN in mammals are thought to provide mental flexibility allowing for adapting to new ecological niches. But why does natural selection not prevent down-regulation of AHN, and why should a rudimentary proliferation rate in humans provide reproductive fitness even for aged individuals? The problem is compounded by species-specific behavioral manifestations of hippocampal functions that depend on brain size and ecological niches. Moreover, in laboratory rodents, proliferation levels of AHN and behavioral covariates appear unpredictable and context-sensitive. Conversely, one might ask why evolutionary mechanisms tolerate in nearly all mammals a certain level of early postnatal or subadult AHN. Specifically, the hypothesis of cognitive flexibility appears odd in species in which AHN is massively reduced in early infancy such as in humans. I suggest that early but not late AHN plays a hidden role in developing randomly different epigenetic personality traits in local populations. Such traits may counteract or enhance natural selection of the underlying genetic architecture-a process known as genetic assimilation. In mammals, protracted neurogenesis occurs in subventrical zones (SVZ) from which neuroblasts migrate rostrally to the olfactory bulb (rostral migratory stream, RMS) and from a secondary proliferation zone in the dentate gyrus, the subgranular zone (SGZ). The ongoing postnatal proliferation there is denoted as "adult" hippocampal neurogenesis (AHN). Molecular markers for migration and differentiation are often not correlated with basic levels of AHN in many species. For example, doublecortin (DCX) is a reasonable proxy for estimating proliferation rates in mice and rats. In other species such markers persist for long periods after the cessation of proliferation or appear even generated de novo (Amrein, 2015; Penz et al., 2015; Lipp and Bonfanti, 2016). Therefore, AHN and its potential relation to natural selection will refer here to simple proliferation only. After all, it is the dogma-breaking role of persisting neurogenesis that dominates the public view of AHN.