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

Abstract

Highlights• The hippocampal architecture of the Damaraland mole-rat corresponds largely to that of other mole-rat species.• No gender differences are found in hippocampal neurogenesis of Damaraland mole-rats.• Neurogenesis is unrelated to relative age in Damaraland mole-rats.• There is an inverse relationship between social status and neurogenesis in Damaraland mole-rats. 1 AbstractDiversity in social structures, from solitary to eusocial, is a prominent feature of subterranean African mole-rat species. Damaraland mole-rats are eusocial, they live in colonies that are characterized by a reproductive division of labour and a subdivision into castes based on physiology and behaviour. Damaraland mole-rats are exceptionally long lived and reproductive animals show delayed aging compared to non-reproductive animals. In the present study, we described the hippocampal architecture and the rate of hippocampal neurogenesis of wild derived, adult Damaraland mole-rats in relation to sex, relative age and social status or caste. Overall, Damaraland mole-rats were found to have a small hippocampus and low rates of neurogenesis. We found no correlation between neurogenesis and sex or relative age. Social status or caste were the most prominent modulator of neurogenesis. An inverse relationship between neurogenesis and social status was apparent, with queens displaying the lowest neurogenesis while the worker mole-rats had the most. As there is no natural progression from one caste to another, social status within a colony was relatively stable and is reflected in the level of neurogenesis. Our results correspond to those found in the naked mole-rat, and may reflect an evolutionary and environmentally conserved trait within social mole-rat species.

From Mice to Mole-Rats: Species-Specific Modulation of Adult Hippocampal Neurogenesis

“…Despite the low rate of neurogenesis, a status dependent amount of hippocampal neurogenesis is evident in the social Damaraland mole-rats. Seemingly in contrast with results from laboratory rodents, the breeding females, or queens, have lower numbers of both proliferating cells and young neurons compared to subordinate colony members (Oosthuizen and Amrein, 2016 ) (Figure 2 ). A similar occurrence is observed in the naked mole-rat, where breeding animals were found to have significantly less young neurons, as visualized by doublecortin (DCX) immunoreactive neurons, compared to the non-breeding animals (Peragine et al, 2014 ).…”

“…Morphologically, the dentate gyrus of mole-rats is comparatively smaller than that of other rodents, with fewer granule cells (Amrein et al, 2014 ). Mole-rats in general have very low levels of neurogenesis in the hippocampus (Amrein et al, 2014 ; Penz et al, 2015 ; Oosthuizen and Amrein, 2016 ). Normalized proliferating cell numbers of mole-rats are comparable with that of other rodents however the normalized young neurons are lower (Amrein et al, 2014 ).…”

“…obs. ], however both the Highveld and Damaraland mole-rats have more proliferating cells compared to Cape mole-rats (Ki67 staining) (Amrein et al, 2014 ; Oosthuizen and Amrein, 2016 ). The numbers of young neurons show large within species variation, thus young neuron numbers of the individual species show some overlap.…”

“… Scatter plots of relative age x body weight, total granule cells × relative age, and proliferation × young neurons in Damaraland mole-rats. (A) The body weight of Damaraland mole-rats does not increase with relative age, (B) total granule cells remains stable with relative age, and (C) a scatter plot of proliferating cells (Ki67) and young neurons (PSA-NCAM) in dominant and subordinate Damaraland mole-rats (Modified from (Oosthuizen and Amrein, 2016 ), with permission from Elsevier). …”

Adult mammalian neurogenesis and motivated behaviors

“…However, there are studies with contradictory findings. For example, in a eusocial animal, the Damaraland mole-rat (Cryptomys damarensis Ogilby, 1838), an inverse relationship between adult neurogenesis and social status was found (Oosthuizen & Amrein 2016). Specifically, queens (dominant animals) displayed the lowest level of adult neurogenesis, while the worker mole rats (subordinate animals) displayed the highest level of adult neurogenesis.…”