Unusual occurrence of domestication syndrome amongst African mole-rats: Is the naked mole-rat a domestic animal?

Abstract

The Naked mole-rat (NMR) is becoming a prominent model organism due to its peculiar traits, such as eusociality, extreme longevity, cancer resistance, and reduced pain sensitivity. It belongs to the African mole-rats (AMR), a family of subterranean rodents that includes solitary, cooperative breeding and eusocial species. We identified and quantified the domestication syndrome (DS) across AMR, a set of morphological and behavioural traits significantly more common and pronounced amongst domesticated animals than in their wild counterparts. Surprisingly, the NMR shows apparent DS traits when compared to the solitary AMR. Animals can self-domesticate when a reduction of the fear response is naturally selected, such as in islands with no predators, or to improve the group’s harmony in cooperative breeding species. The DS may be caused by alterations in the physiology of the neural crest cells (NCC), a transient population of cells that generate a full range of tissues during development. The NCC contribute to organs responsible for transmitting the fear response and various other tissues, including craniofacial bones. Therefore, mutations affecting the NCC can manifest as behavioural and morphological alterations in many structures across the body, as seen in neurocristopathies. We observed that all social AMRs are chisel-tooth diggers, an adaption to hard soils that requires the flattening of the skull. We hypothesise that chisel-tooth digging could impose a selective pressure on the NCC that triggered the DS’s appearance, possibly facilitating the evolution of sociality. Finally, we discuss how DS traits are neutral or beneficial for the subterranean niche, strategies to test this hypothesis and report well-studied mutations in the NMR that are associated with the NCC physiology or with the control of the fear response. In conclusion, we argue that many of the NMR’s unconventional traits are compatible with the DS and provide a hypothesis about its origins. Our model proposes a novel avenue to enhance the understanding of the extraordinary biology of the NMR.