Plasticity and constraints on social evolution in African mole-rats: ultimate and proximate factors

Abstract

Here, we review comparative studies of African mole-rats (family Bathyergidae) to explain how constraints acting at the ultimate (environmental) and proximate (organismal) levels have led to convergent gains and losses of sociality within this extensive adaptive radiation of subterranean rodents endemic to sub-Saharan Africa. At the ultimate level, living in environments that range from mesic through to arid has led to both variation and flexibility in social organization among species, culminating in the pinnacle of social evolution in the eusocial naked and Damaraland mole-rats ( Heterocephalus glaber and Fukomys damarensis ). The common mole-rat ( Cryptomys hottentotus ) provides a model example of how plasticity in social traits exists within a single species inhabiting areas with different ecological constraint. At the proximate level, reproductive strategies and cooperative breeding may be constrained by the correlated evolution of a suite of traits including physiological suppression of reproduction, the development of physiological and morphological castes, and the mode of ovulatory control and seasonality in breeding. Furthermore, recent neurobiological advances indicate that differential patterns of neurotransmitter expression within the forebrain may underpin (and limit) either a solitary or group living/cooperative lifestyle not only in mole-rats, but also more widely among disparate mammalian taxa.

Hamilton's rule and the causes of social evolution

“…African mole-rats (Bathyergidae) food patchiness, aridity and environmental uncertainty (in rainfall) promote sociality [82,83] rstb.royalsocietypublishing.org Phil. Trans.…”

Constraints and flexibility in mammalian social behaviour: introduction and synthesis

“…The contribution by Faulkes & Bennett [141] further illustrates how group-level variation and species differences in social behaviour (among mole rats) are constrained by particular patterns of neurotransmitter expression and physiological control of reproduction. As emphasized by Schradin [130], physiological mechanisms of social flexibility can differ in their temporal impact: neuronal mechanisms can lead to very quick and short-lasting responses, endocrine changes take longer but might also last longer, whereas neuroendocrine changes are predicted to be the slowest and longest-lasting mechanisms.…”

“…The failure of this verbal model to correctly explain or predict many patterns of mammalian social systems has been partly attributed to its primate bias [114]. However, Faulkes & Bennett [141] show that interspecific variation in mole rat social organization can be neatly linked to one environmental variable, in this case aridity. Ecological factors also explain variation in marmot social organization [142].…”

Distributed cognition and social brains: reductions in mushroom body investment accompanied the origins of sociality in wasps (Hymenoptera: Vespidae)

“…Positive correlations of brain region size and social complexity are found in diverse vertebrate taxa [7,[9][10][11], and social brain selection has been invoked as a factor in human brain evolution [12,13]. Vertebrate social groups often comprise associations of unrelated or distantly related individuals from the same generation (excepting mole rats [14]), and considerable opportunity exists for evolutionary conflicts of interest and within-group antagonism. The need to assess and respond to intra-group conflict (including formations of alliances) can be major determinant of cognitive capacity in social vertebrates; social brain theorists refer to this as Machiavellian intelligence [15].…”