The relationship between individual phenotype and the division of labour in naked mole-rats: it’s complicated

Abstract

Background The naked mole-rat (Heterocephalus glaber) is among the most social mammals on the planet, living in eusocial groups of up to 300 individuals that contain a single reproductive female and up to three reproductive males. A critical aspect of their complex social system is the division of labour that allows non-breeders to form an effective workforce. Age- or weight-based polyethisms are widely cited as explanations for how labour is divided, but evidence in support of these hypotheses has been equivocal. Methods To assess the extent to which individual working behaviour is determined by sex, age, weight and social rank, we studied the behaviours of 103 animals from eight captive colonies. We performed focal sampling and ran mixed-effects models to assess which factors explained variation in working behaviour during six ten-minute observation periods per individual. Results Contrary to widely-held beliefs, we found that working behaviour did not decrease linearly with weight, although polynomial regressions indicated younger and medium-sized individuals worked most frequently, while high-ranking individuals worked for the shortest periods of time. Working behaviour and its relationship with individual characteristics also varied between colonies. Conclusions While age- or size-based polyethisms may have some influence on working behaviour, we argue that other characteristics of the individual and colony are also important. In particular, the interactions of individual, social and environmental factors must be considered in order to understand the emergence and effectiveness of the division of labour that is so critical to many social organisms.

Naked mole-rats (Heterocephalus glaber) do not specialise on cooperative tasks

“…Our data reveal that sex differences in work-related cooperative behaviour of naked mole-rats are minor and body mass and age-related patterns are broadly similar in male and female non-breeding individuals. This is consistent with previous studies (Jarvis et al 1991, Lacey and Sherman 1997, Gilbert et al 2020), and it is possible that as in other social mole-rats species, sex-differences are limited to allo-parental care behaviour which we were unable to record in this study (Bennett 1990, Zöttl et al 2016a, Thorley et al 2018, Zöttl et al 2018). The lack of sex-differences contrasts with the distribution of cooperative behaviours in many other cooperatively breeding species where sex differences are common and often linked to sex differences in philopatry (Clutton-Brock et al 2002).…”

“…Mole-rats within the genera Fukomys and Cryptomys show body size related changes in cooperative behaviour and individuals can vary widely in the frequency of burrowing behaviour (Bennett and Jarvis 1988, Bennett 1990, Burda 1990, Bennett 1992, Jarvis et al 1994, Spinks et al 1999, Scantlebury et al 2006). However, longitudinal studies of Damaraland mole-rats of known ages have shown that individuals do not trade-off investment in cooperative behaviours and that the general patterns of the distribution of cooperative behaviour across individuals are similar to those of naked mole-rats shown in this study (Zöttl et al 2016a, Thorley et al 2018, Zöttl et al 2018, Gilbert et al 2020). Evidence from field studies of other Fukomys species also supports the notion that the behavioural similarity of mole-rats societies with obligatorily eusocial insects has probably been overemphasized in the past and evidence for specialisation, divergent developmental trajectories or bimodal trait distributions across individuals are rare (Faulkes and Bennett 2016, Šklíba et al 2016, Zöttl et al 2016b, Van Daele et al 2019, Voigt et al 2019).…”

“…These studies inferred specialisation from size-related variation in cooperative behaviour by showing that burrowing, nest building and food carrying follow divergent size-dependent trends. However, the individuals were mostly of unknown age and it has been found that size and age-related differences may not necessarily be the result of specialisation, but instead are often consequences of the relative costs and benefits to individuals at different life stages (McNamara and Houston 1996, Faulkes and Bennett 2016, Zöttl et al 2016a, Gilbert et al 2020). The results of our study also represent a clear example where size and age-related variation can exist despite a positive correlation of engagement in different tasks within individuals.…”

“…Other studies suggested that variation in cooperative behaviour of naked mole-rats may instead represent temporary specialisation, similar to age-related polyethisms found in some social insects and that contrasts in behaviour may be explained by age-related changes of behaviour, where individuals pass through stages of development and conduct different tasks depending on their age (Lacey and Sherman 1991, Lacey and Sherman 1997, Faulkes and Bennett 2016). More recent studies have suggested that naked mole-rats show behavioural flexibility and that cooperative behaviour may be adjusted to the group composition and other social and environmental factors (Mooney et al 2015, Gilbert et al 2020). However, it remains unclear whether non-breeding naked mole-rats specialise temporarily on specific work-related behaviours, or whether individuals vary mostly in their overall commitment to cooperative behaviours (Thorley et al 2018, Braude et al 2021).…”

Long bone histomorphogenesis of the naked mole‐rat: Histodiversity and intraspecific variation

“…Subordinates are suppressed from releasing sex steroid hormones due to the antagonistic behavior of the queen, which results in delayed puberty and therefore individuals live under a hypogonadic condition (Pinto et al, 2010). Several studies on humans and laboratory rodents have revealed that hypogonadism results in suboptimal skeletal development and may lead to an increased risk of bone fractures later in life (Golden & Carlson, 2008;Pinto et al, 2010;Yingling & Taylor, 2008).…”