Abstract
The evolution of eusociality in social insects, such as termites, ants, and some bees and wasps, has been regarded as a major evolutionary transition (MET). Yet, there is some debate whether all species qualify. Here, we argue that worker sterility is a decisive criterion to determine whether species have passed a MET (= superorganisms), or not. When workers are sterile, reproductive interests align among group members as individual fitness is transferred to the colony level. Division of labour among cooperating units is a major driver that favours the evolution of METs across all biological scales. Many METs are characterised by a differentiation into reproductive versus maintenance functions. In social insects, the queen specialises on reproduction while workers take over maintenance functions such as food provisioning. Such division of labour allows specialisation and it reshapes life history trade-offs among cooperating units. For instance, individuals within colonies of social insects can overcome the omnipresent fecundity/longevity trade-off, which limits reproductive success in organisms, when increased fecundity shortens lifespan. Social insect queens (particularly in superorganismal species) can reach adult lifespans of several decades and are among the most fecund terrestrial animals. The resulting enormous reproductive output may contribute to explain why some genera of social insects became so successful. Indeed, superorganismal ant lineages have more species than those that have not passed a MET. We conclude that the release from life history constraints at the individual level is a important, yet understudied, factor across METs to explain their evolutionary success.
Highlights
Life on earth has evolved through rare but large steps called major evolutionary transitions (METs; Maynard Smith and Szathmáry, 1995; Michod, 1997; Bourke, 2011; West et al, 2015)
We highlight the importance of division of labour and specialisation among lower-level units in overcoming life history trade-offs as potential drivers toward METs
Our definition of a MET in social insects differs from existing definitions (e.g., Helanterä, 2016; Boomsma and Gawne, 2018; Bourke, 2019) and it apparently seems to align with former ones (e.g., Wheeler, 1911; Wells et al, 1929; Buss, 1987; Hölldobler and Wilson, 2009)
Summary
Life on earth has evolved through rare but large steps called major evolutionary transitions (METs; Maynard Smith and Szathmáry, 1995; Michod, 1997; Bourke, 2011; West et al, 2015). Conflict over reproduction among group members is absent as reproductive interests are aligned Based on this consideration, we highlight the importance of division of labour and specialisation among lower-level units in overcoming life history trade-offs as potential drivers toward METs. Three steps characterise a MET (e.g., Bourke, 2011; Korb and Heinze, 2016 for details). In the case of social insects (or more broadly, all fraternal associations), indirect fitness benefits derived from helping relatives are of major importance (e.g., Korb and Heinze, 2004; Foster et al, 2006; Boomsma, 2009; Abbot et al, 2011) They facilitate stable maintenance of associations, and potential selection against cheating, for instance through the evolution of self-restraint (e.g., Frank, 1998; Ratnieks et al, 2006 and references therein). They might contribute to explain the ecological and evolutionary success of social insects
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