Colony size explains the lifespan differences between queens and workers in eusocial Hymenoptera

Abstract

Eusocial Hymenoptera show a unique divergence in lifespan of queens and workers; queens belong to the longest lived insects while workers in most eusocial species have significantly shorter lives. The different phenotypes within a colony emerge through reproductive division of labour, which is a characteristic trait of eusocial animals. Division of labour as a measure of organismal complexity increases with colony size in eusocial species similar to the increase of complexity with size that has been shown for the whole range of living organisms. We show that queen and worker lifespan diverge in closely related species representing the transition from solitary to social life and show that queen and worker lifespan are correlated if colony size is taken into account: with increasing colony size the lifespan differential between queen and worker increases, whereas neither queen nor worker lifespan is associated with colony size. Additionally, the lifespan differential is better explained by colony size than by the weight differences between the castes. The divergence of phenotypes found is in line with the increasing specialization of subunits in larger organisms, which leads to increasing complexity. We argue that division of labour is acting to increase colony efficiency, which in turn shapes the investments made into individuals leading to short‐lived workers and long‐lived queens. Additionally, maintenance investments may be shaped due to the variable extrinsic risk faced by different castes. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 710–724.

An Organismal Perspective on the Evolution of Insect Societies

“…This is especially clear in monogynous species where queen life span equals colony life span (Keller and Genoud, 1997), and within organism conflict is small, as expected from a system that has gone through a transition toward superorganismality already. Furthermore, the life span divergence between queens and workers increases with colony size (Kramer and Schaible, 2013; although polygyny or dependent colony founding may reverse this trend (Keller and Genoud, 1997;Schrempf et al, 2011;Boomsma et al, 2014), presumably reflecting the fact that larger colonies are usually more complex, have resolved many of the conflicts associated with genetic diversity within colonies, and are thus more advanced in the extent of the evolutionary transition in individuality.…”

Worker senescence and the sociobiology of aging in ants

“…Queens may live up to 45 years in the laboratory or field (Keeler 1993; Keller 1998), and the lifespans of reproductives are more than an order of magnitude greater than those of related taxa (Ridley 1993). Prominent in ant caste polyphenisms are sterile workers that may show task-related survival risk, and in sharp contrast to the longevity of queens, live only weeks to months (Kramer and Schaible 2013), illustrating remarkable aging plasticity specified by a single genome (Fjerdingstad and Crozier 2006). Extensive variation in life-history characteristics, colony size and social organization in ants provide opportunities to explore how differences in extrinsic mortality and social structure have led to the evolution of lifespan variation between and within morphological castes.…”

Ageing and somatic maintenance in social insects

“…Queens (the reproductive caste) have been recorded to live as long as 29 years [2], making them the longest-lived adult insects that we know of. Workers (which engage in nest maintenance and brood care) are substantially less long-lived [3] even in laboratory conditions where they are protected from extrinsic sources of mortality such as predation. Furthermore, variation in lifespan also exists among worker castes that specialise in different tasks [4,5].…”