Inquiline social parasites as tools to unlock the secrets of insect sociality

Abstract

Insect societies play a crucial role in the functioning of most ecosystems and have fascinated both scientists and the lay public for centuries. Despite the long history of study, we are still far from understanding how insect societies have evolved and how social cohesion in their colonies is maintained. Here we suggest inquiline social parasites of insect societies as an under-exploited experimental tool for understanding sociality. We draw on examples from obligate inquiline (permanent) social parasites in wasps, ants and bees to illustrate how these parasites may allow us to better understand societies and learn more about the evolution and functioning of insect societies. We highlight three main features of these social parasite–host systems—namely, close phylogenetic relationships, strong selective pressures arising from coevolution and multiple independent origins—that make inquiline social parasites particularly suited for this aim; we propose a conceptual comparative framework that considers trait losses, gains and modifications in social parasite–host systems. We give examples of how this framework can reveal the more elusive secrets of sociality by focusing on two cornerstones of sociality: communication and reproductive division of labour. Together with social parasites in other taxonomic groups, such as cuckoos in birds, social parasitism has a great potential to reveal the mechanisms and evolution of complex social groups. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.

The coevolutionary biology of brood parasitism: a call for integration

“…Riehl & Feeney [14] Cohen et al [18] Cini et al [22] Gloag & Beekman [30] Cotter et al [24] Suhonen et al [64] McClelland et al [76] Medina & Langmore [77] How readily can parasites switch hosts? Are the outcomes of coevolutionary arms' races predictable?…”

“…both common cuckoos and cuckoo wasps time parasitism events for when hosts are less likely to be active at the nest, see [24], this issue) or by avoiding recognition if detected (e.g. many insect brood parasites rely on acquiring chemical signatures of their hosts to reduce aggression; see reviews in this issue [22][23][24]). Understanding which adaptations arise requires knowledge of reciprocal adaptations in host defence, as these alter and determine the strength of selection acting on brood parasites (e.g.…”

Defences against brood parasites from a social immunity perspective

“…There is a comparable range of fitness costs associated with brood parasites in non-avian systems. For example, inquiline social parasites of social hymenopteran colonies can completely replace the colony queen prior to the production of reproductives, thus reducing her LRS to zero [18], which is more extreme than even the most virulent avian brood parasites [16]. Other parasites are less virulent, typically reducing the overall success of the brood, but not destroying it completely, for example the cuckoo fungus in termites, Fibularhizoctonia sp.…”

Behavioural and neurogenomic responses of host workers to social parasite invasion in a social insect

“…their brood care, nest building and food supplies (Wilson 1971). Many of the social parasites that specialise in exploiting the social Hymenoptera (bees, wasps and ants) evolved from a social ancestor (Lowe et al 2002): social parasites are widespread in ants (Hölldobler and Wilson 1990), allodapine bees (Smith et al 2013), honeybees and bumblebees (Lhomme and Hines 2018) and wasps (Cervo 2006;Cini et al 2019b). As parasites strive (in evolutionary terms) to be better exploiters of their social hosts, hosts respond by evolving strategies to reduce the chance and costs of invasion, leading to a coevolutionary arms race between the two species, and dramatically shaping their morphologies, behaviours and other life-history traits (Dawkins and Krebs 1979).…”