Social wasps as models to study the major evolutionary transition to superorganismality

Abstract

The major evolutionary transition to superorganismality has taken place several times in the insects. Although there has been much consideration of the ultimate evolutionary explanations for superorganismality, we know relatively little about what proximate mechanisms constrain or promote this major transition. Here we propose that Vespid wasps represent an understudied, but potentially very useful, model system for studying the mechanisms underpinning superorganismality. We highlight how there is an abundance of behavioural data for many wasp species, confirming their utility in studies of social evolution; however, there is a sparsity of genomic data from which we can test proximate and ultimate hypotheses on this major evolutionary transition. Box 1: Glossary of termsSuperorganism: A concept proposed by Wheeler [1] to suggest that some social insect colonies represent an entirely new type of higher-level organism. The idea behind this is that irreversible caste differentiation in social insects is akin to the germline and soma split among cells of multicellular organisms. See [2] for full review.

Neotropical Social Wasps

“…Indeed, fully understanding the factors that drove the major evolutionary transition to a eusocial lifestyle is surely one of the most important outstanding questions in evolutionary biology today. Social wasps are an excellent model system to study this question (Taylor et al 2018). In fact, at an empirical level, research on primitively and facultatively eusocial wasps has given us some fantastic insights already, e.g., documenting direct fitness benefits of helping (Field et al 2000(Field et al , 2006(Field et al , 2008, which has been matched by similar findings in other taxa (Korb and Heinze 2016;Downing et al 2016), and showing how the evolution of helping behavior is subject to biological market theory (Grinsted and Field 2017b).…”

“…The detailed testing of some of these new models using comparative studies will remain an important task for the future. Lastly, much is yet to be unraveled about the genomic basis of social traits in wasps (Taylor et al 2018). With many full genomes of species of key phylogenetic placement and contrasting social structure expected to become available in the near future (Taylor et al 2018), the study of social wasps are expected to provide key insight in the genomic basis of a diverse set of traits, ranging from group living and altruistic behavior to reproductive plasticity, preimaginal caste differentiation, swarm founding, and queen-worker conflict over male parentage (Jandt and Toth 2015;Patalano et al 2015;Taylor et al 2018).…”

“…Lastly, much is yet to be unraveled about the genomic basis of social traits in wasps (Taylor et al 2018). With many full genomes of species of key phylogenetic placement and contrasting social structure expected to become available in the near future (Taylor et al 2018), the study of social wasps are expected to provide key insight in the genomic basis of a diverse set of traits, ranging from group living and altruistic behavior to reproductive plasticity, preimaginal caste differentiation, swarm founding, and queen-worker conflict over male parentage (Jandt and Toth 2015;Patalano et al 2015;Taylor et al 2018). Key questions that such data will be able to address is the extent to which sociality was built on novel genetic innovations (Ferreira et al 2013) as opposed to the mere repurposing of existing pathways (Hunt and Amdam 2005;Hunt et al 2007a) and how primitive and advanced eusocial systems, including queen-worker signaling systems and various conflict-resolving mechanisms, may have been built from preexisting traits in solitary ancestors (Johnson and Linksvayer 2010;Rehan and Toth 2015;Toth and Rehan 2017).…”

Genetic toolkit for sociality predicts castes across the spectrum of social complexity in wasps

“…Individual heads were stored in RNAlater for brain dissections; abdomens were removed and dissected to determine reproductive status. Ovary development was scored according to 31,61 and the presence/absence of sperm in the spermathecae was identified to determine insemination. Inseminated females with developed ovaries were scored as 'queens'; noninseminated females with undeveloped ovaries were scored as workers.…”

“…A promising group for exploring these questions are the social wasps 31 , with some 1,100 species exhibiting the full spectrum of sociality. We generated brain transcriptomic data of caste-specific phenotypes for nine species of social wasps, representing a range of levels of social complexity in the transition to superorganismality (Fig.…”