The specific aims of the projects were the development of the a conceptual framework for the understanding of the evolutionary origin of phenotypic variation using the evolution of social parasitism from a social ancestor and the test of the conceptual model predictions through the generation of comparative behavioral and transcriptomic data.
Insect social parasites have been identified as unique models for understanding the molecular basis of phenotypic plasticity, as they evolve from social host lineages through losses (and/or reduction) of many social traits and gains (and/or augmentation) of specialist parasite traits. Moreover, the repeated evolution of social parasitism in many insect lineages and the large diversity of host-parasite systems in the Hymenoptera provides a powerful comparative approach. Yet, they have remained largely unexploited until now, due to a relative lack of appreciation of their usefulness and the difficulty of conducting genomic studies on non-model organisms. To fill this knowledge and appreciation gap, in the project I developed a conceptual comparative framework that considers trait loss, gains and modifications in parasite-host systems, in order to use inquiline social parasite as tools to better understand phenotypic evolution. We also provided empirical examples of how this simple framework provides complementary hypotheses to test, by focusing on two cornerstones of sociality: reproductive division of labour and communication (Cini et al., 2019 Philosophical Transaction Roy. Soc. B. fig.1). This project clearly provided evidence of the potential of social parasites as tools in this respect. Although we focus on inquilines, there is huge potential to exploit other guises of social parasites of insects (from slave-makers to temporary facultative social parasites) as well as social parasites from across the animal kingdom (such as cuckoos in breeding birds), as tools to uncover the mechanisms of phenotypic evolution.
The few comparative transcriptomic studies of social parasites and host species attempted to date (on ants and bees) recently confirmed framework predictions, in that social parasites evolve via a combination of the predicted processes of loss, retention and gain. So far, however, research did not investigated social parasites of wasps nor it included sympatric, related non-host species. The project conducted was thus the first to perform such a study, by focusing on the paper wasp of the genus Polistes, which has recently emerged as a key genus for understanding the molecular basis of phenotypic plasticity and whose behavioural ecology is well known. For the second aim of the project, I combined detailed individual behavioral phenotyping with brain gene expression analyses of three species: Polistes sulcifer, which is an obligate parasite of eusocial paper wasps societies; its host and close relative P. dominula and a sympatrically occurring eusocial paper wasp which is not parasitized by P. sulcifer - P. nimphus. Field sampling and laboratory manipulation allowed to generated the first dataset on brain transcriptomics of a wasp social parasite-host model system, which will allow genome-wide assessment of the molecular processes underpinning the dynamics of phenotypic diversity in insect social parasites evolution.
