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Report

Teaser, summary, work performed and final results

Periodic Reporting for period 1 - SocParPhenoEvol (Insect social parasites: behavioural genomics models for understanding the basis of phenotypic evolution)

Teaser

Summary

Understanding how diversity of life, from form to behavior, arises at the level of the genes is one of the biggest challenges in modern biology. A single genome can produce phenotypes so contrasting that they can be mistaken as different species; for example a worker ant can be 20 times smaller than its mother queen, and exhibits specialized morphologies to help it defend its colony. Equally, the same genome enables an individual to be resilient to changes in its environment, expressing different behaviours and/or morphologies in response to dynamic demands of its environment or life-history. This is an exciting time for biologists, as advances in genomic methodologies now allow us to dissect the molecular basis of such phenotypic diversity and plasticity across a range of organisms, from genes to phenotypes. However, natural selection operates directly on phenotypes and only indirectly on the molecular machinery. We lack an integrated study of key phenotypic traits and their dynamic changes in an ecologically relevant setting, with the associated dynamic nature of the underpinning genes. The aim of the SocParPhenoEvol project was to understand how genes give rise to phenotypic traits and the dynamic plasticity required to assure fitness for individuals in the natural environment. The project used an inter-disciplinary approach, by uniting classical ethology with new molecular tools of genomics, and focused on insect social parasites (species that exploit the resources and parental care of a eusocial insect society) and their social hosts. Social parasites represent an ideal model system for determining the molecular basis of phenotypic evolution, as they allow comparisons of related species which have evolved mutually exclusive traits and/or life histories. 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.

Work performed

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.

Final results

Overall, the project allowed to support the importance of social parasites as model system to understand how diversity of life, from form to behavior, arises at the level of the genes. In addition to the conceptual framework and the generation oa large dataset of comparative brain transcriptomic data to test the conceptual model predictions, the project also allowed to document specific adaptations of social parasitism, in particular how social parasites intercept host communication code, by experimentally demonstrating the importance of visual and vibrational communication in paper wasps (Pepiciello, Cini et al., 2018: Cini et al. submitted). Moreover, I extended the research on social parasitism beyond the model system and included an unrelated group of primitively social wasps (Stenogastrinae), where an interesting case of intraspecific social parasitism has been documented. Finally, the project included significant outreach activity. Indeed, despite their important role in ecosystems, wasps are among the least loved insects. During the project I investigated the roots of this negative perception and provided a draft agenda to overcome these negative attitude (Sumner et al 2019). I also championed hornets in a very participated dissemination initiative led by The Wellcome Sanger institute, thus raising public attention on the importance of wasps in our ecosystems.