Behavioural and neurogenomic responses of host workers to social parasite invasion in a social insect
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Insectes Sociaux
RESEARCH ARTICLE
Behavioural and neurogenomic responses of host workers to social parasite invasion in a social insect A. Cini1,2 · R. Branconi3 · S. Patalano4 · R. Cervo2 · S. Sumner1 Received: 10 December 2019 / Revised: 7 March 2020 / Accepted: 20 April 2020 / Published online: 15 May 2020 © The Author(s) 2020
Abstract The strong coevolutionary arms race between social parasites and their hosts has dramatically shaped the life-history traits of both parties. One of the main strategies exhibited by hosts in response to parasitism is reproduction by host workers. We lack a mechanistic understanding of how these defence strategies unfold and, specifically, whether hosts exhibit more subtle strategies to reduce the costs of parasitism from the outset. Here we test the hypothesis that there are both behavioural and neurogenomic signatures of worker responses to parasitism, prior to overt expression in the form of egg-laying; we test this using the social parasite—social host system of the paper wasps Polistes sulcifer-Polistes dominula. We characterized individual workers’ position within the social interaction network of queenright and host colonies immediately after parasite usurpation, weeks before the workers’ reproductive rebellion is evident. Parasitism influenced network centrality measures, with workers in parasitized colonies showing increased connectedness and centrality compared to those in unparasitized ones. Next, we quantified brain gene expression levels for five genes related to physiological and behavioural phenotypes in Polistes wasps. The gene Imaginal disc growth factor (Idgf4), thought to be responsive to changes in the social environment, was significantly down-regulated in workers from parasitized colonies; this may be an indication that parasitized workers are anticipating a shift toward a less worker-like phenotype in preparation for their reproductive rebellion. Our results provide the first evidence of early behavioural and neurogenomic responses of host workers toward the presence of an inquiline social parasite in a social insect. Keywords Brood parasitism · Polistes sulcifer · Polistes dominula · Arms-race · Behavioural gene expression · Social network
Introduction
Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00040-020-00765-6) contains supplementary material, which is available to authorized users. * A. Cini [email protected] 1
Centre for Biodiversity and Environment Research, University College London, Gower Street, London WC1E 6BT, UK
2
Dipartimento di Biologia, Università degli Studi di Firenze, Via Madonna del Piano, 6, 50019 Sesto Fiorentino, Italy
3
Department of Biology, Boston University, 5 Cummington Mall, Boston, MA 02215, USA
4
Institute of Basic Biomedical Sciences (IBBS), B.S.R.C “Alexander Fleming”, Vari, Greece
For social insect colonies, the threat of invasion by social parasites is part of life. From beetles to butterflies, many species have evolved the ability to exploit the
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