PUBLIC GOODS AND SOCIALLY RESPONSIVE FEMALES

Why and how animals cooperate with each other remains a fascinating challenge to explain. We know that individuals within families or that regularly interact with each other are far more likely to gain reciprocal benefits from cooperating with each other. However, there are many examples across the animal kingdom where these conditions don't hold and where cooperation is observed in situations in which it isn't predicted.

We have recently uncovered such an example in our studies of the social responses of fruitflies. They don't live in familial or social groups, which predicts that they should be very unlikely to express socially cooperative behaviour. Nevertheless, we have found that females have remarkably fine-tuned responses to their social environments. For example, when they detect the presence of other females they very rapidly increase their rate of egg laying and alter their sexual receptivity. Eggs laid by groups of females that meet on food substrates females are laid together in clumps together with those of other females and, unexpectedly, these eggs seem to benefit from the cooperative protection offered by the eggs of other females.

Laying eggs in communal batches seems to be beneficial because eggs are laid with an antimicrobial and anticannibalism 'coating': this diffuses and prevents spoilage of the substrate on which the eggs are laid, and prevents eggs from being eaten by any larvae that are present. The defensive coating protects batches of eggs (and resulting larvae) on a food patch. However, the production of these antimicrobial and anticannibalistic chemicals is energetically costly and potentially open to exploitation by others. This is because, if some individuals lay 'defenceless' eggs next to those with a strong antimicrobial coat or with effective anti-cannibalism defences, they can benefit without paying costs and hence can 'free-ride' the system. The explanation for what prevents most individuals from cheating like this resides in a powerful body of theory concerning 'public goods'. Key to the explanation is whether the benefits of producing public goods (i.e. the antimicrobial and anti-cannibalism defences) are 'non linear', for example if the only way everyone can benefit is if a threshold number of cooperating individuals pitch in.

The aim of our project is to measure how and why cooperation over public goods occurs in our test system, and hence test the predictions of this important theory. Using the power of the fruitfly system, we can do this by experimentally manipulating the whole system, from the sensory inputs, to the production of public goods themselves, to the outcome in terms of the reproductive output of individual females.

We will investigate:

(1) The nature of benefits to females from responding to social environments through the production of public goods such as antimicrobial and anti-cannibalistic chemicals.
(2) The shape of the relationship between the production of public goods and fitness.
(3) The gene regulatory mechanisms underlying the production of socially responsive public goods.

The results of this programme will provide a significant step forward in our understanding of fundamental components of social biology. These principles will have broad impact across taxa and will help to show us how and why we behave as we do.

The proposed work is expected to generate significant impacts - we describe below who will benefit and the mechanisms in place to show how that impact will be achieved.

1. NOVEL METHODS OF INSECT CONTROL. The proposed work is relevant to the potential for understanding, manipulating and improving the sexual performance of mass-reared insects subject to mass release programmes for genetic control. Our data will highlight mechanisms by which individuals can respond their environments and identify new candidate loci that could be manipulated for a novel type of insect control via manipulation of public goods production. We have strong links with the applied insect research community (PI in PhD projects with Oxitec, Pirbright and Ecospray Ltd). To elaborate: the PI has previously held 2 NERC iCASE PhD studentships with Oxford Insect technologies (Oxitec Ltd), two more CASE studentships started in Oct 2015 (Institute of Animal Health and a further industry-funded PhD studentship with Oxitec). Oxitec were also a Project Partner on a BBSRC grant BB/K000489/1. These active, ongoing relationships have cemented relevant industry contacts and have built strong research links to the applied community.

2. DISSEMINATION OF FUNDAMENTAL SCIENCE ACROSS ACADEMIC AND PUBLIC DOMAINS: A wealth of data on the different facets of cooperation theory, plasticity and social responses in different environments will be generated. These data are expected to be the springboard for further future studies by us and by other researchers. These impacts will be delivered by the whole team through published papers, press releases, science blogs, twitter, conferences and reports. Public dissemination will be achieved through the whole team via the diverse outreach and engagement activities specified in the Pathways plan. Collectively we have a strong record in such activities (local and national public exhibitions such as at the Royal Society, Norwich Forum, Norwich and Leeds Science Festivals, Leeds 'Be Curious', Sainsbury Centre for Visual Arts, blogging and twitter). We see several possibilities for research outcomes to gain the attention of a broad audience, to increase awareness of social biology in general:

(i) Sexual plasticity: there are strong potential impacts arising from understanding basic processes such as who responds to whom and why. This impact will be disseminated to researchers in this field using the research expertise and research links of the whole team.

(ii) Cooperative behaviour: ultimately we wish to understand the role of plasticity in females in contributing to the persistence of socially cooperative behaviour - in this project we will also identify the underpinning processes. This information should prove important in terms of both public impact and further research in this area, especially given the opportunity to manipulate different sets of genes in order to start to probe causality. Theory suggests that the key information is the shape of fitness benefits as a function of public goods production. Our experiments will yield important key data to test this theory. The PI, PDRAs and Co-Is will drive this potential impact through public exhibitions and talks.

(iii) Variation in social plasticity: we will gain much needed information on differences in female responses to their environments. This impact is expected to be realised in the public domain through its intrinsic interest and via our mechanisms for engagement.