Dynamics and origins of socially induced plasticity of behaviour

Desert locusts are notorious insect pests that periodically devastate crops and pastures at considerable human and economic cost. Unlike other grasshoppers, locusts can reversibly change between two dramatically different forms, one of which is configured for a life in migratory swarms. This transformation, or Phase Change, is driven by large fluctuations in population density. At low population densities locusts occur in the Solitarious Phase, where they are cryptic in appearance and behaviour, and most importantly, actively avoid other locusts. When locusts are forced together, they transform into the Gregarious Phase. Gregarious locusts look very different and are highly active, but crucially are attracted towards other locusts so that they can eventually aggregate into swarms. The change from solitarious to gregarious behaviour takes just a few hours whereas physical changes take several generations. We have previously demonstrated that a surge in the brain chemical serotonin during the early stages of crowding triggers this rapid change in behaviour, although how it does so is unknown. Serotonin has similarly important roles in many other animals, including humans, where it is involved in the regulation of mood and aggression. We now seek to understand how serotonin sets phase change in train, and whether phase change has arisen from behavioural traits such boldness/shyness or activity/quiescence that define 'personality' differences in other animals. We wish to determine whether such basic traits have been co-opted during evolution into the process of phase change, thus explaining their common regulation through serotonin. We will examine this by contrasting locust strains that show differing propensity to change phase, and by contrasting closely related species that do not swarm at all.

Our research makes use of sophisticated automatic movement tracking systems to test the behaviours of locusts faced with different 'problems' such as moving to food across an open space or responding to a crowd of other locusts. We couple these analyses with biochemical techniques for measuring serotonin and other neurochemicals in the same animals, so we can begin to determine what governs the different and changing expressions of behaviour. We will use drugs (including some that are used in humans) to manipulate the serotonin pathway, and electrophysiological methods to record from particular serotonin-containing nerve cells that we suspect are critical to phase change. Our research will use a technique called fast scan cyclic voltammetry to measure the release of serotonin in ways that have not previously been possible in insects, and we will work with a new statistical software company to develop and use innovative analyses of behaviour. A core part of our work is to build on a number of international collaborations including one recently agreed with the Centre for Locust Control in Mauritania. Through these partnership we will gain access to wild locusts that provide an important contrast to the lab strains we already have. Research visits between the labs and field station will permit new insights for both teams of workers. The University of Leicester has recently invested more than £100k in a world-leading locust research facility to support our work.

The key outcomes of our work will be: (1) an increased understanding of the processes leading to the formation and dissipation of locust swarms, with potential applications to swarm control; (2) new insights into the evolution of phase change and its relationship to fundamental behavioural characteristics; (3) increased understanding of the biochemical pathways through which serotonin works, and of how these pathways can be co-opted into new behaviours; and (4) new international and commercial collaborations.

When faced with environmental change, animals can modify their behaviour across multiple traits in a coordinated fashion. Nevertheless there are bounds to such plasticity, and these differ between individuals and species. We will elucidate the neurochemical mechanisms that control the dynamics and limits of socially induced behavioural plasticity. Desert Locusts show extreme phenotypic plasticity in response to crowding or isolation, changing from a shy, cryptic 'solitarious phase' that avoids conspecifics, to a 'gregarious phase' that is actively attracted to other locusts. We will compare wild locusts from Mauritania with a lab strain, and with related non-swarming species that have lost phase change to different extents. We have previously identified serotonin (5HT) as the key neurochemical driving the initial transition from the solitarious to the gregarious phenotype. We will use electrophysiology, fast scan cyclic voltammetry and high performance liquid chromatography to address two fundamental questions about the neurochemical control of behaviour: (1) Do neuromodulators change their function according to behavioural state, which they themselves may regulate? and (2) Is the neuromodulatory release machinery itself subject to the plastic reconfigurations that it mediates? To infer behavioural state from movement trajectories, we will complement our existing statistical toolset with Bayesian hierarchical models with latent time-dependent states. We will investigate the role of 5HT and other neurochemicals in risk-taking and exploration, and relate this to phase state in the same individuals. This will test our hypothesis that phase change has evolved through the co-option of pre-existing behavioural syndromes that are common across many animal species, possibly by recruiting pleiotropic proximate mechanisms.

Our work is centred on understanding the mechanisms underpinning a fundamentally important aspect of all brain function called plasticity. This is the ability to change and adapt to new challenges through learning, remembering and forgetting. Primary beneficiaries of our research will be academic colleagues with cognate research programmes and the wider life science research community. The conceptual impact of our work is by no means limited to specialists, however: the national and international media coverage that our work has received testifies to the public fascination with locust swarms, and with the deep similarities in socially induced transformations across creatures as diverse as insects and humans (latest: BBC FOUR programme 'Metamorphosis: The Science of Change' 17 Mar 2013). In this way, the project will support the science media sector and further public engagement with science in the UK.

We approach the question of socially induced plasticity in one of the most notorious crop pests, the Desert Locust. In 2013 alone, the United Nations Food and Agriculture Organization (FAO) has issued Amber Light-Threat warnings for Sudan, Egypt, Saudi Arabia, Morocco and Israel; and a Yellow Light-Caution warning for Yemen (http://www.fao.org/ag/locusts/en/). The 2004/05 outbreak in West Africa affected many countries including Mauritania, Niger, Sudan, Senegal, Morocco and Tunisia, with locust control agencies applying pesticides to an area of 130,000 km2 at an estimated cost in excess of US$400 million (FAO). The disastrous effects on food security in West Africa went far beyond the monetary value of the lost crop (FAO estimate: up to US$2.5 billion). By elucidating the mechanisms controlling the propensity of locusts to form swarms, our work will influence pest control and food security in the countries affected and, through the scale of the threat, globally. The wider range of beneficiaries therefore includes those whose food is periodically devastated by swarms, government locust control agencies, and - in the very long term - third sector relief organisations through reduced need for food aid.

An immediate private enterprise beneficiary will be Openbrain, a University of Leicester spin-out who are developing a unique web-based Bayesian data modelling platform (letter from the Director enclosed). Openbrain was born out of a previous BBSRC-funded research project into locust neuroscience led by Matheson [BB/H002510/1]. Our new project will generate a large set of videos of locust behaviour in an arena and corresponding movement tracks (estimated 10,000 videos/tracks over the three years) that we will share with Openbrain. This will enable Openbrain to road-test their platform in a new application area while assisting us with our new analyses.

Our project will contribute directly to the BBSRC Strategic Goal of training skilled researchers, with immediate benefit for UK science and industry and the overseas science base. These transferable skills will centre on bringing together diverse technologies and concepts to solve complex problems that do not yield to a one-dimensional approach. Training will focus particularly on study design, analysis and statistical inference. We have a proven track record of hosting and training researchers from our collaborators' labs. Our development of an internationally important solitary locust research facility will create a long-term resource to support training of visiting researchers, including those from countries affected by locust swarms. By establishing functional links with institutions in these countries (e.g. Mauritania: Centre National de Lutte Antiacridienne), and through the sustained interactions that will follow, the project will facilitate the translation of lab-based knowledge into experimental work with greater relevance and impact in the field.