Locust and bee plasticity in a changing world

In a scientific process, models are developed with the objective of helping to answer a question. These questions can be related to fundamental science or on the contrary be applied to solve a real-world problem. Understanding better the behaviours of locusts and the repercussion of their high levels of plasticity on population dynamics have been the topics of multiple researches since the discovery of phase polyphenism by Sir Uvarov in 1921. In this context, ecological models are used to illustrate or combine hypotheses on locust behaviours, though rarely confronting multiple real-world observations to model predictions. On the other end, field data have been very often used to develop models to infer on locust population dynamics but rarely to develop applied tools that would help in the management context. With the help of several examples from works developed in the team of scientists during the last years, this talk will illustrate how they have tackled these two issues: 1- bringing multiple patterns into the representation of behavioural and population dynamics processes; 2- developing operational tools to help the field teams in charge of the preventive management of locusts. Finally, these studies illustrate the power of confronting multiple real-world patterns with models’ outcomes to make strong inferences and being more confident on the model’s reliability when answering key applied questions.

Co-authors: Marie-Pierre Chapuis, Esther Diouf, Jamila Dkhili, Saïd Ghaout, Fanny Herbillon, Amina Idrissi, Michel Lecoq, Lucile Marescot, Christine Meynard, Jean-Pierre Rossi, Camille Vernier. 

Dr Cyril Piou, CIRAD, France

Dr Cyril Piou, CIRAD, France

Cyril Piou received a PhD in ecology from the University of Bremen, Germany in 2007. He specialized into agent-based modelling in ecology and continued on the topic during two postdocs at the University of Dresden, Germany and at the French Research Agronomy Institute (INRA). He was hired by Cirad (French agricultural research and cooperation organization working for the sustainable development of tropical and Mediterranean regions) in 2010 as an ecological modeler in the locust team. Since then, Cyril has developed researches in partnership with Western and Northern African countries to study the ecology and management of Desert Locust. He spent 4 years (2013-2017) working on-site in the National anti-locust centre of Morocco. Since 2010, he supervised 6 PhDs, 4 Post-Docs and several other students and published 40 articles on locust ecology and management. He defended a Habilitation to conduct Researches at the University of Montpellier in 2022.

Flexibility in foraging behaviour allows animals to maximize foraging success in unpredictable environments. The desert locust Schistocerca gregaria exhibits an extreme example of behavioural flexibility. It is well documented that with increasing densities, locusts switch from avoiding conspecifics to approaching them, and from sedentary foraging to collective migrations. In this presentation, I will discuss our work on behavioural, sensory, and neural processes governing gregarious locust behaviour. I will start with a behavioural evaluation of locusts in natural and virtual group contexts, revealing a flexible behaviour that is shaped by the availability of food sources and conspecifics. In the context of marching, visual motion cues from conspecifics are sufficient to drive collective motion in gregarious locusts, while for foraging decisions, the integration of visual and olfactory cues is necessary. Calcium imaging from the primary olfactory centre (the antennal lobe) provides further clues into the mechanisms by which this is achieved. While the neural representation of social odours is similar in gregarious and solitarious locusts, the evaluation of food-related components in the presence of social odours is significantly enhanced in gregarious animals. We describe the antennal lobe components mediating this plasticity and how this can facilitate the detection of sparse food sources in crowded swarms.

Dr Einat Couzin-Fuchs, University of Konstanz, Germany

Dr Einat Couzin-Fuchs, University of Konstanz, Germany

Dr Einat Couzin-Fuchs is a Principal Investigator at the Centre for the Advanced Study of Collective Behaviour, University of Konstanz since 2018. Her training included a PhD in Neuroscience from Tel Aviv University and a postdoc in Mechanical Engineering at Princeton University. These introduced me to diverse concepts and techniques in insect neuroethology, which she now utilize and further develop to study the neural mechanisms of adaptive behaviour. Dr Couzin-Fuchs is fascinated by how the brain integrates noisy, probabilistic and multimodal information for appropriate decisions, especially in social contexts when decisions among individuals are coupled. By combining behavioural assays with 'real' and virtual social environments, as well as establishing tools and protocols for electrophysiology and functional imaging, her group delves into the sensory coding and interpretation of social stimuli. Their goal is to unravel neural mechanisms that allow animals (currently cockroaches and locusts) to flexibly adapt in changing social circumstances. 

The social insect colony has been described as a superorganism, or a factory-fortress. We might expect bee colonies with their stored resources, temperature regulation abilities, social immunity and defences to be particularly resistant to stress, and yet we have seen a worldwide doubling in honey bee colony failure rates in the last two decades. Here we discuss the interaction between the stress responses of individual bees and social stress responses. We propose that the social buffering of stress in a honey bee colony is effective in tolerating a level of chronic stress, but if the buffering capacity is exceeded a hive is vulnerable to rapid and catastrophic social decline. We present new work on how we might reliably detect an early warning that a bee colony is vulnerable to failure while there is still time to effectively intervene.

Professor Andrew Barron, Macquarie University, Australia

Professor Andrew Barron, Macquarie University, Australia

Professor of Comparative Neuroscience, Director of The Macquarie Minds and Intelligences Initiative at Macquarie University. Andrew Barron studies the evolution of cognitive systems. His research is currently supported by awards from the Templeton World Charity Foundation, The Australian Research Council and the Engineering and Physical Sciences Research Council of the United Kingdom. He has held fellowships from the Australian Research Council, the Leverhulme Trust, The Fulbright Commission and The Royal Society of London.

In insects, serotonin is a key neuromodulator that is linked with the regulation of many behaviours, including feeding, socialization, aggression, and mating. In locusts, an increase in serotonin levels in the brain is highly correlated with the solitary phase, whereas a serotonin spike in the thoracic ganglion is known to trigger the transformation of solitary animals into gregarious ones. It is also known that solitary and gregarious locusts have different behavioural responses to a variety of sensory cues including olfactory ones (for example, repulsion to conspecific odorants in the solitary phase must switch to attraction in the gregarious locusts). How such variations arise and the role of serotonin in achieving flexible neural-to-behavioural response mapping is not fully understood. I will present results from our recent study examining how serotonin modulates neural and behavioural responses to odorants in solitary and gregarious locusts (Schistocerca americana). I will explain how serotonin could enhance the olfactory sensitivity without compromising the robustness of odour recognition and present a simple model to explain how serotonin modulates odour-evoked neural and behavioural responses.

Professor Barani Raman, Washington University in St Louis, USA

Professor Barani Raman, Washington University in St Louis, USA

Barani Raman is a Professor in Department of Biomedical Engineering at Washington University. He received his Bachelor of Engineering in Computer Science with distinction from the University of Madras, and the M.S. and Ph.D. degrees in Computer Science from Texas A&M University, respectively. Following his doctoral studies, he became a joint postdoctoral fellow at the National Institutes of Health and the National Institute of Standards and Technology. He is the recipient of the 2011 Wolfgang Gopel Award from the International Society for Olfaction and Chemical Sensing. His research interests include sensory and systems neuroscience, sensor-based machine olfaction, machine learning, biomedical intelligent systems, and dynamical systems.

Phenotypic plasticity is determined by genetic and environmental factors, including social environment. However, organisms can also shape the environmental conditions they experience through their own behaviours. They will discuss examples where bees’ behaviours influence the social and nutritional environment that they experience, and thus determining their phenotypic outcomes. In the first set of examples, they will consider the genetic, nutritional, and social factors that influence reproductive division of labour in honey bees, and how intragenomic conflict between matrigenes and patrigenes modulates social preferences and ultimately phenotype. In the second set of examples, they will discuss how seasonal variation in floral resources may influence seasonal phenotypic plasticity in bees and potentially vice versa, and how these can be impacted by land use and climate change. Understanding how genes, behaviour, and the environment interact to shape phenotype requires detailed analyses in field-realistic conditions where individuals can freely interact with each other and their surroundings.  

Professor Christina Grozinger, Pennsylvania State University, USA

Professor Christina Grozinger, Pennsylvania State University, USA

Christina Grozinger is the Publius Vergilius Maro Professor of Entomology and the Director for the Centre for Pollinator Research at Penn State University. She is a Fellow of the Entomological Society of America and the American Association for the Advancement of Science. She was awarded the 2021 National Academy of Sciences Prize in Food and Agriculture Sciences and 2023 Penn State President’s Award for Excellence in Academic Integration.  Christina received her bachelor's degree in chemistry and biology at McGill University, her master's and doctoral degrees from Harvard University, and was a Beckman Institute Fellow at the University of Illinois, Urbana-Champaign. Grozinger uses an integrative approach – from genes to spatial ecology – to study bee behaviour and support management and conservation of bees.

Social insects provide an attractive model system for studying natural socially-regulated plasticity in circadian rhythms because task performance and the social environment influence the expression of circadian rhythms. We tested the influence of brood care behaviour and colony environment on the whole brain transcriptome in two highly social bee species showing different levels of social complexity. The Western honey bee Apis mellifera is highly social with perennial colonies containing tens of thousands of individuals, whereas colonies of the bumble bee Bombus terrestris are annual and contain up to a few hundred worker bees. We combined behavioural observations and time-series brain RNA sequencing to study the influence of the colony environment and brood tending on circadian gene expression. We sampled bees experiencing four different social environments: Foragers (colony, no brood care), nurses (colony + brood care), individually isolated ("solitary") worker bees (no colony or brood care), and solitary bees with brood (brood care, no colony environment). To identify circadian-regulated genes and molecular processes, we performed circadian analyses, multivariate analysis, WGCNA, and enrichment analyses. In both species, the canonical "clock genes" were cycling as found in previous studies, validating our experimental design and RNA sequencing procedures. As expected, in both species we found significantly more circadian-regulated genes in behaviourally rhythmic foragers and the lowest number of cycling transcripts in nurses that care for the brood around the clock. Surprisingly however, the solitary with brood group had the second highest number of circadian-regulated genes, which suggests that factors in the colony other than the brood have strong influence on circadianly regulated processes in the brain. We will discuss genes and pathways that are circadian-regulated by the colony environment and brood care and the implications of these findings to the social organization of the colony.

Professor Guy Bloch, Hebrew University of Jerusalem, Israel

Professor Guy Bloch, Hebrew University of Jerusalem, Israel

Guy Bloch is a professor of biology at the Hebrew University of Jerusalem and the current Head of the Alexander Institute of Life Sciences. Bloch's group research uses various sociobiological, behavioural, physiological and molecular approaches for understanding the evolution of sociality and the physiological and molecular basis of social behaviour using bees (mainly bumble bees and honey bees) as the main research models. The main research topics include understanding the interrelationships between biological clocks, sleep control and social behaviour, the influence of hormones, especially juvenile hormone (JH), on the evolution of sociality and social behaviour, and deciphering the sociobiology of bumble bee colonies, including mechanisms influencing division of labour, body size and caste determination. 

The genus Schistocerca (Orthoptera: Acrididae) includes some of the most devastating locust species in the world, including the desert locust (S. gregaria), the Central American locust (S. piceifrons), and the South American locust (S. cancellata). These locust species show an extreme form of density-dependent phenotypic plasticity in which cryptic and shy individuals, known as the solitarious phase, can transform into conspicuous and gregarious individuals, known as the gregarious phase, in response to changes in local population density. In fact, this “locust phase polyphenism” is what makes the locusts distinctly different from regular grasshoppers. Intriguingly, Schistocerca includes 45 species, most of which are non-swarming sedentary grasshopper species, and phylogenetic studies have shown that the locust species do not form a monophyletic group, suggesting that locust phase polyphenism has evolved multiple times in the genus. Furthermore, recent experimental studies have indicated that some of the non-swarming grasshopper species show reduced density-dependent phenotypic plasticity, suggesting that Schistocerca as a whole is an exciting model clade that can be used to study how phenotypic plasticity has evolved as species diverge.

In 2020, the Behavioral Plasticity Research Institute (BPRI) was launched with funding from the National Science Foundation Biology Integration Institute (NSF-BII) program. Through the BPRI, high-quality chromosome-length assemblies of six Schistocerca species, including three locust and three non-swarming grasshopper species, were produced. In this presentation, the author will discuss the new insights enabled by the new omics data on the evolution of phenotypic plasticity in Schistocerca as well as other novel findings enabled by this collaborative initiative. 

Professor Hojun Song, Texas A&M University, USA

Professor Hojun Song, Texas A&M University, USA

Dr Hojun Song received his PhD in Entomology from the Ohio State University in 2006. He joined the Department of Entomology as Assistant Professor in 2015, was promoted to Associate Professor in 2016, and Full Professor in 2022. Dr Song’s two main research areas are: (i) biodiversity of Orthoptera and (ii) the evolution and mechanisms of phenotypic plasticity using swarming locusts as a model system. Dr Song has received over $16 million in external research funding from the National Science Foundation and the United States Department of Agriculture, and has published 85 peer-reviewed articles. He has received a number of awards, including NSF CAREER award (2013), Fulbright Fellowship (2019), and the Distinguished Achievement Awards in Teaching from the Entomological Society of America (Southwestern Branch) (2021). Dr Song is Co-Director of the NSF Behavioural Plasticity Research Institute (BPRI) and Editor-in-Chief of the journal Insect Systematics & Evolution.