SNMP1 is critical for sensitive detection of the desert locust aromatic courtship inhibition pheromone phenylacetonitrile.

BACKGROUND: Accurate detection of pheromones is crucial for chemical communication and reproduction in insects. In holometabolous flies and moths, the sensory neuron membrane protein 1 (SNMP1) is essential for detecting long-chain aliphatic pheromones by olfactory neurons. However, its function in hemimetabolous insects and its role for detecting pheromones of a different chemical nature remain elusive. Therefore, we investigated the relevance of SNMP1 for pheromone detection in a hemimetabolous insect pest of considerable economic importance, the desert locust Schistocerca gregaria, which moreover employs the aromatic pheromone phenylacetonitrile (PAN) to govern reproductive behaviors. RESULTS: Employing CRISPR/Cas-mediated gene editing, a mutant locust line lacking functional SNMP1 was established. In electroantennography experiments and single sensillum recordings, we found significantly decreased electrical responses to PAN in SNMP1-deficient (SNMP1-/-) locusts. Moreover, calcium imaging in the antennal lobe of the brain revealed a substantially reduced activation of projection neurons in SNMP1-/- individuals upon exposure to PAN, indicating that the diminished antennal responsiveness to PAN in mutants affects pheromone-evoked neuronal activity in the brain. Furthermore, in behavioral experiments, PAN-induced effects on pairing and mate choice were altered in SNMP1-/- locusts. CONCLUSIONS: Our findings emphasize the importance of SNMP1 for chemical communication in a hemimetabolous insect pest. Moreover, they show that SNMP1 plays a crucial role in pheromone detection that goes beyond long-chain aliphatic substances and includes aromatic compounds controlling reproductive behaviors.

Synergistic olfactory processing for social plasticity in desert locusts.

Desert locust plagues threaten the food security of millions. Central to their formation is crowding-induced plasticity, with social phenotypes changing from cryptic (solitarious) to swarming (gregarious). Here, we elucidate the implications of this transition on foraging decisions and corresponding neural circuits. We use behavioral experiments and Bayesian modeling to decompose the multi-modal facets of foraging, revealing olfactory social cues as critical. To this end, we investigate how corresponding odors are encoded in the locust olfactory system using in-vivo calcium imaging. We discover crowding-dependent synergistic interactions between food-related and social odors distributed across stable combinatorial response maps. The observed synergy was specific to the gregarious phase and manifested in distinct odor response motifs. Our results suggest a crowding-induced modulation of the locust olfactory system that enhances food detection in swarms. Overall, we demonstrate how linking sensory adaptations to behaviorally relevant tasks can improve our understanding of social modulation in non-model organisms.

An effective hydrodynamic description of marching locusts.

A fundamental question in complex systems is how to relate interactions between individual components ('microscopic description') to the global properties of the system ('macroscopic description'). Furthermore, it is unclear whether such a macroscopic description exists and if such a description can capture large-scale properties. Here, we address the validity of a macroscopic description of a complex biological system using the collective motion of desert locusts as a canonical example. One of the world's most devastating insect plagues begins when flightless juvenile locusts form 'marching bands'. These bands display remarkable coordinated motion, moving through semiarid habitats in search of food. We investigated how well macroscopic physical models can describe the flow of locusts within a band. For this, we filmed locusts within marching bands during an outbreak in Kenya and automatically tracked all individuals passing through the camera frame. We first analyzed the spatial topology of nearest neighbors and found individuals to be isotropically distributed. Despite this apparent randomness, a local order was observed in regions of high density in the radial distribution function, akin to an ordered fluid. Furthermore, reconstructing individual locust trajectories revealed a highly aligned movement, consistent with the one-dimensional version of the Toner-Tu equations, a generalization of the Navier-Stokes equations for fluids, used to describe the equivalent macroscopic fluid properties of active particles. Using this effective Toner-Tu equation, which relates the gradient of the pressure to the acceleration, we show that the effective 'pressure' of locusts increases as a linear function of density in segments with the highest polarization (for which the one-dimensional approximation is most appropriate). Our study thus demonstrates an effective hydrodynamic description of flow dynamics in plague locust swarms.

Information integration for decision-making in desert locusts.

Locust swarms can extend over hundred kilometers, and starvation compels this ancient pest to devour everything in its path. Theory suggests that gregarious behavior benefits foraging efficiency, yet the role of social cohesion remains elusive. To this end, we collected high-resolution trajectories of individual and grouped gregarious desert locusts in a 2-choice assay with patches of either similar or different quality. Carefully maintaining animals' identities allowed us to monitor each individual's experience and estimate the leaky accumulation process of personally acquired and socially derived evidence. We fitted data to a Bayesian model to gain insight into the decision-making system for patch selection. By disentangling the relative contribution of each information class, our study suggests that locusts balance incongruent evidence but reinforce congruent ones. We provide insight into the collective foraging decisions of social (but non-eusocial) insects and present locusts as a powerful empirical system to study individual choices and consequent collective dynamics.

Locomotor resilience through load-dependent modulation of muscle co-contraction.

Terrestrial locomotor behavior in variable environments requires resilience to sudden changes in substrate properties. For example, walking animals can adjust to substantial changes in slope and corresponding changes in load distribution among legs. In insects, slope-dependent adjustments have mainly been examined under steady-state conditions, whereas the transition dynamics have been largely neglected. In a previous study, we showed that steady-state adjustments of stick insects to ±45 deg slopes involve substantial changes in joint torques and muscle activity with only minor changes in leg kinematics. Here, we took a close look at the time course of these adjustments as stick insects compensate for various kinds of disturbances to load distribution. In particular, we tested whether the transition from one steady state to another involves distinct transition steps or follows a graded process. To resolve this, we combined simultaneous recordings of whole-body kinematics and hindleg muscle activity to elucidate how freely walking Carausius morosus negotiated a step-change in substrate slope. Step-by-step adjustments revealed that muscle activity changed in a graded manner as a function of body pitch relative to gravity. We further show analogous transient adjustment of muscle activity in response to destabilizing lift-off events of neighboring legs and the disappearance of antagonist co-activation during crawling episodes. Given these three examples of load-dependent regulation of antagonist muscle co-contraction, we conclude that stick insects respond to both transient and sustained changes in load distribution by regulating joint stiffness rather than through distinct transition steps.

Social modulation of individual preferences in cockroaches.

In social species, decision-making is both influenced by, and in turn influences, the social context. This reciprocal feedback introduces coupling across scales, from the neural basis of sensing, to individual and collective decision-making. Here, we adopt an integrative approach investigating decision-making in dynamical social contexts. When choosing shelters, isolated cockroaches prefer vanillin-scented (food-associated) shelters over unscented ones, yet in groups, this preference is inverted. We demonstrate that this inversion can be replicated by replacing the full social context with social odors: presented alone food and social odors are attractive, yet when presented as a mixture they are avoided. Via antennal lobe calcium imaging, we show that neural activity in vanillin-responsive regions reduces as social odor concentration increases. Thus, we suggest that the mixture is evaluated as a distinct olfactory object with opposite valence, providing a mechanism that would naturally result in individuals avoiding what they perceive as recently exploited resources.