bioRxiv Science⌕ Search

bioRxiv · 10.1101/2023.06.29.546928

Behavioral and Neural Resilience to Isolation in a Eusocial Insect

Abstract

Social experience early in life appears to be necessary for the development of species-typical behavior. Although isolation during critical periods of maturation has been shown to impact behavior by altering gene expression and brain development in invertebrates and vertebrates, workers of some ant species appear resilient to social deprivation and other neurobiological challenges that occur during senescence or due to loss of sensory input. It is unclear if and to what degree neuroanatomy, neurochemistry, and behavior will show deficiencies if social experience in the early adult life of worker ants is compromised. We reared newly-eclosed adult workers of Camponotus floridanus under conditions of social isolation for 2 to 53 days, quantified brain compartment volumes, recorded biogenic amine levels in individual brains, and evaluated movement and behavioral performance to compare the neuroanatomy, neurochemistry, brood-care behavior, and foraging (predatory behavior) of isolated workers with that of workers experiencing natural social contact after adult eclosion. We found that the volume of the antennal lobe, which processes olfactory inputs, was significantly reduced in workers isolated for an average of 40 days, whereas the size of the mushroom bodies, centers of higher-order sensory processing, increased after eclosion and was not significantly different from controls. Titers of the neuromodulators serotonin, dopamine, and octopamine remained stable and were not significantly different in isolation treatments and controls. Brood care, predation, and overall movement were reduced in workers lacking social contact early in life. These results suggest that the behavioral development of isolated workers of C. floridanus is specifically impacted by a reduction in the size of the antennal lobe. Task performance and locomotor ability therefore appear to be sensitive to a loss of social contact through a reduction of olfactory processing ability rather than change in the size of the mushroom bodies, which serve important functions in learning and memory, or the central complex, which controls movement. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=133 SRC="FIGDIR/small/546928v2_ufig1.gif" ALT="Figure 1"> View larger version (33K): org.highwire.dtl.DTLVardef@199228aorg.highwire.dtl.DTLVardef@aacd50org.highwire.dtl.DTLVardef@18d657corg.highwire.dtl.DTLVardef@1b9eb_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOVisual Abstract.C_FLOATNO Newly eclosed (callow) Camponotus floridanus minor workers were subjected to variable periods of isolation to determine whether and how diminished social experience and isolation influence the development of the brain, including compartment volumes, biogenic amine levels, and behavioral performance. C_FIG

Source connections

Explore related subjects

Keep this discovery

Explore connections, maps & timelines

BibTeXRIS

Goolsby, B. C., Smith, E. J., Muratore, I. B., Coto, Z. N., Muscedere, M. L., Traniello, J. F. A.. 2023-07-01. Behavioral and Neural Resilience to Isolation in a Eusocial Insect. https://doi.org/10.1101/2023.06.29.546928

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related preprints

Deconstructing Boldness: Latent behavioural structure across novelty, predation, and exploration in an endangered species translocation program

Risk-related behaviours including neophobia, exploration, and predator avoidance are often assumed to covary along a general boldness axis. Although some translocation studies have linked one or more of these behaviours with fitness, it is possible that the underlying behavioural structure varies under different selective environments. Conservation breeding programs provide a unique opportunity to evaluate the structure of behavioural correlations in a non-domestic species under artificial conditions. We tested whether risk-related behaviours represent a unified boldness syndrome in a captive population of the endangered Attwaters prairie chicken (APC; Tympanuchus cupido attwateri). We quantified the repeatable behaviours of 257 juveniles and compared 11 models of behavioural covariation structure using multivariate mixed models and confirmatory factor analysis. There was no support for a single risk-taking axis; instead, we found three dimensions representing responses to novelty and environmental stimuli (Engagement), predator avoidance (Threat Response), and maze exploration (Maze Progression). Our results indicate that these risk-related behaviours are not organized along a single axis in captive APCs, challenging assumptions that risk-taking represents a universal behavioural syndrome. To anticipate post-release success accurately, conservation managers should understand the exact behavioural architecture of the captive population rather than assume that the classical bold-shy structure occurs in all contexts.

animal behavior and cognition↗

Shared brain transcriptome signatures of social evolution and plasticity in shell-dwelling cichlid fishes

Inter-individual variability in phenotypic traits is widespread in nature both across and within species, with similar patterns of variation often occurring between and within species. Given that these two types of variation are generated by evolutionary and plasticity processes respectively, it raises the question to what extent the causal mechanisms underlying such variability at these two different levels are shared or not. To address this question, we studied the variation in brain transcriptomes in Tanganyikan cichlids that exhibit both intra- and interspecific variation in social behavior. We compared two facultatively social cichlid species, each containing naturally occurring solitary and social-living individuals, with a closely related obligatory solitary resembling the ancestral state. Differential gene expression and Gene Set Enrichment Analyses were performed in the telencephalon and diencephalon transcriptomes to investigate the molecular basis of both behavioral plasticity and the evolution of sociality. Behavioral plasticity involved few differentially expressed genes but extensive changes in biological pathways, supporting a highly polygenic architecture of social behavior. Across both species, social-living individuals consistently upregulated pathways involved in translation, protein homeostasis, and energy metabolism, whereas solitary individuals showed enrichment of neuronal morphogenesis, cell adhesion, and structural plasticity. Remarkably, these same functional programs were associated with the independent evolution of sociality, revealing a strong overlap between evolutionary and plastic transcriptional responses. This convergence was largely restricted to the telencephalon, while the diencephalon showed limited and inconsistent functional signatures. Together, our results support the repeated recruitment of gene regulatory programs during the evolution of sociality and demonstrate that behavioral plasticity and evolutionary transitions share common neurogenomic responses, consistent with a conserved genetic toolkit for social behavior.

animal behavior and cognition↗

Inductive bias anchors a scaling law for biological learning

The speed of animal learning varies substantially across individuals and task domains, and does not always track intuitive notions of task complexity. A nominally simple binary decision task can take thousands of rewards to reach proficiency, whereas seemingly complex naturalistic tasks can be learned within dozens. A long-standing explanation is that learning speed reflects the alignment between an animal's inductive biases and the task at hand. However, without a precise notion of alignment, it is difficult to translate this idea into quantitative predictions. Here, modeling an animal as a Bayesian learner that improves through iterative reward feedback, we use statistical learning theory to derive a scaling law for biological learning. The law makes two predictions. First, inductive bias multiplicatively sets the speed of learning through a single quantity, the effective complexity. This quantity measures how well the task aligns with the animal's prior, and corresponds to the number of bits required to represent the task solution under that prior. We demonstrate this multiplicative scaling in a human motor learning dataset, where behavioral measurements before learning can precisely predict subsequent learning speed. Second, task performance improves as a power law in experience. We validate this power law in a large-scale mouse learning dataset and show that a two-parameter rescaling collapses individual learning curves onto a universal function predicted by the theory. These results suggest that behavioral measurements before learning can be used to predict task-dependent learning speeds, and they explain why learning speed reflects alignment with prior knowledge rather than nominal task complexity.

animal behavior and cognition↗