Abstract
How a nervous system assembles and coordinates a suite of elementary behavioral steps into a complex behavior is not well understood. While often presented as a stereotyped sequence of events, even extensively studied behaviors such as fly courtship are rarely a strict repetition of the same steps in a predetermined sequence in time. We are focusing on oviposition, the act of laying an egg, in flies of the genus Drosophila to describe the elementary behavioral steps or microbehaviors that a single female fly undertakes prior to and during egg laying. We have analyzed the hierarchy and relationships in time of these microbehaviors in three closely related Drosophila species with divergent egg-laying preferences and uncovered cryptic differences in their behavioral patterns. Using high-speed imaging, we quantified in depth the oviposition behavior of single females of Drosophila suzukii, Drosophila biarmipes and Drosophila melanogaster in a novel behavioral assay. By computing transitions between microbehaviors, we identified a common ethogram structure underlying oviposition of all three species. Quantifying parameters such as relative time spent on a microbehavior and its average duration, however, revealed clear differences between species. In addition, we examined the temporal dynamics and probability of transitions to different microbehaviors relative to a central event of oviposition, ovipositor contact. Although the quantitative analysis highlights behavioral variability across flies, it reveals some interesting trends for each species in the mode of substrate sampling, as well as possible evolutionary differences. Larger datasets derived from automated video annotation will overcome this paucity of data in the future, and use the same framework to reappraise these observed differences. Our study reveals a common architecture to the oviposition ethogram of three Drosophila species, indicating its ancestral state. It also indicates that Drosophila suzukii’s behavior departs quantitatively and qualitatively from that of the outgroup species, in line with its known divergent ethology. Together, our results illustrate how a global shift in ethology breaks down in the quantitative reorganization of the elementary steps underlying a complex behavior.
Highlights
The diversity of complex animal behaviors is perceptible in the most subtle differences of innate behaviors between closely related species
To observe the egg-laying behavior of individual flies, we built chambers where the only suitable spot for oviposition was a 3 mm2 area filled with a ripe piece of strawberry, an egg-laying substrate well accepted by all three species in no-choice assays (Karageorgi et al, 2017), the rest of the arena being hard plastic (Polytetrafluoroethylene)
We have established a method to reliably record and annotate egg laying in Drosophila at a single fly level and with a very precise spatial and temporal resolution
Summary
The diversity of complex animal behaviors is perceptible in the most subtle differences of innate behaviors between closely related species. Wolves and dog breeds looking like wolves are unmistakingly identified by a suite of different elementary behaviors (Heberlein et al, 2016). Bird species of the same genus can be identified on the sole basis of their songs (Slabbekoorn and Smith, 2002). The same holds true for cicadas (Young, 1972). Drosophila flies from different species engage in distinct courtship rituals (Spieth, 1952). Different innate complex behaviors, such as feeding or reproductive behaviors, stem from simple differences in the suite of behavioral steps that together constitute the overall action (Spieth, 1952)
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