Behavioral Evolution of Drosophila: Unraveling the Circuit Basis

Abstract

Behavior is a readout of neural function. Therefore, any difference in behavior among different species is, in theory, an outcome of interspecies diversification in the structure and/or function of the nervous system. However, the neural diversity underlying the species-specificity in behavioral traits and its genetic basis have been poorly understood. In this article, we discuss potential neural substrates for species differences in the courtship pulse song frequency and mating partner choice in the Drosophila melanogaster subgroup. We also discuss possible neurogenetic mechanisms whereby a novel behavioral repertoire emerges based on the study of nuptial gift transfer, a trait unique to D. subobscura in the genus Drosophila. We found that the conserved central circuit composed primarily of fruitless-expressing neurons (the fru-circuit) serves for the execution of courtship behavior, whereas the sensory pathways impinging onto the fru-circuit or the motor pathways downstream of the fru-circuit are susceptible to changes associated with behavioral species differences.

Inter-species comparison of the orientation algorithm directing larval chemotaxis in the genus Drosophila

“…It also emerges from changes in higher-order functions, such as the acquisition of social traits in feeding behavior (De Bono and Bargmann 1998) or the specialization of motor programs to cope with the properties of different physical environments (Karageorgi, Bräcker et al 2017). Consistent with the idea that evolution can act by manipulating the properties of neural circuits, variations in the courtship rituals of drosophilids has been associated with changes in the functional logic of central circuits without major differences in the ability to detect pheromonal cues at the sensory periphery (Seeholzer, Seppo et al 2018, Khallaf, Auer et al 2020, Sato, Tanaka et al 2020. While the genetic mechanisms underlying the functional diversification of neural circuits remain poorly understood, speciesspecific differences in courtship songs have been linked to differences in the genomic sequences of an ion channel widely expressed in the fly nervous system (Ding, Berrocal et al 2016).…”

“…These findings led to the idea that evolution can adjust behavior by modifying the functional properties of hubs in neural circuits. Together, specialization in courtship behavior can arise from changes in the peripheral olfactory system, signal processing units and motor pathways (Sato, Tanaka et al 2020). The relevance of each level of regulation remains to be determined.…”

From fruitless to sex: On the generation and diversification of an innate behavior

“…Furthermore, fru M expression in the visual system is also observed in female D. suzukii 47 . Given the rapid change of fru M expression and the diversity of male courtship behaviors across Drosophila species, 49,50 it is conceivable that changes in the fru M regulatory regions during evolution would alter the functional mode of the sex circuitry to generate diverse courtship behaviors across species.…”

Evolution of a neuromuscular sexual dimorphism in the Drosophila montium species group

“…Sexually dimorphic characteristics have been a focus of evolutionary studies because they represent an important signature of the history of sexual selection 1 . Although male-specific external structures have attracted substantial interest among biologists 1 , 2 , sex differences in the structure and function of internal organs have not been thoroughly studied from an evolutionary point of view 3 . As an attempt to understand how internal sexual dimorphisms evolve, we studied a male-specific muscle called the muscle of Lawrence or MOL 4 in the Drosophila montium group 5 , 6 , in which the male courtship display varies widely across species 7 , 8 , suggesting a unique evolutionary history of sexually dimorphic traits.…”