UC Berkeley

The remarkable diversity of animal behaviors have long attracted biologists from different fields. However, the genetic architecture and molecular changes behind the diversification of these behavioral traits have remained elusive due to technical limitations, preventing deeper understanding of evolutionary processes of behaviors. My dissertation work aims to dissect the evolution, genetic architecture, and molecular basis of behavioral traits using a herbivorous drosophilid fly, Scaptomyza flava, with a particular emphasis on the evolution of its chemosensory behaviors that are specifically tuned to the specialized chemicals produced by mustard plants in the order Brassicales.

In Chapter 1, I briefly summarized the historical context and recent trends in the study of behavioral evolution in animals. I argue that the evolution of chemosensory behavior in insects provides an excellent model for uncovering the genetic architecture and molecular basis of behavioral change across lineages. I further introduced S. flava as a unique system to address such questions that allows us to bridge genomic and functional approaches by leveraging the power of model organisms in genetics, the vinegar fly Drosophila melanogaster and the model mustard Arabidopsis thaliana.

In Chapter 2, I investigated transcriptional evolution in the chemosensory organs, in the genus Scaptomyza with a particular emphasis on six major insect chemosensory gene families. I conducted a comparative bulk RNA-sequencing between S. flava and its microbe-feeding relative, S. pallida, and searched for genes experiencing larger expression divergence between species as candidates behind chemosensory evolution. This approach successfully illuminated evolutionary patterns across gene families and narrowed down the candidates that provide insight into specific sensory changes aided the colonization of Brassicales host plants.

In contrast to the exploratory analyses in the previous chapter, Chapter 3 conducted a detailed investigation on a single gene and its products, TrpA1, which encodes a chemosensory ion channel detecting electrophilic toxins, including mustard-derived isothiocyanates (ITCs). Again, I took a comparative approach between the mustard-feeding S. flava and the microbe-feeding relatives to address how the functional evolution of TRPA1 has been intertwined with the dietary and chemosensory evolution among the drosophilids. I integrated multiple experimental approaches spanning from genomics and genetics to electrophysiology, and found that the reduced chemical sensitivity of the TRPA1 channel and the modified composition of alternatively spliced isoforms were likely two major molecular changes behind the weak avoidance toward ITCs in the S. flava lineage. However, I also found that the TRPA1 activity from the distantly-related generalist D. melanogaster was even weaker than S. flava, despite the strong behavioral aversion to ITCs, suggesting that the evolutionary relationship of the TRPA1 channel function and the gustatory preferences is more complicated than it seems, and requires careful investigations on multiple characteristics of the gene.