Expression of defensin genes across house fly (Musca domestica) life history gives insight into immune system subfunctionalization

Authors: ASGARI, DANIAL - University Of Houston; Purvis, Tanya; PICKENS, VICTORIA - Kansas State University; SASKI, CHRISTOPER - Clemson University; MEISEL, RICHARD - University Of Houston; Nayduch, Dana

Submitted to: Genome
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/15/2024
Publication Date: 5/9/2024
Citation: Asgari, D., Purvis, T.J., Pickens, V., Saski, C., Meisel, R.P., Nayduch, D. 2024. Expression of defensin genes across house fly (Musca domestica) life history gives insight into immune system subfunctionalization. Genome. https://doi.org/10.1139/gen-2024-0016.
DOI: https://doi.org/10.1139/gen-2024-0016

Interpretive Summary: Insects produce antimicrobial peptides (AMPs) in response to microbial infections or as part of their routine activities. Defensins are AMPs used by a wide array of animals to defend against microbial assaults. House flies breed in and feed upon filth, spending their entire life cycle in contact with microbes. As a result, flies exhibit a unique adaptation to this lifestyle by having 12 copies of slightly different Defensin genes, forming an expanded arsenal to use against microbes. In this study, we investigated the temporal activation of these 12 Defensins across the house fly life cycle, from eggs to adults. Four Defensin genes were activated during the larval and pupal stages, likely in response to microbial encounters, while another set was utilized by adults, even in the absence of microbe exposure or feeding. Notably, the proteins coding for adult Defensins showed more evolutionary changes compared to their larval counterparts, featuring a distinct and rapidly evolving protein sequence. These findings underscore the impact of microbe exposure on the evolutionary trajectory of Defensin genes in house flies. Exploring the inhibition of these AMPs could provide novel avenues for fly control. Moreover, given the potent antimicrobial activity of Defensins that safeguard flies from diverse pathogens throughout their lifetime, this research holds significance for considering Defensins as potential therapeutic agents against a variety of microbial infections.

Technical Abstract: Animals encounter diverse microbial communities throughout their lifetime, which exert varying selection pressures. Antimicrobial peptides (AMPs), which lyse or inhibit microbial growth, are a first line of defense against some of these microbes. Here examine how developmental variation in microbial exposure has shaped the expression and amino acid sequences of Defensins (an ancient class of AMPs) in the house fly (Musca domestica). The house fly is a well-suited model for this work because it trophically associates with varying microbial communities throughout its life history and its genome shows largely expanded families of AMPs, including Defensins. We identified two subsets of house fly Defensins expressed during distinct developmental stages (larval/pupal and adult), which form separate monophyletic clades. The adult-expressed Defensins evolve faster than larval/pupal Defensins, consistent with different selection pressures across developmental stages. Our results therefore suggest that varied microbial communities encountered during its life history can shape the evolutionary trajectories of immune genes.