Post-mating gene expression of Mexican fruit fly females: disentangling the effects of the male accessory glands

Authors: SIROT, LAURA - College Of Wooster; Bansal, Raman; ESQUIVEL, CARLOS - The Ohio State University; ARTEAGA-VAZQUEZ, MARIO - University Of Veracruzana; HERRERA-CRUZ, MARIANA - Autonomous University "benito Juárez" Of Oaxaca; PAVINATO, VITOR - The Ohio State University; ABRAHAM, SOLANA - Liemen; MEDINA-JIMÉNEZ, KARINA - University Of Veracruzana; REYES-HERNÁNDEZ, MARTHA - University Of Veracruzana; DORANTES-ACOSTA, ANA - University Of Veracruzana; PÉREZ-STAPLES, DIANA - University Of Veracruzana

Submitted to: Insect Molecular Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/16/2021
Publication Date: 6/2/2021
Citation: Sirot, L., Bansal, R., Esquivel, C.J., Arteaga-Vazquez, M., Herrera-Cruz, M., Pavinato, V.A., Abraham, S., Medina-Jiménez, K., Reyes-Hernández, M., Dorantes-Acosta, A., Pérez-Staples, D. 2021. Post-mating gene expression of Mexican fruit fly females: disentangling the effects of the male accessory glands. Insect Molecular Biology. Available: https://onlinelibrary.wiley.com/journal/13652583?tabActivePane=undefined. https://doi.org/10.1111/imb.12719.
DOI: https://doi.org/10.1111/imb.12719

Interpretive Summary: Mexican fruit fly is a polyphagous pest attacking at least 60 species of fruits, most prominently citrus and mango. During the mating process, female insects receive not only sperm but also an ejaculate containing several proteins and other molecules from male reproductive tissues, primarily the reproductive accessory glands (AG). In this study, we studied the potential impact of AG products on female behavior and physiological processes. We employed comparative transcriptomics approach to study gene expression in mated, unmated and AG-injected female flies. We found that mating and AG products regulate several female processes such as egg development, chemosensory perception, host attraction, immune response, muscle development, lifespan etc. This research improves our understanding into reproductive physiology of this important pest and has potential to contribute towards developing the improved monitoring and control tactics.

Technical Abstract: Mating has profound physiological and behavioural consequences for female insects. During copulation, female insects typically receive not only sperm, but a complex ejaculate containing hundreds of proteins and other molecules from male reproductive tissues, primarily the reproductive accessory glands. The post-mating phenotypes affected by male accessory gland (MAG) proteins include egg development, attraction to oviposition hosts, mating, attractiveness, sperm storage, feeding and lifespan. In the Mexican fruit fly, Anastrepha ludens, mating increases egg production and the latency to remating. However, previous studies have not found a clear relationship between injection of MAG products and oviposition or remating inhibition in this species. We used RNAseq to study gene expression in mated, unmated and MAG-injected females to understand the potential mating- and MAG-regulated genes and pathways in A. ludens. Both mating and MAG-injection regulated transcripts and pathways related to egg development. Other transcripts regulated by mating included those with orthologs predicted to be involved in immune response, musculature and chemosensory perception, whereas those regulated by MAG-injection were predicted to be involved in translational control, sugar regulation, diet detoxification and lifespan determination. These results suggest new phenotypes that may be influenced by seminal fluid molecules in A. ludens. Understanding these influences is critical for developing novel tools to manage A. ludens.