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

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 RNA‐seq 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.

Mating, but Not Male Accessory Gland Products, Changes Female Response to Olfactory Cues in Anastrepha Fruit Flies

“…In A. ludens, transcriptomic studies have shown important changes after mating and MAG-injection suggesting that MAGs could be performing functions such as increasing life span in response to stressful environmental factors, (e.g., low humidity or nutrient limitation), as well as dietary detoxification, glucose regulation, and increasing egg production through translation stimulation (Sirot et al, 2021). In A. obliqua, MAG function is unknown, but, based on the results of our study, they do not seem to have an effect on olfactory response.…”

Effects of Mating on Gene Expression in Female Insects: Unifying the Field

“…aegypti (downregulated), D. melanogaster (upregulated) and the sweet potato white fly B. tabaci (upregulated; [29,39,41] and glyceraldehyde 3 phosphate dehydrogenase is upregulated by mating in Anastrepha ludens (Diptera: Tephritdae) [24]. The lipid biosynthesis pathway is significantly upregulated by mating in A. ludens and genes involved in fatty acid synthesis are upregulated by mating in both A. ludens and Anastatus disparis [24,47]. Fatty acid synthesis contributes to egg development, embryogenesis, fecundity, and digestion in some insects [48,49].…”

“…It is plausible that mating-regulation of CYPs could contribute to detoxification of seminal fluid molecules that impact female survival [23,55,56]. Further, the many proteolysis-related mating-regulated genes are likely to play a role in other processes including: immune response; the activation, inactivation, and/or degradation of seminal fluid molecules; and protection of sperm from proteolytic degradation [24,29,31,39,57]. Together, the regulation of many different genes involved in immunity and detoxification are likely to be involved in the female response to the introduction of foreign substances during the mating process.…”

“…gambiae and abolishes Plasmodium ookinete melanization in a refractory strain, which becomes susceptible in the TEP1-silenced background [68]. Another gene associated with pathogen melanization, prophenoloxidase (PPO) and CLIP proteases, are also regulated by mating in several species [24,50,61,[69][70][71]. Further, phenoloxidase activity increases after mating in the female of the ground cricket, Allonemobius socius (Orthoptera: Gryllidae) [72].…”

“…Such studies have been conducted in several insect species and have revealed interesting patterns. Some expression changes are in genes with predicted functions related to known female post-mating changes (e.g., egg production, immunity, and chemosensation; [21][22][23][24][25], whereas others are in genes with unexpected predicted functions (e.g., muscle development, pH regulation; and translation initiation factors; [26][27][28] which have led to new candidate phenotypes to test for post-mating changes. However, most such studies have resulted in as-of-yet untested hypotheses about the connections between mating-regulated genes and mating-regulated phenotypes.…”