Maternal body condition and season influence RNA deposition in the oocytes of alfalfa leafcutting bees (Megachile rotundata)

Authors: HAGADORN, MALLORY - Utah State University; HUNTER, FRANCES - Utah State University; DELORY, TIM - Utah State University; Johnson, Makenna; Pitts Singer, Theresa; KAPHEIM, KAREN - Utah State University

Submitted to: Frontiers in Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/28/2022
Publication Date: 1/4/2023
Citation: Hagadorn, M.A., Hunter, F.K., DeLory, T., Johnson, M.M., Pitts Singer, T., Kapheim, K.M. 2023. Maternal body condition and season influence RNA deposition in the oocytes of alfalfa leafcutting bees (Megachile rotundata). Frontiers in Genetics. 13. Article 1064332. https://doi.org/10.3389/fgene.2022.1064332.
DOI: https://doi.org/10.3389/fgene.2022.1064332

Interpretive Summary: There are mechanisms by which mother animals (including insects) can affect the physical and genetic outcomes of their offspring. Importantly, they can determine the developmental pathway of offspring in response to changing environmental conditions. For our example, a mother alfalfa leafcutting bee can influence whether her offspring become adults to be active in the same summer as their mothers, or whether offspring enter diapause (similar to hibernation) for the winter and become adults in the following summer. However, relatively little is known about the mechanisms by which the experiences of the mother (e.g., her exposure to certain daylengths or her general health) is translated into molecular signals that shape offspring development. One such signal may be via maternal RNA transcripts (mRNAs and miRNAs = specific genetic materials) deposited into maturing oocytes (pre-embryos). These regulate the earliest stages of development of all animals, but are understudied in most insects. Here we investigated the effects of female internal (body condition) and external (time of season) environmental conditions on maternal RNA in the maturing oocytes and 24 hr old eggs of alfalfa leafcutting bees. Using gene expression and specialized analytical techniques, we found that females adjust the quantity of mRNAs related to certain physiological processes that are deposited into maturing oocytes in response to both poor body condition and shorter day lengths that accompany the late season. However, the magnitude of these changes was higher for time of season. Females also adjusted miRNA deposition in response to seasonal changes, but not body condition. We did not observe significant changes in maternal RNAs in response to either body condition or time of season in 24 hr old eggs, which were past the transition point of where the mother's genetic material impacts the genetic make-up of the new, developing egg. Our results suggest that females adjust the RNA transcripts they provide for offspring to regulate development in response to both internal and external environmental cues. Variation in maternal RNAs may, therefore, be important for regulating offspring phenotype (physical outcome) in response to environmental change.

Technical Abstract: Maternal effects are an important source of phenotypic variance, whereby females influence offspring developmental trajectory beyond direct genetic contributions, often in response to changing environmental conditions. However, relatively little is known about the mechanisms by which maternal experience is translated into molecular signals that shape offspring development. One such signal may be via maternal RNA transcripts (mRNAs and miRNAs) deposited into maturing oocytes. These regulate the earliest stages of development of all animals, but are understudied in most insects. Here we investigated the effects of female internal (body condition) and external (time of season) environmental conditions on maternal RNA in the maturing oocytes and 24 hr old eggs of alfalfa leafcutting bees. Using gene expression and WGCNA analysis, we found that females adjust the quantity of mRNAs related to protein phosphorylation, transcriptional regulation, and nuclease activity deposited into maturing oocytes in response to both poor body condition and shorter day lengths that accompany the late season. However, the magnitude of these changes was higher for time of season. Females also adjusted miRNA deposition in response to seasonal changes, but not body condition. We did not observe significant changes in maternal RNAs in response to either body condition or time of season in 24 hr old eggs, which were past the maternal-zygote-transition. Our results suggest that females adjust the RNA transcripts they provide for offspring to regulate development in response to both internal and external environmental cues. Variation in maternal RNAs may, therefore, be important for regulating offspring phenotype in response to environmental change.