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

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 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-h-old eggs (24-h 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-h eggs, which were past the maternal-to-zygotic 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.

Keywords: development; diapause; maternal RNA; maternal effects; maternal-to-zygotic transition; microRNA; oogenesis; photoperiod.

FIGURE 1

Principal component analysis showing mRNA and miRNA expression profiles for (A,B) oocyte (blue color scheme) and (C,D) egg (green color scheme) samples. Each data point represents an individual sample. Manipulations of maternal body condition included both control (circle) and poor condition (triangle) treatment groups. Time of season includes early (light shade) and late (dark shade). Percent of variance captured by each principal component (PC) is included in the axes labels for PC1 and PC2.

FIGURE 2

Dendrograms depicting gene module relationships for oocyte and egg tissues. Lines (moving left to right) indicate where genes from oocyte modules significantly correlated with time of season (oocyteMod4, oocyteMod16, oocyteMod20, oocyteMod29) are distributed throughout egg modules. The line color represents oocyte module membership, including gold, dark blue, turquoise, and magenta as oocyteMod4, oocyteMod16, oocyteMod20, oocyteMod29, respectively. Egg modules that shared significant overlap across these four oocyte modules are indicated with a gray box. The shaded box highlights (eggMod4), the egg module that shared a significant number of genes with three of these oocyte modules (oocyteMod16, oocyteMod4, and oocyteMod29). Line thickness scales to the percentage of genes from the oocyte modules that belong to each respective egg module. Line scale (from smallest to largest): <1%, 1–10%, 10–20%, 20–30%, 30–40%, 40–50%, 50–60%, and 60–70%.