A Transcriptomic Atlas Underlying Developmental Plasticity of Seasonal Forms of Bicyclus anynana Butterflies

Abstract

Organisms residing in regions with alternating seasons often develop different phenotypes, or forms, in each season. These forms are often adaptations to each season and result from an altered developmental response to specific environmental cues such as temperature. While multiple studies have examined form-specific gene expression profiles in a diversity of species, little is known about how environments and developmental transitions, cued by hormone pulses, alter post-transcriptional patterns. In this study, we examine how gene expression, alternative splicing, and miRNA-mediated gene silencing in Bicyclus anynana butterfly hindwing tissue, varies across two rearing temperatures at four developmental timepoints. These timepoints flank two temperature-sensitive periods that coincide with two pulses of the insect hormone 20E. Our results suggest that developmental transitions, coincident with 20E pulses, elicit a greater impact on all these transcriptomic patterns than rearing temperatures per se. More similar transcriptomic patterns are observed pre-20E pulses than those observed post-20E pulses. We also found functionally distinct sets of differentially expressed and differentially spliced genes in the seasonal forms. Furthermore, around 10% of differentially expressed genes are predicted to be direct targets of, and regulated by, differentially expressed miRNAs between the seasonal forms. Many differentially expressed genes, miRNAs, or differentially spliced genes potentially regulate eyespot size plasticity, and we validated the differential splicing pattern of one such gene, daughterless. We present a comprehensive and interactive transcriptomic atlas of the hindwing tissue of both seasonal forms of B. anynana throughout development, a model organism of seasonal plasticity.

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

“…One possible explanation for this pattern is that the biochemical signatures of early embryogenesis dominated the transcriptomic profiles of 24-h eggs, making any signal of maternal effects either difficult to detect or non-existent. For example, previous research in butterflies suggests that hormone pulses demarcating developmental transitions elicit a greater influence on gene expression profiles than environmental influences, such as temperature ( Tian and Monteiro, 2022 ). Our WGCNA analyses also showed signs of embryogenesis dominating transcriptional signatures in 24-h eggs.…”

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

“…One possible explanation for this pattern is that the biochemical signatures of early embryogenesis dominated the transcriptomic profiles of 24-hr eggs, making any signal of maternal effects either difficult to detect or non-existent. For example, previous research in butterflies suggests that hormone pulses demarcating developmental transitions elicit a greater influence on gene expression profiles than environmental influences, such as temperature (Tian & Monteiro 2022). Our WGCNA analyses also showed signs of embryogenesis dominating transcriptional signatures in 24-hr eggs.…”

A micro-RNA is the effector gene of a classic evolutionary hotspot locus

“…Taking advantage of a complete set of miRNAs annotated in B. anynana butterflies (Tian and Monteiro, 2022), we screened the whole cortex locus and only found two deeply conserved miRNAs embedded in it, mir-193 and mir-2788 (Fig. 1B).…”

“…Here, we aimed to test if miRNAs present in the cortex locus are the actual effectors of this locus. We began by screening the entire cortex locus (2Mb genomic region flanking cortex ) for the presence of any miRNAs in Bicyclus anynana , a model species which enjoys a comprehensive annotation of miRNAs expressed throughout wing development ( 20 ). Two miRNAs, mir-193 and mir-2788, were found, ∼5.2 kb apart, in the intergenic region between cortex and the adjacent protein-coding gene poly(A)-specific ribonuclease ( parn ) (Fig.…”

“…When both strands are expressed at high levels (in the case of mir-2788 ), both can be potential guides. The expression profiles are from a previous small RNA-seq (sRNA-seq) dataset generated across wing development in B. anynana (15).…”