Evolved Differences in cis and trans Regulation Between the Maternal and Zygotic mRNA Complements in the Drosophila Embryo

Abstract

How gene expression can evolve depends on the mechanisms driving gene expression. Gene expression is controlled in different ways in different developmental stages; here we ask whether different developmental stages show different patterns of regulatory evolution. To explore the mode of regulatory evolution, we used the early stages of embryonic development controlled by two different genomes, that of the mother and that of the zygote. During embryogenesis in all animals, initial developmental processes are driven entirely by maternally provided gene products deposited into the oocyte. The zygotic genome is activated later, when developmental control is handed off from maternal gene products to the zygote during the maternal-to-zygotic transition. Using hybrid crosses between sister species of Drosophila (D. simulans, D. sechellia, and D. mauritiana) and transcriptomics, we find that the regulation of maternal transcript deposition and zygotic transcription evolve through different mechanisms. We find that patterns of transcript level inheritance in hybrids, relative to parental species, differ between maternal and zygotic transcripts, and maternal transcript levels are more likely to be conserved. Changes in transcript levels occur predominantly through differences in trans regulation for maternal genes, while changes in zygotic transcription occur through a combination of both cis and trans regulatory changes. Differences in the underlying regulatory landscape in the mother and the zygote are likely the primary determinants for how maternal and zygotic transcripts evolve.

The role of heterochronic gene expression and regulatory architecture in early developmental divergence

“…We found that the number of genes with compensatory regulatory modifications increases sharply after gastrulation, indicating that gene expression may be more tightly controlled past that point. Studies across Drosophila species, for example, have indicated that maternal effects are regulated differently than zygotic effects, but in this case there are larger trans -acting factors in early (maternally controlled) developmental stages (Cartwright and Lott 2020). We do not see such a clear effect; trans -acting factors make up most of the regulatory architecture throughout development.…”

“…Essentially a few trans -acting regulatory modifications, such as changes to transcription factors, could account for most of the developmental and phenotypic differences between morphs. As species divergence time increases, cis -acting elements can arise and refine gene expression of individual genes (Coolon et al 2014; Cartwright and Lott 2020; Wittkopp et al 2004). These regulatory architecture trends have been reported in other species, but none have examined the short evolutionary window of divergent morphs within the same species.…”

Evolution and genetics of accessory gland transcriptome divergence betweenDrosophila melanogasterand D.simulans

“…Further, just a handful of genes have complete GOF or LOF expression phenotypes. These results suggest that the accessory gland is not prone to widespread dysgenesis between these species, in contrast to results from Drosophila testis or female whole-animal data (Ranz et al 2004;Haerty and Singh 2006;Moehring, Teeter, and Noor 2007;McManus et al 2010;Coolon et al 2014;Cartwright and Lott 2020;Ranz et al 2023), Caenorhabditis data (Sánchez-Ramírez et al 2021), mouse liver (Goncalves et al 2012) and testis (Mack, Campbell, and Nachman 2016) data. Thus, our transcriptomic data are consistent with the observations of Stumm-Zollinger and Chen (1988), that hybrid accessory glands have relatively normal morphology, seminal fluid, and ability to induce the female PMR.…”

Maternal patterns of inheritance alter transcript expression in eggs

“…Variation in maternal mRNA deposition can certainly occur within a species, particularly due to maternal condition or genotype. For example, in Drosophila melanogaster the difference in oocyte gene expression between extreme maternal environmental conditions (starved mothers fed 5% of control mothers’ diet) is ~ 1.8% [ 62 , 63 ]. Another study, which sampled a much greater amount of genetic diversity, found maternal mRNA from embryos within populations of D. melanogaster to be much greater (40–60% of expressed genes differentially expressed; [ 64 ].…”

“…An advantage of our cross design is that we can determine the mode of regulation for differentially expressed genes. Typically regulatory analyses of cis and trans acting factors are conducted in hybrids [ 38 – 41 , 63 , 84 ], however, we were able to carry out these analyses in intraspecific comparisons with the caveat that there are fewer distinguishing polymorphisms between the alleles of the two parents. As such, we focus on the genes that are differentially expressed between the two morphs and therefore are not capturing the genetic architecture of genome-wide divergence between morphs, but rather the mode of regulation of genes that are differently expressed.…”