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Modes of natural selection on maternal and zygotic gene expression in Drosophila melanogaster embryos

Thomas O'Leary, Brent Lockwood

Posted on: 19 August 2026

Preprint posted on 29 May 2026

What drives evolutionary change in early embryonic gene expression?

Selected by Girish Kale, preLights peer support

Categories: developmental biology, ecology, evolutionary biology

Written by: Franziska Traub (Bachelor student at the University of Hohenheim, Stuttgart. Germany)

Background

Evolutionary factors affect organismal development and how organisms respond to their environment. To better understand evolutionary mechanisms, it is important to consider how developmental processes are regulated and how they may evolve over time. Embryogenesis is characterized by many tightly regulated events, in which developmental robustness is preserved while allowing evolutionary change. This balance between maintaining fundamental processes and allowing flexibility determines later developmental outcomes and organismal fitness. It is a balance that offers an interesting entry point for understanding evolutionary processes in a developmental context. To examine this more closely, the preprint highlighted here investigated the genetic control of embryogenesis and how it is shaped by natural selection in the model organism Drosophila melanogaster.

While previous research has examined how gene expression diverges between species over millions of years, much less is known about microevolutionary changes and how gene expression might diverge across wild populations of the same species. The preprint of Thomas O’Leary and Brent Lockwood therefore focuses on shorter timescales, such as hundreds to thousands of generations in Drosophila, which might be relevant to local adaptation in wild populations. The authors examine whether intraspecific variation in maternal and zygotic gene expression is primarily maintained by stabilizing or directional selection.

Experimental design

To appreciate the authors’ definitions of stabilizing and directional selection, it is necessary to understand the experimental design. The study compared two natural populations of Drosophila from different environments, one from the tropical St. Kitts and the other from the temperate Vermont. These populations were crossed reciprocally, so each population served as both the maternal and paternal genotype. Different crossing schemes were required to generate F2 offspring, which were used to estimate the neutral level of transcriptional variation.

Experimental design to identify stabilising vs. directional selection (adapted from preprint Supplementary Figure 1)

Using the F2 offspring, the authors examined gene expression at two developmental stages: Bownes’ stage 2, representing maternal activity; and Bownes’ stage 5, representing zygotic expression after the maternal-to-zygotic transition. This approach enabled the authors to compare gene expression before and after genetic control shifted from maternal regulation to zygotic transcription.

With this experimental setup, expression differences could be quantified and compared between the parental populations, with the neutral expectation estimated from the F2 hybrids. This allowed the authors to determine whether each gene is consistent with stabilizing or directional selection. Under directional selection, the parental populations show greater expression divergence than expected from the F2 hybrids, whereas stabilizing selection is indicated when parental divergence is less than the transcriptional variation among F2 embryos.

Key findings

From my perspective, perhaps the most surprising finding was that directional selection was more common than stabilizing selection across the embryonic transcriptome. It suggests that adaptive changes in gene regulation might occur more often than previously thought.

Maternally deposited transcripts were more likely to show signatures of selection than zygotically expressed transcripts, with 10.2% of maternal genes and 5.4% of zygotic genes affected. This raises an interesting point, suggesting that embryogenesis may offer greater evolutionary flexibility than expected. Only a small number of genes were under selection during both developmental stages, indicating that the maternal-to-zygotic transition involves not only a regulatory change but also a shift in the evolutionary pressures shaping gene expression.

Another fascinating finding was that although directional selection dominated the genome-wide pattern, genes involved in fundamental developmental processes were primarily associated with more stabilizing expression patterns. This indicates that expression levels should be maintained near optimal levels, since these zygotic genes regulate essential processes such as axis formation and tissue specification. Therefore, stabilizing selection likely contributes to the robustness of embryonic development while allowing other parts of the transcriptome to evolve more freely.

Building on these findings, the authors compared tropical and temperate populations to assess the potential for local adaptation. This prompted them to examine heat-shock proteins more closely. Heat-shock proteins stabilize newly synthesized or damaged proteins after exposure to stressful conditions and help ensure proper folding. Several heat-shock genes displayed patterns of directional selection. Maternal heat-shock genes showed higher expression in the St. Kitts population, whereas several zygotic heat-shock genes were more highly expressed in embryos from Vermont. These contrasting expression patterns indicate that different stages of embryogenesis might respond independently to environmental conditions experienced by natural populations. However, the authors note that the zygotic heat-shock genes were activated after the peak of the most heat-sensitive phase of embryogenesis and may therefore be more related to later developmental physiological needs than to early embryonic heat tolerance.

Alongside heat-shock proteins, genes of the piRNA pathway also showed signatures of directional selection. Interestingly, many of these genes displayed higher expression in the Vermont population. This difference might be due to greater thermal variation in temperate regions. The authors therefore conclude that increased activity of the piRNA pathway may buffer embryos against temperature-induced transposon activity. However, this hypothesis remains to be tested experimentally.

Importance of the findings

This study offers valuable insights into how gene regulation evolves during early development. The chosen approach, comparing natural variation within a single species, enables us to observe evolutionary change in gene expression. The study establishes a solid framework for distinguishing directional from stabilizing selection.

I think this preprint offers an interesting perspective on ongoing intraspecific variation and microevolutionary processes. I appreciate its emphasis on how gene expression among natural populations of the same species differs, rather than focusing only on differences between species that have evolved over millions of years. I also like the idea that this perspective can be applied to early developmental processes, offering the opportunity to examine evolutionary processes in a developmental context. While I found it quite challenging to follow, as a bachelor’s student with a limited background in evolutionary genetics and statistical methods, I think the approach in this preprint provides valuable insights into how selection can act on embryonic gene regulation and how this might contribute to evolutionary change.

Questions for the authors

  1. Your experimental design is based on divergence between two natural populations. To extend this further, would you expect this prevalence of directional selection to be a general feature of Drosophila melanogaster populations, rather than an adaptive consequence of the environmental differences between Vermont and St. Kitts?
  2. Several heat-shock proteins and piRNA pathway genes showed signatures of directional selection. Would you suggest that these pathways represent independent adaptive responses to thermal conditions, or could they be functionally linked?
  3. Directional selection on gene expression does not necessarily translate into phenotypic differences. Therefore, which directionally selected genes would you prioritize for functional validation, and which experimental design would you use to identify the contribution of altered gene expression to embryonic fitness?
  4. In this preprint, you focused on expression measurements taken at a constant 25°C. Do you think it would be interesting to further examine buffering systems under stressful conditions? I suppose, to test this experimentally, it would be necessary to use acute stress or fluctuating temperatures to assess the adaptive buffering function of piRNA pathways or heat-shock proteins, and such experiments may provide an opportunity to evaluate the direct contribution to developmental robustness and better fitness outcomes. What are your thoughts on this?

 

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Author's response

Brent Lockwood shared

  1. Yes, we would expect these patterns to extend to other populations. We have investigated physiological responses to temperature in the embryonic stage of D. melanogaster among broader sets of populations that span thermal gradients in North America, Europe, Africa, and Asia, and we see consistent evidence of divergence. Thus, we expect directional selection to influence gene expression in embryos across the species range.
  2. I think HSPs and the piRNA pathway are probably functionally independent of one another and yet both respond to thermal selection due to the ubiquitous effects of temperature on biochemical and cellular systems. To my knowledge, there has not been a functional link established between HSPs and the piRNA pathway. Although, it is important to note that HSPs are important regulators of cell signalling and thus may be indirectly involved in numerous pathways. So, there could be some link that we haven’t uncovered yet.
  3. In fact, it is well established that the expression of particular genes, such as HSP genes, has fitness consequences in nature. But there is much less known about local adaptation of piRNA pathway genes. Identifying directional selection in the expression of piRNA pathway genes was one of the surprising findings of the study. Thus, I would focus on the piRNA pathway genes, using targeted misexpression constructs to phenocopy expression patterns in different genetic backgrounds and assay transposable element activity in the focal animals and in subsequent generations.
  4. Yes, I think further investigating variation in transcriptomic responses to environmental stress is the logical next step. We have investigated embryonic gene expression in the context of acute heat stress, but we have never done this with a genetic approach that would allow us to infer signals of natural selection. One challenge with a developmental system is that increases in temperature speed up development. Thus, the experiment would need to be designed to accurately define the stage of the embryo and whether it has undergone the maternal-to-zygotic transition.

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