Comparative Transcriptomics Reveals Heterochronic and Morph-Specific Gene Expression Underlying Developmental Divergence in a Marine Annelid

Core Concepts

Heterochronic shifts in gene expression timing and morph-specific gene expression contribute similarly to developmental differences between two larval morphs of the marine annelid Streblospio benedicti, with the regulatory architecture being predominantly trans-acting.

Abstract

The study examines the gene expression differences between two developmental morphs of the marine annelid Streblospio benedicti, which exhibit a developmental dimorphism. The authors use comparative RNA-seq analysis across six developmental stages to quantify the extent to which modifications to gene expression timing (heterochrony) and morph-specific gene expression contribute to the observed developmental differences.
Key findings:

Only a small proportion (36.2%) of expressed genes are differentially expressed between the two morphs at any stage, despite major differences in larval development and life-history.
Heterochronic shifts in gene expression timing and morph-specific gene expression contribute similarly to the developmental differences, with 29% and 25.3% of differentially expressed genes falling into these categories, respectively.
The regulatory architecture underlying the gene expression differences is predominantly trans-acting, suggesting that early divergence is driven by a few highly pleiotropic trans-acting factors.
Reciprocal F1 crosses show that maternal effects are limited to early development, with most parental effects disappearing by the gastrula stage.
The authors conclude that both novel gene expression and heterochronic shifts in developmental timing are important mechanisms driving developmental evolution in this system, and that the regulatory architecture involves primarily trans-acting factors.

Stats

"Approximately 36.2% of all expressed genes are significantly differentially expressed between PP and LL at any stage in this dataset."
"We find that early in development over a third of these DE genes are significantly different between the morphs, but these differences tend to be quite small in magnitude."
"At gastrulation the number of significant genes decreases to less than 5% of the total DE genes, however these remaining expression differences are much larger in magnitude."

Quotes

"Only 36.2% of all expressed genes are significantly differentially expressed (DE) between PP and LL at any stage in this dataset."
"We find that early in development over a third of these DE genes are significantly different between the morphs, but these differences tend to be quite small in magnitude."
"At gastrulation the number of significant genes decreases to less than 5% of the total DE genes, however these remaining expression differences are much larger in magnitude."

Key Insights Distilled From

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

by Harry,N. D.,... at www.biorxiv.org 08-18-2023

https://www.biorxiv.org/content/10.1101/2023.08.18.553877v3

Deeper Inquiries

What are the specific developmental processes and pathways that are most impacted by the heterochronic and morph-specific gene expression differences observed in this study

In this study, the heterochronic and morph-specific gene expression differences impact several specific developmental processes and pathways. The heterochronic genes, which change in their expression timing between the two developmental morphs, are associated with critical developmental processes such as mesoderm specification, cell fate specification pathways, and various organogenesis pathways. These genes play a crucial role in regulating the timing of gene expression during development, influencing the differentiation of cell types and the formation of organs. On the other hand, the morph-specific genes, which are only expressed in one morph and not the other, are involved in different functional processes. In this study, the morph-specific genes expressed in the planktotrophic larvae are related to cell fate specification and signaling pathways, while those in the lecithotrophic larvae show a distinct lack of genes involved in metabolic processes. These differences in gene expression patterns contribute to the divergence in developmental processes and life-history traits between the two morphs of Streblospio benedicti.

How do the trans-acting regulatory changes identified in this study compare to the regulatory architecture underlying developmental divergence in other closely related species or across larger evolutionary timescales

The trans-acting regulatory changes identified in this study, which are the predominant mode of regulatory modification underlying the gene expression differences, provide insights into the regulatory architecture of developmental divergence within a species. Compared to regulatory architectures in other closely related species or across larger evolutionary timescales, the prevalence of trans-acting factors in early developmental stages suggests that few, highly pleiotropic regulatory modifications drive the initial divergence in gene expression and developmental processes. This finding is consistent with the idea that early in evolutionary divergence, trans-acting factors play a significant role in initiating developmental changes, while cis-acting elements may arise and refine gene expression patterns over longer evolutionary timescales. The regulatory architecture identified in this study highlights the importance of trans-acting factors in driving developmental evolution within a species.

Could the limited maternal effects observed in the F1 crosses be an adaptation to the developmental dimorphism in this species, and if so, what are the potential evolutionary implications

The limited maternal effects observed in the F1 crosses could potentially be an adaptation to the developmental dimorphism in Streblospio benedicti, with important evolutionary implications. The reduced impact of maternal effects on gene expression in the F1 offspring suggests that the developmental differences between the two morphs are primarily driven by genetic factors rather than maternal contributions. This may indicate that the species has evolved mechanisms to minimize the influence of maternal factors on developmental divergence, allowing for greater genetic control over the expression of genes associated with morphological and life-history differences. This adaptation could enhance the genetic basis of developmental divergence and facilitate the evolution of distinct developmental modes within the species. Additionally, the limited maternal effects in the F1 crosses may contribute to the maintenance of the developmental dimorphism and the stability of the two morphs over evolutionary time.