Deciphering the origin of developmental stability : The role of intracellular expression variability in evolutionary conservation

© 2024 Wiley Periodicals LLC..

Progress in evolutionary developmental biology (evo-devo) has deepened our understanding of how intrinsic properties of embryogenesis, along with natural selection and population genetics, shape phenotypic diversity. A focal point of recent empirical and theoretical research is the idea that highly developmentally stable phenotypes are more conserved in evolution. Previously, we demonstrated that in Japanese medaka (Oryzias latipes), embryonic stages and genes with high stability, estimated through whole-embryo RNA-seq, are highly conserved in subsequent generations. However, the precise origin of the stability of gene expression levels evaluated at the whole-embryo level remained unclear. Such stability could be attributed to two distinct sources: stable intracellular expression levels or spatially stable expression patterns. Here we demonstrate that stability observed in whole-embryo RNA-seq can be attributed to stability at the cellular level (low variability in gene expression at the cellular levels). We quantified the intercellular variations in expression levels and spatial gene expression patterns for seven key genes involved in patterning dorsoventral and rostrocaudal regions during early development in medaka. We evaluated intracellular variability by counting transcripts and found its significant correlation with variation observed in whole-embryo RNA-seq data. Conversely, variation in spatial gene expression patterns, assessed through intraindividual left-right asymmetry, showed no correlation. Given the previously reported correlation between stability and conservation of expression levels throughout embryogenesis, our findings suggest a potential general trend: the stability or instability of developmental systems-and the consequent evolutionary diversity-may be primarily anchored in intrinsic fundamental elements such as the variability of intracellular states.

Medienart:

E-Artikel

Erscheinungsjahr:

2024

Erschienen:

2024

Enthalten in:

Zur Gesamtaufnahme - volume:26

Enthalten in:

Evolution & development - 26(2024), 2 vom: 27. März, Seite e12473

Sprache:

Englisch

Beteiligte Personen:

Uchida, Yui [VerfasserIn]
Tsutsumi, Masato [VerfasserIn]
Ichii, Shunsuke [VerfasserIn]
Irie, Naoki [VerfasserIn]
Furusawa, Chikara [VerfasserIn]

Links:

Volltext

Themen:

Developmental stability
Evolvability
Journal Article
Phenotypic conservation
Variability

Anmerkungen:

Date Completed 13.03.2024

Date Revised 13.03.2024

published: Print-Electronic

Citation Status MEDLINE

doi:

10.1111/ede.12473

funding:

Förderinstitution / Projekttitel:

PPN (Katalog-ID):

NLM369040406