Proceedings of the Royal Society B: Biological Sciences
Restricted accessResearch articles

Genetic independence between traits separated by metamorphosis is widespread but varies with biological function

Julie M. Collet

Julie M. Collet

CBGP, Univ Montpellier, CIRAD, INRAE, Institut Agro, IRD, Montpellier, France

[email protected]

Contribution: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Validation, Visualization, Writing – original draft, Writing – review & editing

Google Scholar

Find this author on PubMed

,
Sabine Nidelet

Sabine Nidelet

CBGP, Univ Montpellier, CIRAD, INRAE, Institut Agro, IRD, Montpellier, France

Contribution: Methodology, Resources, Supervision, Writing – review & editing

Google Scholar

Find this author on PubMed

and
Simon Fellous

Simon Fellous

CBGP, Univ Montpellier, CIRAD, INRAE, Institut Agro, IRD, Montpellier, France

Contribution: Conceptualization, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Writing – original draft, Writing – review & editing

Google Scholar

Find this author on PubMed

Published:https://doi.org/10.1098/rspb.2023.1784

Why is metamorphosis so pervasive? Does it facilitate the independent (micro)evolution of quantitative traits in distinct life stages, similarly to how it enables some limbs and organs to develop at specific life stages? We tested this hypothesis by measuring the expression of 6400 genes in 41 Drosophila melanogaster inbred lines at larval and adult stages. Only 30% of the genes showed significant genetic correlations between larval and adult expression. By contrast, 46% of the traits showed some level of genetic independence between stages. Gene ontology terms enrichment revealed that across stages correlated traits were often involved in proteins synthesis, insecticide resistance and innate immunity, while a vast number of genes expression traits associated with energy metabolism were independent between life stages. We compared our results to a similar case: genetic constraints between males and females in gonochoric species (i.e. sexual antagonism). We expected selection for the separation between males and females to be higher than between juvenile and adult functions, as gonochorism is a more common strategy in the animal kingdom than metamorphosis. Surprisingly, we found that inter-stage constraints were lower than inter-sexual genetic constraints. Overall, our results show that metamorphosis enables a large part of the transcriptome to evolve independently at different life stages.

Footnotes

Present address: INRAE, Université de Tours, BOA, Nouzilly, France.

Electronic supplementary material, is available online at https://doi.org/10.6084/m9.figshare.c.6887658.

References