Large-scale coding sequence change underlies the evolution of postdevelopmental novelty in honey bees

Area of Science:

• Evolutionary biology
• Developmental biology
• Genomics

Background:

• The relative importance of coding versus regulatory genetic changes in driving evolutionary novelty is a key unresolved question.
• The evo-devo field emphasizes regulatory changes in early development, but their role in adult phenotypic novelty is less clear.

Purpose of the Study:

• To investigate the extent to which post-developmental novelty in adult organisms arises from changes in gene coding regions.
• To explore the characteristics of genes underlying novel adult phenotypes in the honey bee.

Main Methods:

• Conducted ten RNA-Sequencing (RNA-Seq) experiments in honey bees.
• Analyzed gene expression in both novel and conserved tissues.
• Examined gene expression networks and evolutionary selection pressures.

Main Results:

• Positively selected, highly expressed, tissue-specific genes are crucial for novel adult physiological functions, often being taxonomically restricted genes (TRGs).
• Genes under positive selection, including TRGs and conserved genes, exhibit low connectivity within gene expression networks.
• Contrary to evo-devo predictions, low network connectivity facilitates rapid coding sequence evolution for specialized functions in adult novelty.

Conclusions:

• The evo-devo paradigm, emphasizing regulatory changes and network constraints, is insufficient to explain post-developmental novelty.
• Adult phenotypic evolution follows distinct rules, where coding sequence changes in lowly connected genes drive rapid adaptation and specialized functions.