Molecular Evolution of Antigen-Processing Genes in Salamanders: Do They Coevolve with MHC Class I Genes?

Area of Science:

• Evolutionary immunology
• Molecular evolution
• Comparative genomics

Background:

• Antigen-processing genes (APGs) are crucial for presenting antigens via major histocompatibility complex class I (MHC I) molecules.
• A proposed coevolution hypothesis predicts tight linkage and positive selection for APGs alongside MHC I, particularly in ancestral gnathostomes.
• Observed variations in MHC I gene numbers across taxa challenge the simplicity of this coevolutionary model.

Purpose of the Study:

• To test the coevolution hypothesis by examining APG linkage to MHC I in urodele amphibians (salamanders).
• To assess the evolutionary pressures on APGs by searching for evidence of adaptive evolution across diverse urodele species.
• To investigate the evolutionary dynamics of APGs in salamanders, considering gene duplication, loss, and allelic variation.

Main Methods:

• Genetic linkage analysis was performed on APGs (PSMB8, PSMB9, TAP1, TAP2, TAPBP) and MHC I in Lissotriton newts.
• Phylogenetic and molecular evolutionary analyses were conducted on APGs from 42 urodele species to detect positive selection.
• Comparative genomic approaches were used to identify gene duplications, losses, and divergent lineages within APGs.

Main Results:

• Five key APGs were found to be tightly linked (<0.5 cM) to MHC I in Lissotriton newts, supporting the linkage prediction.
• While some APG codons showed episodic positive selection, a pervasive signal consistent with strong coevolutionary adaptation was not detected.
• Significant evolutionary dynamics, including gene duplications, putative losses, and divergent allelic lineages, were observed in urodele APGs.

Conclusions:

• The tight linkage of APGs to MHC I in urodeles is consistent with part of the coevolution hypothesis.
• The limited evidence for pervasive positive selection suggests that APG-MHC I coevolution in salamanders may be more complex than initially proposed.
• The observed gene duplications, losses, and allelic variations highlight the dynamic evolutionary history of APGs in this amphibian group.