Limited directional selection but coevolutionary signals among imprinted genes in A. lyrata

Genomic imprinting is a form of gene regulation leading to the unequal expression of maternal and paternal alleles. The main hypothesis invoked to explain the evolution of imprinted genes is the kinship theory, which posits a conflict between parental genomes over resource allocation in progeny. According to this theory, imprinted genes are expected to undergo a shift from balancing to directional selection, in coding or regulatory regions. However, most studies addressing selection in imprinted genes have focused on self-fertilizing species, where conflicts over resource allocation are predicted to be weak. Consequently, the impact of kinship theory on the evolution of imprinted genes remains largely untested. Furthermore, the predicted coevolution between certain imprinted genes under kinship theory has not been tested yet empirically.

Combined phylogenetic and population genomic approaches, we investigated signatures of selection on imprinted genes across the Brassicaceae family and in autogamous and allogamous populations of Arabidopsis lyrata , and searched for evidence of coevolution among imprinted genes. We found that endosperm-expressed genes exhibited signals of balancing selection across Brassicaceae and within allogamous populations, consistent with unresolved intralocus conflicts. Supporting the kinship theory, these signals varied with mating system. Moreover, phylogenetic analyses further indicated negative directional selection acting on imprinted genes. However, population-level signals were independent of mating system and showed limited concordance with kinship predictions, possibly due to stronger selection acting on expression than on coding sequences. Finally, we identified coevolution between imprinted genes, although not at specific sites, suggesting that interactions beyond protein sequence drive this process.