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

Abstract

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, such conflicts select for parent-of-origin–dependent expression of genes involved in resource allocation. How such conflicts translate into signatures of selection at coding or regulatory sequences remains model-dependent and is not explicitly predicted by the kinship theory. However, most studies addressing selection in imprinted genes in flowering plants, particularly those based on population-genomic or phylogenetic analyses, have focused on self-fertilizing species, where conflicts over resource allocation are predicted to be weak. Consequently, the impact of the kinship theory on the evolution of imprinted genes remains largely unexplored in systems where parental conflict is expected to be strong. Furthermore, potential coevolution between antagonistically acting imprinted genes, as proposed in extensions of parental conflict models, has not yet been tested empirically. Using 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 models of unresolved intralocus conflict. These population-level signals varied with the mating system, in line with expectations that parental conflict is reduced under self-fertilization. Moreover, phylogenetic analyses indicated signatures of purifying (negative) selection acting on imprinted genes. However, the population-level signatures of selection were independent of the 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 may contribute to this process.

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