Detecting signals of adaptive evolution in grape plastomes with a focus on the Cretaceous-Palaeogene (K/Pg) transition

Abstract

Background and aims: Although plastid genes are widely used in phylogenetic studies, signals of positive selection have been scarcely investigated in the grape family. The plastomes from 91 accessions of Vitaceae were examined to understand the extent to which positive selection is present and to identify which genes are involved. Moreover, the changes through time of genes under episodic positive selection were investigated and the hypothesis of an adaptive process following the Cretaceous-Palaeogene (K/Pg) transition about 66 million years ago was tested.

Methods: Different codon-substitution models were used to assess pervasive and episodic positive selection events on 70 candidate plastid genes. Divergence times between lineages were estimated and stochastic character mapping analysis was used to simulate variation over time of the genes found to be under episodic positive selection.

Key results: A total of 20 plastid genes (29 %) showed positive selection. Among them, 14 genes showed pervasive signatures of positive selection and nine genes showed episodic signatures of positive selection. In particular, four of the nine genes (psbK, rpl20, rpoB, rps11) exhibited a similar pattern showing an increase in the rate of variation close to the K/Pg transition.

Conclusion: Multiple analyses have shown that the grape family has experienced ancient and recent positive selection events and that the targeted genes are involved in essential functions such as photosynthesis, self-replication and metabolism. Our results are consistent with the idea that the K/Pg transition has favoured an increased rate of change in some genes. Intense environmental perturbations have influenced the rapid diversification of certain lineages, and new mutations arising on some plastid genes may have been fixed by natural selection over the course of many generations.

Keywords: Vitis vinifera; Adaptive evolution; Cretaceous–Palaeogene; Vitaceae; episodic selection; grape; mass extinction; plastid genes; plastomes; positive selection.