Evolutionary history of inversions in directional mutational pressures in crustacean mitochondrial genomes: Implications for evolutionary studies

Abstract

Inversions of the origin of replication (ORI) in mitochondrial genomes produce asymmetrical mutational pressures that can cause strong base composition skews. Due to skews often being overlooked, the total number of crustacean lineages that underwent ORI events remains unknown. We analysed skews, cumulative skew plots, conserved sequence motifs, and mitochondrial architecture of all 965 available crustacean mitogenomes (699 unique species). We found indications of an ORI in 159 (22.7%) species, and mapped these to 23 ORI events: 16 identified with confidence and 7 putative (13 newly proposed, and for 5 we improved the resolution). Two ORIs occurred at or above the order level: Isopoda and Copepoda. Shifts in skew plots are not a precise tool for identifying the replication mechanism. We discuss how ORIs can produce mutational bursts in mitogenomes and show how these can interfere with various types of evolutionary studies. Phylogenetic analyses were plagued by artefactual clustering, and ORI lineages exhibited longer branches, a higher number of synonymous substitutions, higher mutational saturation, and higher compositional heterogeneity. ORI events also affected codon usage and protein properties. We discuss how this may have caused erroneous interpretation of data in previous studies that did not account for skew patterns.

Keywords: Base composition skew; Inversed skew; Long-branch attraction; Mitochondrial architecture; Nonadaptive evolution; Origin of replication.