Mitochondrial architecture rearrangements produce asymmetrical nonadaptive mutational pressures that subvert the phylogenetic reconstruction in isopoda

Abstract

The phylogeny of Isopoda, a speciose order of crustaceans, remains unresolved, with different data sets (morphological, nuclear, mitochondrial) often producing starkly incongruent phylogenetic hypotheses. We hypothesized that extreme diversity in their life histories might be causing compositional heterogeneity/heterotachy in their mitochondrial genomes, and compromising the phylogeneticreconstruction.Wetestedtheeffectsofdifferentdatasets(mitochondrial,nuclear,nucleotides,aminoacids, concatenated genes, individual genes, gene orders), phylogenetic algorithms (assuming data homogeneity, heterogeneity, and heterotachy), and partitioning; andfoundthat almost allofthemproduceduniquetopologies.Aswe alsofoundthatmitogenomesofAsellota andtwo Cymothoida families (Cymothoidae and Corallanidae) possess inversed base (GC) skew patterns in comparison to other isopods, we concluded that inverted skews cause long-branch attraction phylogenetic artifacts between these taxa. These asymmetrical skews are most likely driven by multiple independent inversions of origin of replication (i.e., nonadaptive mutational pressures). Although the PhyloBayes CAT-GTR algorithm managedto attenuate some ofthese artifacts (and outperform partitioning), mitochondrial data have limited applicabilityforreconstructingthephylogenyof Isopoda.Regardlessofthis,our analyses allowedustoproposesolutions to some unresolved phylogenetic debates, and support Asellota are the most likely candidate for the basal isopod branch. As our findings show that architectural rearrangements might produce major compositional biases even on relatively short evolutionary timescales, the implications are that proving the suitability of data via composition skew analyses should be a prerequisite for every study that aims to use mitochondrial data for phylogenetic reconstruction, even among closely related taxa.