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 phylogenetic reconstruction. We tested the effects of different data sets (mitochondrial, nuclear, nucleotides, amino acids, concatenated genes, individual genes, gene orders), phylogenetic algorithms (assuming data homogeneity, heterogeneity, and heterotachy), and partitioning; and found that almost all of them produced unique topologies. As we also found that mitogenomes of Asellota and two 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 managed to attenuate some of these artifacts (and outperform partitioning), mitochondrial data have limited applicability for reconstructing the phylogeny of Isopoda. Regardless of this, our analyses allowed us to propose solutions 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.

Keywords: Cymothoida; GC skew; base composition skew; compositional heterogeneity; mitochondrial phylogenomics; replication origin inversion.

Fig. 1.

—Mitochondrial phylogenomics of Isopoda (suborder information shown) reconstructed using partitioned nucleotide sequences of PCGs and rRNAs (NUC data set) and BI algorithm. A set of nine nonisopod Malacostraca species and Limulus polyphemus were used as outgroups (order information shown). The scale bar corresponds to the estimated number of substitutions per site. Bayesian posterior support values are shown next to corresponding nodes. Star sign indicates a putative origin of replication inversion scenario implied by the topology (see Discussion).

Fig. 2.

—A phylogram reconstructed using nonpartitioned NUC data set and an algorithm designed to address compositional heterogeneity: CAT-GTR (PB). Posterior Bayesian support values are shown. See figure 1 for other details.

Fig. 3.

—A phylogram reconstructed using amino acid data set (AAs; 13 PCGs) in combination with data partitioning strategy and BI algorithm. See figure 1 for other details.

Fig. 4.

—A phylogram reconstructed using AAs data set and CAT-GTR algorithm designed for heterogeneous data sets (PB). See figure 1 for other details.

Fig. 5.

—A phylogram inferred using the nuclear 18S gene and CAT-GTR algorithm (PB). See figure 1 for other details.

Fig. 6.

—Cumulative GC skews of the majority strands of a selected subset of mitogenomes used for phylogenetic analyses.