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 datasets often producing starkly incongruent phylogenetic hypotheses. We hypothesised 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 datasets (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 artefacts 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 artefacts (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 can produce major compositional biases even on 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.

New insights into Oniscidea (Crustacea: Isopoda) mitogenome structural features and phylogenetic placement of targeted taxa using mitogenomic and nuclear data

“…Solely based on mitochondrial data recently published works failed to support the monophyly of Oniscidea [20,21,51]. The monophyly of Oniscidea mainly relies on the phylogenetic origin of the key genera Ligia, Ligidium, Tylos and Helleria whose close evolutionary relationship with marine ancestors was repeatedly highlighted in the past [9,15,22]. Therefore, two species of the genus Ligia were added in this paper to explore the monophyly of the suborder Oniscidea.…”

“…Furthermore, these loci were translated in AA sequences and run under a heterogeneous CAT-GTR model. In this way we avoided phylogenetic artifacts attributed to biases due to similar GC skews among distant taxa [22]. On the other hand, nuclear non-coding genes were treated with Gblocks in order to eliminate poorly aligned regions.…”

“…Monophyly of Oniscidea have been questioned by several phylogenetic analyses including molecular data [9,14,22,23,58]. Solely based on mitochondrial data recently published works failed to support the monophyly of Oniscidea [20,21,51].…”

“…Although a series of synapomorphies have been proposed to support the monophyly of the group [7,8,10,12,13], molecular phylogenetic analyses have questioned the common origin of all Oniscidea and also recovered varied topologies for the relationship of oniscids to other isopods [9,[14][15][16][17][18][19][20][21][22][23]. Recently, in a study based on four highly conserved nuclear genes Dimitriou et al (2019) failed to recover a monophyletic Oniscidea, with Ligia recovered with valviferan and sphaeromatid isopods.…”

“…Isopods mitogenomes exhibit substantial diversity and unusual structures with unique linear/circular organization in some oniscids and inverted GC skew in cymothoids [39,40]. The majority of isopods studied exhibit an inversed strand asymmetry (positive GC skew), while a negative GC skew in some is attributed to double-inversion [22,23]. So far mitogenomic data are currently available for only 10 Oniscidea, including one species of Ligia (Table 1).…”