The complete mitochondrial genome of parasitic nematode Camallanus cotti: extreme discontinuity in the rate of mitogenomic architecture evolution within the Chromadorea class

Zou

et al. 2020

Preprint

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Inversions of the origin of replication (ORI) of mitochondrial genomes produce asymmetrical mutational pressures that can cause artefactual clustering in phylogenetic analyses. It is therefore an absolute prerequisite for all molecular evolution studies that use mitochondrial data to account for ORI events in the evolutionary history of their dataset. The number of ORI events in crustaceans remains unknown; several studies reported ORI events in some crustacean lineages on the basis of fully inversed (e.g. negative vs. positive) GC skew patterns, but studies of isolated lineages could have easily overlooked ORI events that produced merely a reduction in the skew magnitude. In this study, we used a comprehensive taxonomic approach to systematically study the evolutionary history of ORI events in crustaceans using all available mitogenomes and combining signals from lineage-specific skew magnitude and direction (+ or -), cumulative skew diagrams, and gene rearrangements.We inferred 24 putative ORI events (14 of which have not been proposed before): 17 with relative confidence, and 7 speculative. Most of these were located at lower taxonomic levels, but there are indications of ORIs that occurred at or above the order-level: Copepoda, Isopoda, and putatively in Branchiopoda and Poecilostomatida+Cyclopoida. Several putative ORI events did not result in fully inversed skews. In many lineages skew plots were not informative for the prediction of replication origin and direction of mutational pressures, but inversions of the mitogenome fragment comprising the ancestral CR (rrnS-CR-trnI) were rather good predictors of skew inversions. We also found that skew plots can be a useful tool to indirectly infer the relative strengths of mutational/purifying pressures in some crustacean lineages: when purifying pressures outweigh mutational, GC skew plots are strongly affected by the strand distribution of genes, and when mutational > purifying, GC skew plots can be even completely (apparently) unaffected by the strand distribution of genes. This observation has very important repercussions for phylogenetic and evolutionary studies, as it implies that not only the relatively rare ORI events, but also much more common gene strand switches and same-strand rearrangements can produce mutational bursts, which in turn affect phylogenetic and evolutionary analyses. We argue that such compositional biases may produce misleading signals not only in phylogenetic but also in other types of evolutionary analyses (dN/dS ratios, codon usage bias, base composition, branch length comparison, etc.), and discuss several such examples. Therefore, all studies aiming to study the evolution of mtDNA sequences should pay close attention to architectural rearrangements.

Section: Astacidea (Superfamily)supporting

confidence: 82%

Section: No Class Subclass Order Suborder/family Genus/species Gc Comentioning

confidence: 61%

Evolutionary history of inversions in the direction of architecture-driven mutational pressures in crustacean mitochondrial genomes

Zou

et al. 2020

Preprint

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“…Similarly, gene orders produced topological instability, very low support, and almost nonsensical topologies, with paraphyletic Isopoda. As highly rearranged gene orders were at the base of the isopod clade, we hypothesise that the discontinuous evolution of mitogenomic architecture evolution (Zou et al, 2017) produces phylogenetic artefacts, such as LBA. This corroborates the hypothesis that gene orders are not a useful phylogenetic marker in lineages exhibiting destabilised mitogenomic architecture (Zhang et al, 2017; Zou et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

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

Zou

Hua

et al. 2019

Preprint

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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.

“…Amplification reaction mixture and conditions used were described before [17]; briefly: 50μL with 5 U/μL of TaKaRa LA Taq polymerase (TaKaRa, Japan), 10×LATaq Buffer II, 2.5μM dNTP mixture, 0.2–1.0μM each primer, 60ng DNA template. Conditions: denaturation 98°C/2min, and 40 cycles of 98°C/10s, 50°C/15s, 68°C/1min per kb.…”

Section: Methodsmentioning

confidence: 99%

“…All obtained fragments were quality-proofed by visually inspecting the electropherograms and BLASTed [47] to confirm that the amplicon is the actual target sequence. Mitogenome was assembled, annotated, and comparative analyses conducted, roughly as described previously [17,48]. Briefly: assembly was conducted manually using DNAstar v7.1 [49].…”

Section: Methodsmentioning

confidence: 99%

The complete mitochondrial genome of Cymothoa indica has a highly rearranged gene order and clusters at the very base of the Isopoda clade

et al. 2018

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As a result of great diversity in life histories and a large number of described species, taxonomic and phylogenetic uncertainty permeates the entire crustacean order of Isopoda. Large molecular datasets capable of providing sufficiently high phylogenetic resolution, such as mitochondrial genomes (mitogenomes), are needed to infer their evolutionary history with confidence, but isopod mitogenomes remain remarkably poorly represented in public databases. We sequenced the complete mitogenome of Cymothoa indica, a species belonging to a family from which no mitochondrial genome was sequenced yet, Cymothoidae. The mitogenome (circular, 14484 bp, A+T = 63.8%) is highly compact, appears to be missing two tRNA genes (trnI and trnE), and exhibits a unique gene order with a large number of rearrangements. High compactness and the existence of palindromes indicate that the mechanism behind these rearrangements might be associated with linearization events in its evolutionary history, similar to those proposed for isopods from the Armadillidium genus (Oniscidea). Isopods might present an important model system to study the proposed discontinuity in the dynamics of mitochondrial genomic architecture evolution. Phylogenetic analyses (Bayesian Inference and Maximum Likelihood) conducted using nucleotide sequences of all mitochondrial genes resolved Oniscidea and Cymothoida suborders as paraphyletic. Cymothoa indica was resolved as a sister group (basal) to all remaining isopods, which challenges the accepted isopod phylogeny, where Cymothoida are the most derived, and Phreatoicidea the most basal isopod group. There is growing evidence that Cymothoida suborder might be split into two evolutionary distant clades, with parasitic species being the most basal split in the Isopoda clade, but a much larger amount of molecular resources carrying a high phylogenetic resolution will be needed to infer the remarkably complex evolutionary history of this group of animals with confidence.