Mitochondrial Phylogenomics Research Articles

Improving Evolutionary Models for Mitochondrial Protein Data with Site-Class Specific Amino Acid Exchangeability Matrices

Adequate modeling of mitochondrial sequence evolution is an essential component of mitochondrial phylogenomics (comparative mitogenomics). There is wide recognition within the field that lineage-specific aspects of mitochondrial evolution should be accommodated through lineage-specific amino-acid exchangeability matrices (e.g., mtMam for mammalian data). However, such a matrix must be applied to all sites and this implies that all sites are subject to the same, or largely similar, evolutionary constraints. This assumption is unjustified. Indeed, substantial differences are expected to arise from three-dimensional structures that impose different physiochemical environments on individual amino acid residues. The objectives of this paper are (1) to investigate the extent to which amino acid evolution varies among sites of mitochondrial proteins, and (2) to assess the potential benefits of explicitly modeling such variability. To achieve this, we developed a novel method for partitioning sites based on amino acid physiochemical properties. We apply this method to two datasets derived from complete mitochondrial genomes of mammals and fish, and use maximum likelihood to estimate amino acid exchangeabilities for the different groups of sites. Using this approach we identified large groups of sites evolving under unique physiochemical constraints. Estimates of amino acid exchangeabilities differed significantly among such groups. Moreover, we found that joint estimates of amino acid exchangeabilities do not adequately represent the natural variability in evolutionary processes among sites of mitochondrial proteins. Significant improvements in likelihood are obtained when the new matrices are employed. We also find that maximum likelihood estimates of branch lengths can be strongly impacted. We provide sets of matrices suitable for groups of sites subject to similar physiochemical constraints, and discuss how they might be used to analyze real data. We also discuss how the general approach might be employed to improve a variety of mitogenomic-based research activities.

Crawling through time: Transition of snails to slugs dating back to the Paleozoic, based on mitochondrial phylogenomics

Sea slugs (Gastropoda: Opisthobranchia) are characterized by extensive morphological homoplasy. In particular, reduced or absent shells are predominant throughout the group. This trend towards shell loss has resulted in a poor fossil record. DNA-based phylogenies have been helpful in improving our understanding of the evolution of this group and major clades are emerging. We report 13 new complete opisthobranch mitochondrial genomes that provide robust support for some of these emerging nodes. We name three new clades within the Opisthobranchia, the Actopleura (Acteonoidea plus Nudipleura), Placoesophaga (Cephalaspidea plus Anaspidea), and Siphoglossa (Sacoglossa plus the Siphonaria). Finally we use molecular clock dating that suggests an earlier opisthobranch divergence than previously reported. The implications of this evolutionary scenario are discussed.

When phylogenetic assumptions are violated: base compositional heterogeneity and among-site rate variation in beetle mitochondrial phylogenomics

The ability to generate large molecular datasets for phylogenetic studies benefits biologists, but such data expansion introduces numerous analytical problems. A typical molecular phylogenetic study implicitly assumes that sequences evolve under stationary, reversible and homogeneous conditions, but this assumption is often violated in real datasets. When an analysis of large molecular datasets results in unexpected relationships, it often reflects violation of phylogenetic assumptions, rather than a correct phylogeny. Molecular evolutionary phenomena such as base compositional heterogeneity and among-site rate variation are known to affect phylogenetic inference, resulting in incorrect phylogenetic relationships. The ability of methods to overcome such bias has not been measured on real and complex datasets. We investigated how base compositional heterogeneity and among-site rate variation affect phylogenetic inference in the context of a mitochondrial genome phylogeny of the insect order Coleoptera. We show statistically that our dataset is affected by base compositional heterogeneity regardless of how the data are partitioned or recoded. Among-site rate variation is shown by comparing topologies generated using models of evolution with and without a rate variation parameter in a Bayesian framework. When compared for their effectiveness in dealing with systematic bias, standard phylogenetic methods tend to perform poorly, and parsimony without any data transformation performs worst. Two methods designed specifically to overcome systematic bias, LogDet and a Bayesian method implementing variable composition vectors, can overcome some level of base compositional heterogeneity, but are still affected by among-site rate variation. A large degree of variation in both noise and phylogenetic signal among all three codon positions is observed. We caution and argue that more data exploration is imperative, especially when many genes are included in an analysis.

Mitochondrial phylogenomics of the Bivalvia (Mollusca): searching for the origin and mitogenomic correlates of doubly uniparental inheritance of mtDNA

BackgroundDoubly uniparental inheritance (DUI) is an atypical system of animal mtDNA inheritance found only in some bivalves. Under DUI, maternally (F genome) and paternally (M genome) transmitted mtDNAs yield two distinct gender-associated mtDNA lineages. The oldest distinct M and F genomes are found in freshwater mussels (order Unionoida). Comparative analyses of unionoid mitochondrial genomes and a robust phylogenetic framework are necessary to elucidate the origin, function and molecular evolutionary consequences of DUI. Herein, F and M genomes from three unionoid species, Venustaconcha ellipsiformis, Pyganodon grandis and Quadrula quadrula have been sequenced. Comparative genomic analyses were carried out on these six genomes along with two F and one M unionoid genomes from GenBank (F and M genomes of Inversidens japanensis and F genome of Lampsilis ornata).ResultsCompared to their unionoid F counterparts, the M genomes contain some unique features including a novel localization of the trnH gene, an inversion of the atp8-trnD genes and a unique 3'coding extension of the cytochrome c oxidase subunit II gene. One or more of these unique M genome features could be causally associated with paternal transmission. Unionoid bivalves are characterized by extreme intraspecific sequence divergences between gender-associated mtDNAs with an average of 50% for V. ellipsiformis, 50% for I. japanensis, 51% for P. grandis and 52% for Q. quadrula (uncorrected amino acid p-distances). Phylogenetic analyses of 12 protein-coding genes from 29 bivalve and five outgroup mt genomes robustly indicate bivalve monophyly and the following branching order within the autolamellibranch bivalves: ((Pteriomorphia, Veneroida) Unionoida).ConclusionThe basal nature of the Unionoida within the autolamellibranch bivalves and the previously hypothesized single origin of DUI suggest that (1) DUI arose in the ancestral autolamellibranch bivalve lineage and was subsequently lost in multiple descendant lineages and (2) the mitochondrial genome characteristics observed in unionoid bivalves could more closely resemble the DUI ancestral condition. Descriptions and comparisons presented in this paper are fundamental to a more complete understanding regarding the origins and consequences of DUI.