Capturing the Phylogeny of Holometabola with Mitochondrial Genome Data and Bayesian Site-Heterogeneous Mixture Models

Abstract

After decades of debate, a mostly satisfactory resolution of relationships among the 11 recognized holometabolan orders of insects has been reached based on nuclear genes, resolving one of the most substantial branches of the tree-of-life, but the relationships are still not well established with mitochondrial genome data. The main reasons have been the absence of sufficient data in several orders and lack of appropriate phylogenetic methods that avoid the systematic errors from compositional and mutational biases in insect mitochondrial genomes. In this study, we assembled the richest taxon sampling of Holometabola to date (199 species in 11 orders), and analyzed both nucleotide and amino acid data sets using several methods. We find the standard Bayesian inference and maximum-likelihood analyses were strongly affected by systematic biases, but the site-heterogeneous mixture model implemented in PhyloBayes avoided the false grouping of unrelated taxa exhibiting similar base composition and accelerated evolutionary rate. The inclusion of rRNA genes and removal of fast-evolving sites with the observed variability sorting method for identifying sites deviating from the mean rates improved the phylogenetic inferences under a site-heterogeneous model, correctly recovering most deep branches of the Holometabola phylogeny. We suggest that the use of mitochondrial genome data for resolving deep phylogenetic relationships requires an assessment of the potential impact of substitutional saturation and compositional biases through data deletion strategies and by using site-heterogeneous mixture models. Our study suggests a practical approach for how to use densely sampled mitochondrial genome data in phylogenetic analyses.

Higher‐level phylogeny and evolutionary history of Pentatomomorpha (Hemiptera: Heteroptera) inferred from mitochondrial genome sequences

“…Several other studies have suggested that model adequacy is critical for accurate tree reconstruction in insect mitochondrial phylogenomics. The site-heterogeneous mixture model implemented in phylobayes can provide greater flexibility for modelling different classes of sites, reducing systematic errors (Li et al, 2015;Timmermans et al, 2015;Song et al, 2016b;Feuda et al, 2017;Wang et al, 2017;Liu et al, 2018). phylobayes analyses with the CAT + GTR model recovered a Lygaeoidea + Pyrrhocoroidea clade.…”

The phylogeny of Galerucinae (Coleoptera: Chrysomelidae) and the performance of mitochondrial genomes in phylogenetic inference compared to nuclear rRNA genes

“…The Phy-loBayes software implements the CAT model, which uses a variable number of rate categories that each are defined by different equilibrium frequencies of nucleotide or amino acid characters estimated from the empirical data (Lartillot and Philippe, 2004). This model is less susceptible to long-branch attraction from compositional and rate biases (Lartillot et al, 2007;Talavera and Vila, 2011;Song et al, 2016). In addition, we removed 3rd codon positions to assess the confounding effects from these fastest evolving markers.…”

“…The effort required for sequencing full mitogenomes has dropped dramatically with the possibility to assemble these sequences from mixtures of specimens that are shotgun-sequenced either from long-range PCR products (Timmermans et al, 2010) or directly from total genomic DNA (Gillett et al, 2014;Crampton-Platt et al, 2015;Tang et al, 2015;Breeschoten et al, 2016). The approach has been applied to resolve various phylogenetic questions in entomology at taxonomic levels from within families to interordinal relationships (Timmermans et al, 2010(Timmermans et al, , 2016bLi et al, 2012;Wan et al, 2012;Gillett et al, 2014;G omez-Rodriguez et al, 2015;Song et al, 2016).…”

Fossil Calibrations for the Arthropod Tree of Life

“…Support for monophyly comes from phylogenetic analysis of transcriptomes Peters et al, 2014) and morphology . A recent analysis of mitochondrial genomes finds Amphiesmenoptera within Antliophora under some analytical conditions, potentially challenging antliophoran monophyly (Song et al, 2016).…”