Phylogenomic analyses clarify the pattern of evolution of Adephaga (Coleoptera) and highlight phylogenetic artefacts due to model misspecification and excessive data trimming

Abstract

Adephaga is the second largest suborder of Coleoptera and contains aquatic and terrestrial groups that are sometimes classified as Hydradephaga and Geadephaga, respectively. The phylogenetic relationships of Adephaga have been studied intensively, but the relationships of the major subgroups of Geadephaga and the placement of Hygrobiidae within Dytiscoidea remain obscure. Here, we infer new DNA‐hybridization baits for exon‐capture phylogenomics and we combine new hybrid‐capture sequence data with transcriptomes to generate the largest phylogenomic taxon sampling within Adephaga presented to date. Our analyses show that the new baits are suitable to capture the target loci across different lineages of Adephaga. Phylogenetic analyses of moderately trimmed supermatrices confirm the hypothesis of paraphyletic ‘Hydradephaga’, with Gyrinidae placed as sister to all other families as in morphology‐based phylogenies, even though quartet‐concordance analyses did not support this result. All analyses conducted with site‐heterogeneous models suggest Trachypachidae as sister to a clade Carabidae + Cicindelidae in congruence with results from morphological studies. Haliplidae is inferred as sister to Dytiscoidea, while a clade of Noteridae (+ most likely Meruidae) is inferred as sister to all remaining Dytiscoidea. A strongly supported clade Hygrobiidae + (Amphizoidae + monophyletic Aspidytidae) is inferred in most analyses of moderately trimmed supermatrices when a site‐heterogeneous model is used. In general, we find that stringent trimming of supermatrices results in reduced deviation from model assumptions but also in reduction of phylogenetic information. We also find that site‐heterogeneous C60 models provide greater stability of phylogenetic relationships of Adephaga across analyses of different amino‐acid supermatrices than site‐homogeneous models. Thus, site‐heterogeneous C60 models can potentially reduce incongruence in phylogenomics. Lastly, we show that gene‐tree errors are prominent in the data, even after sub‐sampling genes to reduce these errors, but we also show that subsampling genes based on the likelihood mapping criterion in summary coalescent analyses results in higher topological congruence with the concatenation‐based tree. Overall, our analyses demonstrate that moderate alignment trimming strategies, application of site‐heterogeneous models and mitigation of gene‐tree errors should be routinely included in the phylogenomic pipeline in order to more accurately infer the phylogeny of species.

Systematic bias and the phylogeny of Coleoptera—A response to Cai et al. (2022) following the responses to Cai et al. (2020)

“…In this case, the CAT model would be contraindicated and the need to demonstrate heterogeneity becomes explicitly more important, whereas the authors' claim is further undermined as CEA22 did not compare heterogeneity tests before and after trimming. We further note that CEA22 cited CEA20 in their introduction as evidence for systematic bias in beetle phylogenomics (p. 3 therein), despite the fact that they did not directly test heterogeneity in their earlier study, as already discussed by Vasilikopoulos et al (2021).…”

“…4 This is not true. CEA22 conveniently ignored both the methodological critique of this study by Vasilikopoulos et al (2021) and the morphological critique by Gustafson et al (2021). The latter is significant in this context because those authors directly re-examined the anatomical evidence for the claims of CEA20 and found them to be both falsified by the evidence and based on misinterpretation of the literature.…”

“…Open Sci . on the phylogeny, evolution and classification of the Coleoptera by Cai et al (2022) (hereafter CEA22, to differentiate this study from Cai et al, 2020, which we label as CEA20, as this prior study was referred to as ‘CEA’ in the critiques of Vasilikopoulos et al, 2020, 2021 and Gustafson et al, 2021).…”

“…In contrast,Zhang et al (2018)-whose data the authors added a single taxon to from another study(Kusy et al, 2018)-performed coalescent analysis via ASTRAL for 95 amino acid alignments, and recovered the Polyphaga-as-sister hypothesis, with the collapse of numerous nodes, including those of the Adephaga and the possible Archostemata-Myxophaga clade. Coalescence was also overlooked in CEA20, as pointed out byVasilikopoulos et al (2021).…”

Phylogeny of the flea beetles (Galerucinae: Alticini) and the position of Aulacothorax elucidated through anchored phylogenomics (Coleoptera: Chrysomelidae: Alticini)

“…A number of studies have sought to improve phylogenomic analyses by filtering loci based on a variety of criteria beyond amount of missing data (e.g. Bossert et al, 2017; Chen et al, 2015; Evangelista et al, 2021; Vasilikopoulos et al, 2021), with criteria of low mean pairwise sequence distance among loci, and a high number of resolved quartets being particularly promising and practicable. Using the latter criterion, Vasilikopoulos et al (2021) found improved congruence of their coalescent topology with the preferred concatenated result after filtering.…”