Arthropod Phylotranscriptomics With a Special Focus on the Basal Phylogeny of the Myriapoda

Abstract

Arthropoda represents the most diverse animal phylum, but clarifying the phylogenetic relationships among arthropod taxa remains challenging given the numerous arthropod lineages that diverged over a short period of time. In order to resolve the most controversial aspects of deep arthropod phylogeny, focusing on the Myriapoda, we conducted phylogenetic analyses based on ten super-matrices comprised of 751 to 1,233 orthologous genes across 64 representative arthropod species, including 28 transcriptomes that were newly generated in this study. Our findings provide unambiguous support for the monophyly of the higher arthropod taxa, Chelicerata, Mandibulata, Myriapoda, Pancrustacea, and Hexapoda, while the Crustacea are paraphyletic, with the class Remipedia supported as the lineage most closely related to hexapods. Within the Hexapoda, our results largely affirm previously proposed phylogenetic relationships among deep hexapod lineages, except that the Paraneoptera (Hemiptera, Thysanoptera, and Psocodea) was recovered as a monophyletic lineage in some analyses. The results corroborated the recently proposed phylogenetic framework of the four myriapod classes, wherein Symphyla and Pauropoda, as well as Chilopoda and Diplopoda, are each proposed to be sister taxa. The findings provide important insights into understanding the phylogeny and evolution of arthropods.

Keywords: arthropods; evolution; myriapods; phylogenetics; transcriptome.

Fig. 1.

Major hypotheses for phylogenetic relationships among the four myriapod classes proposed to date. a, b) Traditional views based on morphology (Pocock 1893a, 1893b; Tiegs 1947; Fernández et al. 2018) and supported by some molecular analyses (Fernández et al. 2018). c, d) Hypotheses based primarily on molecular analyses (Regier et al. 2010; Dong et al. 2012a, 2012b; Zwick et al. 2012; Miyazawa et al. 2014; Rehm et al. 2014; Noah et al. 2020). e) Hypothesis based on Szucsich et al. (2020), Wang et al. (2021), Benavides et al. (2023), and this study.

Fig. 2.

Workflow showing data matrix compilation and the tree reconstruction.

Fig. 3.

RAxML tree derived from Dataset A1, which contains all arthropod species analyzed in this study. BS values and PP for tree topologies inferred from Dataset A1 and four other datasets (Datasets A2 to A5) are displayed at the tree nodes. These datasets were compiled using the core orthologous gene set, insecta_hmmer3_2 (Ebersberger et al. 2009) (Coreset a) and different sample sets (refer to supplementary tables S2 to S6, Supplementary Material online). For the trees inferred based on these datasets (see supplementary figs. S1 to S5, Supplementary Material online).

Fig. 4.

RAxML tree based on Dataset B1 containing all of the arthropod species used in this study. BS and PP for the tree topologies, derived from Dataset B1 and four other datasets (Datasets B2 to B5), are merged and displayed at the tree nodes. These datasets are compiled based on the core orthologous gene set, arthropoda_hmmer3 (Ebersberger et al. 2009) (Coreset B), incorporating various sample sets (see supplementary tables S7 to S11, Supplementary Material online). For the trees resulting from these datasets (see supplementary figs. S6 to S11, Supplementary Material online).

Fig. 5.

Arthropod phylogeny strongly supported across all phylogenetic analyses conducted in this study.