Major revisions in Pancrustacea phylogeny through improved taxon sampling with recommendations for resolving remaining difficult nodes

Authors: BERNOT, JAMES - Smithsonian Institute; Owen, Christopher; WOLFE, JOANNE - Harvard University; MELAND, KENNETH - University Of Bergen; OLESEN, JORGEN - University Of Copenhagen; CRANDALL, KEITH - George Washington University

Submitted to: Molecular Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/27/2023
Publication Date: 8/8/2023
Citation: Bernot, J., Owen, C.L., Wolfe, J., Meland, K., Olesen, J., Crandall, K. 2023. Major revisions in Pancrustacea phylogeny through improved taxon sampling with recommendations for resolving remaining difficult nodes. Molecular Biology and Evolution. 40(8):msad175. https://doi.org/10.1093/molbev/msad175.
DOI: https://doi.org/10.1093/molbev/msad175

Interpretive Summary: Pancrustacea is a clade of arthropods that includes some of the most agriculturally important animals such as aphids, bees, beetles, and copepods. Despite the agricultural importance of pancrustaceans, the evolutionary relationships between lineages within this group have been shown to be incongruent based on the species sampling and the data types. This paper synthesizes nearly all publicly available genome data for deep pancrustacean lineages, generates novel genomic data, and estimates their evolutionary relationships. We demonstrate with a novel dataset of 576 genes that the evolutionary history of pancrustaceans supports non-traditional relationships. Moreover, we show that our results support non-traditional relationships due to strategic taxon sampling during the study design. These results are important because taxon sampling is often overlooked when estimating evolutionary relationships and inaccurate evolutionary relationships can cause problems estimating precise pathway analyses that seek to identify the geographic route a non-native species entered the country.

Technical Abstract: The clade Pancrustacea, comprising crustaceans and hexapods, is the most diverse group of animals on earth, comprising more than 80% of animal species, and has dominated much of the planet for over 500 million years. It has been the subject of a number of recent phylogenomic analyses, but despite multiple analyses of hundreds of genes, relationships within Pancrustacea show a notable lack of stability. In this study, the pancrustacean phylogeny is estimated with expanded taxon sampling, particularly of malacostracans, using 106 transcriptomes and genomes and a precise tree-based approach to orthology inference. We completed more than 50 independent tree searches on continually expanded taxon sets using ML, BI, and coalescent methods, and our results show that outgroup selection and changes in taxon sampling have a large impact on the topologies recovered. We show that small differences in taxon sampling have a large impact on ortholog identification and phylogenetic estimation. By analyzing only shared orthologs between two slightly different taxon sets, we show that the differences in the resulting species trees are due to the effects of taxon sampling on the phylogenetic estimation, not on ortholog identification. In our final taxon set, we identify 576 protein-coding orthologs comprising 121,508 amino acid positions. We compare trees resulting from our analyses with others from the literature to explore the large tree space of pancrustacean phylogenetic estimates and find that statistical topology tests of our dataset reject the previously published trees in favor of the ML trees produced here. Our results reject a number of clades including Caridoida, Eucarida, Multicrustacea, Vericrustacea, and Syncarida but support other classically recognized taxa, such as the Peracarida, and suggest some new clades. In contrast to the traditional Eucarida, we recover a novel relationship between decapods, euphausiids, and two clades of syncarids that we refer to as the Syneucarida. Additionally, with denser taxon sampling, we find Stomatopoda as sister to this clade. In recognition of these new relationships, we propose the name Stomatocaridea for Stomatopoda, Eucarida, and the two separate clades of “Syncarida”, which divides Malacostraca into three clades: Leptostraca, Peracarida, and Stomatocaridea. A new Bayesian divergence time estimation is conducted using 13 vetted fossils. We review our results in the context of other pancrustacean analyses and highlight key taxa and strategies for future phylogenetic studies.