Phylogenomic Resolution of Sea Spider Diversification through Integration of Multiple Data Classes

Abstract

Despite significant advances in invertebrate phylogenomics over the past decade, the higher-level phylogeny of Pycnogonida (sea spiders) remains elusive. Due to the inaccessibility of some small-bodied lineages, few phylogenetic studies have sampled all sea spider families. Previous efforts based on a handful of genes have yielded unstable tree topologies. Here, we inferred the relationships of 89 sea spider species using targeted capture of the mitochondrial genome, 56 conserved exons, 101 ultraconserved elements, and three nuclear ribosomal genes. We inferred molecular divergence times by integrating morphological data for fossil species to calibrate 15 nodes in the arthropod tree of life. This integration of data classes resolved the basal topology of sea spiders with high support. The enigmatic family Austrodecidae was resolved as the sister group to the remaining Pycnogonida and the small-bodied family Rhynchothoracidae as the sister group of the robust-bodied family Pycnogonidae. Molecular divergence time estimation recovered a basal divergence of crown group sea spiders in the Ordovician. Comparison of diversification dynamics with other marine invertebrate taxa that originated in the Paleozoic suggests that sea spiders and some crustacean groups exhibit resilience to mass extinction episodes, relative to mollusk and echinoderm lineages.

Taxonomic sampling and rare genomic changes overcome long-branch attraction in the phylogenetic placement of pseudoscorpions

“…We therefore assembled a dataset of 26 Panarthropoda, sampling genomes or developmental transcriptomes of all three major lineages of Arachnopulmonata sensu Sharma et al (2014a) (i.e., spiders, scorpions, and Pedipalpi [Amblypygi + Thelyphonida + Schizomida]), as well as mites, ticks, harvestmen, horseshoe crabs, and sea spiders. This dataset leveraged recent developmental genetic resources generated by us for several non-model chelicerate groups, such as mygalomorph spiders, whip spiders, harvestmen, and sea spiders (Sharma et al 2012; Gainett and Sharma 2020; Gainett et al 2020; Ballesteros et al 2020). We included in our analysis two adult transcriptomes of pseudoscorpions previously analyzed by Leite et al (2018), which had been shown to harbor few homeobox genes and exhibited short contigs for many homeobox homologs.…”

“…We therefore investigated whether duplicates of these four genes also occurred in the developmental transcriptome of C. crassus . To the surveys previously generated by Nolan et al (2020), we searched for and added homologs of these genes from developmental transcriptomes of the pseudoscorpion, the whip spider species Phrynus marginemaculatus (Gainett and Sharma 2020), five sea spider species (Setton et al 2018; Ballesteros et al 2020) and the tarantula A. hentzi (Setton et al 2019). We discovered two copies of all four genes in the developmental transcriptome of the pseudoscorpion, except for dachshund , wherein three putative homologs were discovered.…”

“…For phylogenetic reconstruction, we generated a dataset of 117 chelicerates (40 pseudoscorpions, 12 scorpions, 17 spiders, 4 Pedipalpi, 13 Opiliones, 5 Ricinulei, 3 Xiphosura, 2 Solifugae, 9 Parasitiformes, 10 Acariformes, 2 Pycnogonida) and 15 outgroups (3 Onychophora, 4 Myriapoda, 8 Pancrustacea), with most of these taxa sequenced previously by us. Taxon selection prioritized the representation of basal splits in all major groups (Sharma et al 2015c; Fernández et al 2017, 2018; Ballesteros et al 2019, 2020; Santibáñez-López et al 2019, 2020; Benavides et al 2019). Libraries of high quality were additionally selected such that all chelicerate orders were represented in >95% of loci in all matrices constructed.…”

The genome of a daddy-long-legs (Opiliones) illuminates the evolution of arachnid appendages and chelicerate genome architecture

“…Together with the genome architecture of model systems like Ixodes scapularis and Tetranychus urticae, the harvestman genome supports the notion that an unduplicated genome is the ancestral condition for arachnids. This reconstruction is further supported by the advent of recent genomic resources for Pycnogonida (Ballesteros et al, 2020) (sea spiders), the sister group to the remaining Chelicerata.…”

The First Pycnogonid Draft Genome of Nymphon striatum

“…These recent phylogenomic studies provided newly sequenced chelicerate genomes or transcriptomes, in addition to invaluable insights on the evolution of Euchelicerata (Sharma et al, 2014;Ballesteros and Sharma, 2019;Lozano-Fernandez et al, 2019). However, studies using such an approach on the Pycnogonida are currently very limited and fail to incorporate a de novo assembled pycnogonid genome (Dietz et al, 2019;Ballesteros et al, 2020). This lack of pycnogonid genome assembly is also a challenging obstacle for studies on the evolution of their distinctive morphology that requires high-quality genome assemblies with reliable annotations (Garb et al, 2018).…”