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. This group of arthropods appeared early in the fossil record, with the oldest unambiguous fossils dating to the Silurian. Due to the inaccessibility of some small-bodied lineages, few phylogenetic studies have sampled all sea spider families. In addition, previous efforts based on a handful of genes have yielded unstable tree topologies from one analytical approach to the next. 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 Page 3 of 31 robust-bodied family Pycnogonidae. This stable, dated phylogeny of Pycnogonida enables confident polarization of of cephalic appendage loss across pycnogonid families, with the consistent lack of the adult chelifore in a grade of basally diverging lineages. 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

“…This data set 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 ; Setton et al 2019 ; Ballesteros et al. 2020 ; Gainett and Sharma 2020 ; Gainett et al.…”

“…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 and Sharma 2018 ; Ballesteros et al. 2020 ), and the tarantula A. hentzi ( Setton et al.…”

“…2017 , 2018 ; Ballesteros et al. 2019 , 2020 ; Benavides et al 2019 ; Santibáñez-López et al. 2019 , 2020 ).…”

A postlarval instar of Phoxichilidium femoratum (Pycnogonida, Phoxichilidiidae) with an exceptional malformation

“…Pycnogonida (sea spiders) is an old lineage of marine chelicerates that diversified in the Paleozoic and survived with its unmistakable body organization for more than 400 million years until today (Ballesteros et al, 2020; Siveter et al, 2004). Compared to many other arthropods, the pycnogonid trunk is unusually small in relation to its appendages, most prominently among them the anteriorly directed proboscis and (mostly) four pairs of long legs (Arnaud & Bamber, 1987; King, 1973; Figure 1(a),(b)).…”

Analyzing drivers of speciation in the Southern Ocean using the sea spider species complex Colossendeis megalonyx as a test case

“…One taxon consisting of a remarkable amount of recently diverged lineages are pycnogonids (Mahon et al 2008; Krabbe et al 2010;Arango et al 2011;Weis and Melzer 2012;Weis et al 2014;Dietz et al 2015Dietz et al , 2019Dömel et al 2015Dömel et al , 2017Ballesteros et al 2020). Pycnogonids, also called sea spiders, are a group of exclusively marine arthropods that are especially diverse in the Southern Ocean (Aronson et al 2007), showing high endemism to this region (Munilla and Soler-Membrives 2009).…”