Ordered phylogenomic subsampling enables diagnosis of systematic errors in the placement of the enigmatic arachnid order Palpigradi

Abstract

The miniaturized arachnid order Palpigradi has ambiguous phylogenetic affinities owing to its odd combination of plesiomorphic and derived morphological traits. This lineage has never been sampled in phylogenomic datasets because of the small body size and fragility of most species, a sampling gap of immediate concern to recent disputes over arachnid monophyly. To redress this gap, we sampled a population of the cave-inhabiting species Eukoenenia spelaea from Slovakia and inferred its placement in the phylogeny of Chelicerata using dense phylogenomic matrices of up to 1450 loci, drawn from high-quality transcriptomic libraries and complete genomes. The complete matrix included exemplars of all extant orders of Chelicerata. Analyses of the complete matrix recovered palpigrades as the sister group of the long-branch order Parasitiformes (ticks) with high support. However, sequential deletion of long-branch taxa revealed that the position of palpigrades is prone to topological instability. Phylogenomic subsampling approaches that maximized taxon or dataset completeness recovered palpigrades as the sister group of camel spiders (Solifugae), with modest support. While this relationship is congruent with the location and architecture of the coxal glands, a long-forgotten character system that opens in the pedipalpal segments only in palpigrades and solifuges, we show that nodal support values in concatenated supermatrices can mask high levels of underlying topological conflict in the placement of the enigmatic Palpigradi.

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

“…DNA was extracted using the Qiagen DNeasy Blood and Tissue Kit (Valencia, CA) from one to five specimens, prioritizing tissue from the propodus and main claw (gut-free leg podomeres) where possible. Taxonomic sampling consisted of 89 sea spiders; outgroups consisted of 14 Arachnida (including one Xiphosura, which has recently been shown to be possibly nested within the arachnids; Ballesteros and Sharma 2019 ; Ballesteros et al. 2019 ), 3 Myriapoda, 3 Pancrustacea, and 1 Onychophora.…”

Phylogenomic resolution of sea spider diversification through integration of multiple data classes

“…A list of taxa sampled from field expeditions, museum collections, and multiple deep sea cruises is provided as electronic supplementary material, table S1. Taxonomic sampling consisted of 89 sea spiders; outgroups consisted of 14 Arachnida (including one Xiphosura, which has recently been shown to be nested within the arachnids [21,22]), three Myriapoda, three Pancrustacea, and one Onychophora.…”

“…Previous efforts to decipher the higher-level relationships of sea spiders have been hindered by the omission of key lineages [11,12], inaccessibility of many families for phylotranscriptomic approaches [18,21,22], limited informativeness of legacy Sangersequenced markers [5,[11][12], compositional bias of mitochondrial genes [11], ineffectiveness of mitogenomes for resolving deep relationships of Chelicerata [13,14], and the potential for gut or epibiont contamination [5]. Here, we surmounted these challenges by integrating multiple data classes and using a target capture approach optimized for sea spider (or chelicerate) genomic sequence.…”

Systemic paralogy and function of retinal determination network homologs in arachnids

“…The second concern in extrapolating developmental processes derived from pancrustaceans is that a subset of Arachnida exhibits an ancient shared genome duplication, resulting in numerous paralogs of developmental patterning genes. Recent phylogenetic and comparative genomic works on Arachnida have shown that Arachnopulmonata [ 36 – 38 ], the clade of arachnids that bear book lungs (e.g., spiders, scorpions, whip spiders), retain duplicates of many key transcription factors, such as homeobox genes, often in conserved syntenic blocks [ 39 – 42 ]. Many of the ensuing paralogs exhibit non-overlapping expression patterns and a small number have been shown to have subdivided the ancestral gene function (subfunctionalization) or acquired new functions (neofunctionalization) [ 42 – 44 ].…”