A congruent solution to arthropod phylogeny: phylogenomics, microRNAs and morphology support monophyletic Mandibulata

Abstract

While a unique origin of the euarthropods is well established, relationships between the four euarthropod classes-chelicerates, myriapods, crustaceans and hexapods-are less clear. Unsolved questions include the position of myriapods, the monophyletic origin of chelicerates, and the validity of the close relationship of euarthropods to tardigrades and onychophorans. Morphology predicts that myriapods, insects and crustaceans form a monophyletic group, the Mandibulata, which has been contradicted by many molecular studies that support an alternative Myriochelata hypothesis (Myriapoda plus Chelicerata). Because of the conflicting insights from published molecular datasets, evidence from nuclear-coding genes needs corroboration from independent data to define the relationships among major nodes in the euarthropod tree. Here, we address this issue by analysing two independent molecular datasets: a phylogenomic dataset of 198 protein-coding genes including new sequences for myriapods, and novel microRNA complements sampled from all major arthropod lineages. Our phylogenomic analyses strongly support Mandibulata, and show that Myriochelata is a tree-reconstruction artefact caused by saturation and long-branch attraction. The analysis of the microRNA dataset corroborates the Mandibulata, showing that the microRNAs miR-965 and miR-282 are present and expressed in all mandibulate species sampled, but not in the chelicerates. Mandibulata is further supported by the phylogenetic analysis of a comprehensive morphological dataset covering living and fossil arthropods, and including recently proposed, putative apomorphies of Myriochelata. Our phylogenomic analyses also provide strong support for the inclusion of pycnogonids in a monophyletic Chelicerata, a paraphyletic Cycloneuralia, and a common origin of Arthropoda (tardigrades, onychophorans and arthropods), suggesting that previous phylogenies grouping tardigrades and nematodes may also have been subject to tree-reconstruction artefacts.

Arthropod fossil data increase congruence of morphological and molecular phylogenies

“…The latter is supported by a number of independent lines of evidence, including nuclear ribosomal genes 8,15 , mitochondrial genomes and gene order, nuclear protein-coding genes 1 and transcriptomics [2][3][4] , but has so far remained elusive in morphological phylogenies, apart from those based solely on neural characters 16 , which resolve malacostracan crustaceans closer to hexapods than to branchiopods. The position of the pycnogonids is equally controversial, being variously resolved as the closest relatives of euchelicerates 1,3,15 (Fig. 1a,b) or as sister taxon to all other euarthropods 17 ( Fig.…”

“…1c), monophyletic Crustacea DS-VI All taxa Non-morphological characters Chelicerata (Fig. 1b) Onychophora [2] Pycnogonida [3] Xiphosura [2] Arachnida [19] Myriapoda [13] Hexapoda [13] Malacostraca [20] Branchiopoda [9] Ichthyostraca [2] Thecostraca [2] Ostracoda with remipedes rather than with myriapods. We therefore conclude that crustacean monophyly is influenced by the convergent acquisition of terrestrial adaptations in myriapods and hexapods, with the result that crustaceans attract to each other when hexapods group with myriapods.…”

“…1a), considered so surprising it was named Paradoxopoda 8 (alternatively Myriochelata 9 ). Although a few neuroanatomical and developmental characters were later proposed as putative novelties of Paradoxopoda 10,11 , subsequent exploration of molecular data sets suggested that this grouping is a long-branch artefact 3,12 .…”

“…1): pycnogonids (sea spiders), euchelicerates (horseshoe crabs and arachnids), myriapods (centipedes and millipedes), hexapods (insects and their flightless relatives) and crustaceans (crabs, lobsters, barnacles and so on). Each group is characterized by a distinct set of morphological features and their monophyly is little disputed, except for the crustaceans [1][2][3][4] . Molecular clock estimates calibrated by new fossil discoveries indicate that these groups originated and had begun to diversify by at least the midCambrian 5 .…”

A critical appraisal of the use of microRNA data in phylogenetics

“…Typically in these studies, the phylogeny is first estimated from some other source of data, and then the correspondence of the inferred tree to select miRNA families is discussed (e.g., refs. [23][24][25][26][27]]. …”