Chelicerata

Arthropoda is the largest and most morphologically diverse phylum in the history of life on Earth, comprising more than 1.25 million described living species (~80% of all known animal species) across marine, freshwater, terrestrial, and aerial ecosystems. For more than a century, comparative anatomists debated how the four extant arthropod subphyla—Chelicerata (horseshoe crabs, scorpions, spiders, mites, and sea spiders), Myriapoda (centipedes, millipedes, pauropods, and symphylans), Crustacea (crabs, lobsters, shrimp, barnacles, copepods, remipedes, and branchiopods), and Hexapoda (insects, springtails, proturans, and diplurans)—are related to one another and to extinct Paleozoic Trilobita.

Over the past two decades, large-scale phylogenomic supermatrices (Regier et al., 2010; Rota-Stabelli et al., 2011; Misof et al., 2014; Schwentner et al., 2017; Lozano-Fernandez et al., 2019) combined with site-heterogeneous CAT-GTR models and developmental neuroanatomy have overturned the classical textbook clade "Atelocerata" (Tracheata: Myriapoda + Hexapoda) and established the modern consensus phylogeny of crown-group Euarthropoda:

1. A basal split between Chelicerata and Mandibulata (Myriapoda + Pancrustacea);
2. Within Mandibulata, Myriapoda is the sister group to Pancrustacea (Tetraconata);
3. "Crustacea" is paraphyletic: Hexapoda (insects) evolved directly inside Crustacea as a terrestrialized branch of Allotriocarida (closest to blind anchialine cave crustaceans of the class Remipedia and branchiopods).

1. Mandibulata vs. "Paradoxopoda" (Myriochelata): A Classic Long-Branch Attraction Case

In the early 2000s, several mitochondrial and ribosomal RNA phylogenies unexpectedly grouped Myriapoda with Chelicerata into a hypothetical clade called "Myriochelata" or "Paradoxopoda", contradicting the morphological clade Mandibulata (which unites myriapods, crustaceans, and insects by homologous deutocerebral antennae and gnathobasic mandibles). In 2011, Omar Rota-Stabelli, Maximilian Telford, Davide Pisani, and colleagues demonstrated that "Paradoxopoda" is a textbook long-branch attraction (LBA) and compositional artifact: fast-evolving arachnids and myriapods were artificially pushed together by compositional convergence and outgroup attraction under site-homogeneous WAG/JTT substitution models. Applying site-heterogeneous CAT-GTR models, Dayhoff-6 amino-acid recoding, and rare microRNA genes restored 100% support for Mandibulata.

2. Pancrustacea (Tetraconata) vs. "Tracheata" (Atelocerata): Convergent Terrestrialization

Throughout the 20th century, zoologists grouped Myriapoda and Hexapoda into "Tracheata" (or "Atelocerata" / "Uniramia") because both groups breathe air through branched tracheal tubes, excrete nitrogenous waste via Malpighian tubules, possess uniramous (single-branched) walking legs, and lack second antennae on the tritocerebral (intercalary) head segment.

However, neuroanatomical studies by Wolfgang Dohle (2001) and Nicholas Strausfeld, together with every nuclear phylogenomic dataset since Friedrich & Tautz (1995), proved that Hexapoda and Crustacea form a monophyletic clade—Pancrustacea (named Tetraconata by Dohle after the shared architecture of their tetrapartite crystalline cone inside each ommatidium of the compound eye, produced by four Semper cells, plus identical neuroblast stem-cell division patterns in the brain and ventral nerve cord). Consequently, Myriapoda and Hexapoda invaded land independently during the Ordovician–Silurian (~470–420 Ma), evolving tracheal respiratory tubes, Malpighian tubules, and loss of the second antennae convergently as adaptations to subaerial life!

While mandibulate arthropods (insects, crustaceans, and myriapods) retain a single canonical Hox gene cluster (without whole-genome duplications), comparative chromosome-level sequencing of chelicerates by Alistair P. McGregor, Prashant P. Sharma, Guojie Zhang, and colleagues (2017–2021) discovered that independent whole-genome duplications (WGDs) shaped Chelicerata:

1. The Arachnopulmonata Whole-Genome Duplication: The common ancestor of spiders (Araneae), scorpions (Scorpiones), whip spiders (Amblypygi), and whip scorpions (Uropygi)—collectively termed Arachnopulmonata (the book-lung-bearing arachnids)—underwent an ancient whole-genome duplication (~430–450 Ma). Spiders (Parasteatoda tepidariorum) and scorpions (Centruroides sculpturatus) retain two complete Hox clusters (Hox-A and Hox-B) whose duplicated paralogs diverged in spatial expression boundary and timing (subfunctionalization and neofunctionalization), driving the developmental specialization of spider spinnerets, book lungs, and cheliceral venom glands. Meanwhile, non-pulmonate arachnids (mites, ticks, harvestmen, pseudoscorpions) have only a single Hox cluster.
2. Three Rounds of Whole-Genome Duplication in Horseshoe Crabs (Xiphosura): Living horseshoe crabs (Limulus polyphemus, Tachypleus tridentatus, Carcinoscorpius rotundicauda)—often called morphological "living fossils"—actually underwent three independent rounds of whole-genome duplication (3R-WGD), retaining up to four to eight copies of Hox clusters and systemic immune genes (such as coagulogen in their copper-hemocyanin blue amoebocyte blood).

How did insect wings evolve from ancestral crustacean appendages?

For over a century, two rival hypotheses debated the origin of insect wings (Pterygota): the paranotal (tergal) hypothesis (wings budded de novo as rigid lateral extensions of the dorsal thoracic tergum) and the exite (gill) hypothesis (wings evolved from the movable dorsal gill branches—epipodites/exites—of ancestral biramous crustacean legs). Developmental genetics and CRISPR-Cas9 knockouts in the crustacean Parhyale hawaiensis and insects (Tribolium, Blattella) by Nipam H. Patel, Heather S. Bruce, Yoshinori Tomoyasu, and colleagues (2020) resolved the debate through the dual-origin (fusion) model: as the proximal leg segments (pre-coxa and subcoxa) of the ancestral crustacean fused into the lateral thoracic body wall (pleuron) of insects, the dorsal crustacean exite/epipodite (expressing pdm/nubbin, apterous, and vestigial) merged with the lateral tergal margin to form the articulated, muscled insect wing.

Why are blind cave-dwelling Remipedia the closest living crustacean relatives of insects?

Discovered in 1979 in submerged marine caves (anchialine cenotes) in the Bahamas and Yucatan Peninsula, Remipedia (Speleonectes, Xibalbanus tulumensis) are blind, elongate crustaceans with a homonomous series of up to 42 biramous swimming segments and venomous maxillules. Despite their worm-like body plan, phylogenomic matrices and neuroanatomy show that Remipedia and Hexapoda share a derived brain architecture (fan-shaped body, mushroom body circuitry, and olfactory glomeruli), specialized hemocyanin subunits, and dozens of orthologous single-copy nuclear genes—making Remipedia (or Remipedia + Cephalocarida, the Xenocarida) the living sister clade to Hexapoda within Allotriocarida (Labiocarida).

Are scorpions and spiders more closely related to horseshoe crabs than to ticks and mites?

Traditionally, horseshoe crabs (Xiphosura) were placed as the marine sister group to all terrestrial Arachnida. However, recent phylogenomic analyses by Jesús Ballesteros and Prashant Sharma (2019–2022) accounting for the ultra-fast substitution rates of miniature acariform mites and pseudoscorpions raised the provocative possibility that horseshoe crabs may nest inside Arachnida (or that marine-to-terrestrial transitions occurred more than once in Chelicerata), while unequivocally confirming the monophyly of Arachnopulmonata (spiders + scorpions + pedipalpi) via their shared whole-genome duplication and 2×2=4 pair of book lungs.

1. Regier, J. C., Shultz, J. W., Zwick, A., Hussey, A., Ball, B., Wetzer, R., ... & Cunningham, C. W. (2010). Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature, 463(7284), 1079–1083. doi:10.1038/nature08742
2. Rota-Stabelli, O., Campbell, L., Brinkmann, H., Edgecombe, G. D., Longhorn, S. J., Cook, C. E., ... & Telford, M. J. (2011). A congruent solution to arthropod phylogeny: phylogenetics, microRNAs and morphology support monophyletic Mandibulata. Proceedings of the Royal Society B: Biological Sciences, 278(1703), 298–306. doi:10.1098/rspb.2010.0590
3. Misof, B., Liu, S., Meusemann, K., Peters, R. S., Donath, A., Mayer, C., ... & Zhou, X. (2014). Phylogenomics resolves the timing and pattern of insect evolution. Science, 346(6210), 763–767. doi:10.1126/science.1257570
4. Schwentner, M., Combosch, D. J., Nelson, J. P., & Giribet, G. (2017). A phylogenomic solution to the origin of insects by resolving crustacean-hexapod relationships. Current Biology, 27(12), 1818–1824. doi:10.1016/j.cub.2017.05.040
5. Schwager, E. E., Sharma, P. P., Clarke, T., Leite, D. J., Wierschin, T., Pechmann, M., ... & McGregor, A. P. (2017). The house spider genome reveals an ancient whole-genome duplication during arachnid evolution. BMC Biology, 15(1), 62. doi:10.1186/s12915-017-0399-x