Box 7.1. Relationships of the Hexapoda to other Arthropoda

The immense phylum Arthropoda, the joint-legged animals, includes several major lineages: the myriapods (centipedes, millipedes, and their relatives), the chelicerates (horseshoe crabs and arachnids), the crus- taceans (crabs, shrimps, and relatives), and the hexapods (the six-legged arthropods — the Insecta and their relatives). The onychophorans (velvet worms, lobopods) have been included in the Arthropoda, but are considered now to lie outside, amongst probable sister groups. Traditionally, each major arthropod lineage has been considered monophyletic, but at least some investigations have revealed non-monophyly of one or more groups. Analyses of molecular data (some of which were naïve in sampling and analytical methods) suggested paraphyly, possibly of myriapods and/or crustaceans. Even accepting monophyly of arthropods, estimation of inter-relationships has been contentious with almost every possible relationship proposed by someone. A once-influential view of the late Sidnie Manton proposed three groups of arthropods, namely the Uniramia (lobopods, myriapods, and insects, united by having single-branched legs), Crustacea, and Chelicerata, each derived independently from a different (but unspecified) non-arthropod group. More recent morphological and molecular studies reject this hypothesis, asserting monophyly of arthropodization, although proposed internal relationships cover a range of possibilities. Part of Manton’s Uniramia group — the Atelocerata (also known as Tracheata) comprising myriapods plus hexapods — is supported by some morphology. These features include the presence (in at least some groups) of a tracheal system, Malpighian tubules, unbranched limbs, eversible coxal vesicles, postantennal organs, and anterior tentorial arms. Furthermore, there is no second antenna (or homolog) as seen in crustaceans. Proponents of this myriapod plus hexapod relationship saw Crustacea either grouping with the chelicerates and the extinct trilobites, distinct from the Atelocerata, or forming its sister group in a clade termed the Mandibulata. In all these schemes, the closest relatives of the Hexapoda always were the Myriapoda or a subordinate group within Myriapoda.

In contrast, certain shared morphological features, including ultrastructure of the nervous system (e.g. brain structure, neuroblast formation, and axon development), the visual system (e.g. fine structure of the ommatidia, optic nerves), and developmental processes, especially segmentation, argued for a closer relationship of Hexapoda to Crustacea. Such a grouping, termed the Pancrustacea, excludes myriapods. Molecular sequence data alone, or combined with morphology, tend to support Pancrustacea over Atelocerata. However, not all analyses actually recover Pancrustacea and certain genes evidently fail to retain phylogenetic signal from what was clearly a very ancient divergence.

If the Pancrustacea hypothesis of relationship is correct, then features understood previously to support the monophyly of Atelocerata need re-consideration. Postantennal organs occur only in Collembola and Protura in Hexapoda, and may be convergent with similar organs in Myriapoda or homologous with the second antenna of Crustacea. The shared absence of features such as the second antenna provides poor evidence of relationship. Malpighian tubules of hexapods must exist convergently in arachnids and evidence for homology between their structure and development in hexapods and myriapods remains inadequately studied. Coxal vesicles are not always developed and may not be homologous in the Myriapoda and those Hexapoda (apterygotes) possessing these structures. Thus, morphological characters supporting Atelocerata may be non-homologous and may have been convergently acquired in association with the adoption of a terrestrial mode of life.

A major finding from molecular embryology is that the developmental expression of the homeotic (developmental regulatory) gene Dll (Distal-less) in the mandible of studied insects resembled that observed in sampled crustaceans. This finding refutes Manton’s argument for arthropod polyphyly and the claim that hexapod mandibles were derived independently from those of crustaceans. Data derived from the neural, visual, and developmental systems, although sampled across few taxa, may reflect more accurately the phylogeny than did many earlier-studied morphological features. Whether the Crustacea in totality or a component thereof constitute the sister group to the Hexapoda is still debatable. Morphology generally supports a monophyletic Crustacea, but inferences from some molecular data imply paraphyly, including a suggestion that Malacostraca alone form the sister taxon to Hexapoda. Given that analysis of combined morphological and molecular data supports monophyly of Crustacea and Pancrustacea, a single origin of Crustacea seems most favored. Nonetheless, some data imply a quite radically different relationship of Collembola to Crustacea, implying a polyphyletic Hexapoda. In this view, aberrant collembolan morphology (entognathy, unusual abdominal segmentation, lack of Malpighian tubules, single claw, unique furcula, unique embryology) derives from an early-branching pancrustacean ancestry, with terrestriality acquired independently of Hexapoda. Such a view deserves further study — evidently there remain many questions in the unraveling of the evolution of the Hexapoda and Insecta.

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