The chelifores of sea spiders (Arthropoda, Pycnogonida) are the appendages of the deutocerebral segment

Abstract

Within the last decade, gene expression patterns and neuro-anatomical data have led to a new consensus concerning the long-debated association between anterior limbs and neuromeres in the arthropod head. According to this new view, the first appendage in all extant euarthropods is innervated by the second neuromere, the deutocerebrum, whereas the anterior-most head region bearing the protocerebrum lacks an appendage. This stands in contrast to the clearly protocerebrally targeted "antennae" of Onychophora and to some evidence for protocerebral limbs in fossil euarthropod representatives. Yet, the latter "frontal appendages" or "primary antennae" have most likely been reduced or lost in the lineage, leading to extant taxa. Surprisingly, a recent neuro-anatomical study on a pycnogonid challenged this evolutionary scenario, reporting a protocerebral innervation of the first appendages, the chelifores. However, this interpretation was soon after questioned by Hox gene expression data. To re-evaluate the unresolved controversy, we analyzed neuro-anatomy and neurogenesis in four pycnogonid species using immunohistochemical techniques. We clearly show the postprotocerebral innervation of the chelifores, which is resolved as the plesiomorphic condition in pycnogonids when evaluated against a recently published comprehensive phylogeny. By providing direct morphological support for the deutocerebral status of the cheliforal ganglia, we reconcile morphological and gene expression data and argue for a corresponding position between the anterior-most appendages in all extant euarthropods. Consequently, other structures have to be scrutinized to illuminate the fate of a presumptive protocerebral appendage in recent euarthropods. The labrum and the "frontal filaments" of some crustaceans are possible candidates for this approach.

Silurian horseshoe crab illuminates the evolution of arthropod limbs

“…The evidence of Hox gene expression (16) and the deutocerebral innervation of the chelifore in pycnogonids, which corresponds to the chelicera in euchelicerates (17), show that the chelicera is equivalent to the antennule (first antenna) in other arthropod groups even though the two are very different in morphology. The chelicera of Dibasterium is elongate and apparently flexible, and represents a morphology more antenniform than in other chelicerates.…”

A conserved genetic mechanism specifies deutocerebral appendage identity in insects and arachnids

“…Whereas the correspondence of arthropod head segments has a basis in neuroanatomical and developmental genetic evidence [6][7][8][9][10][11], the correspondence of antennae and chelicerae remains unsubstantiated.…”

“…A general consensus has formed that the first appendage-bearing segments of Mandibulata and Chelicerata are homologous, based both on the innervation of these appendages by the deutocerebral ganglia (the second part of the tripartite arthropod brain), and on the absence of Hox gene expression in the deutocerebral segment across arthropods [6,7,[9][10][11]. Implicit in this homology statement is the homology of the deutocerebral appendages, which are markedly different in both morphology and function between mandibulates and chelicerates.…”

Posição filogenética dos ácaros Actinotrichida (Chelicerata) e espermatologia comparada dos Halacaridae (Actionotrichida)

“…Dunlop (1996) apresentou uma série de possíveis apomorfias ligando os Ricinulei à ordem fóssil Trigonotarbida, a que se adicionou as descobertas recentes a respeito da morfologia do palpo (Dunlop et al, 2009 (Damen et al, 1998;Telford & Thomas, 1998;Manuel et al, 2006, Brenneis et al, 2008 (Guttel et al 1994). Pareamentos entre adenina e citosina são extremamente raros, mas são similares geometricamente aos entre guanina e uracila, se protonados (Nagaswamy et al, 2000;Fox, 2005).…”

“…Dunlop (1996) (Damen et al, 1998; Telford & Thomas, 1998; Manuel et al., 2006, Brenneis et al, 2008 (Guttel et al 1994). Pareamentos entre adenina e citosina são extremamente raros, mas são similares geometricamente aos entre guanina e uracila, se protonados (Nagaswamy et al, 2000;Fox, 2005).…”