The velvet worm brain unveils homologies and evolutionary novelties across panarthropods

Abstract

Background The evolution of the brain and its major neuropils in Panarthropoda (comprising Arthropoda, Tardigrada and Onychophora) remains enigmatic. As one of the closest relatives of arthropods, onychophorans are regarded as indispensable for a broad understanding of the evolution of panarthropod organ systems, including the brain, whose anatomical and functional organisation is often used to gain insights into evolutionary relations. However, while numerous recent studies have clarified the organisation of many arthropod nervous systems, a detailed investigation of the onychophoran brain with current state-of-the-art approaches is lacking, and further inconsistencies in nomenclature and interpretation hamper its understanding. To clarify the origins and homology of cerebral structures across panarthropods, we analysed the brain architecture in the onychophoran Euperipatoides rowelli by combining X-ray micro-computed tomography, histology, immunohistochemistry, confocal microscopy, and three-dimensional reconstruction. Results Here, we use this detailed information to generate a consistent glossary for neuroanatomical studies of Onychophora. In addition, we report novel cerebral structures, provide novel details on previously known brain areas, and characterise further structures and neuropils in order to improve the reproducibility of neuroanatomical observations. Our findings support homology of mushroom bodies and central bodies in onychophorans and arthropods. Their antennal nerve cords and olfactory lobes most likely evolved independently. In contrast to previous reports, we found no evidence for second-order visual neuropils, or a frontal ganglion in the velvet worm brain. Conclusion We imaged the velvet worm nervous system at an unprecedented level of detail and compiled a comprehensive glossary of known and previously uncharacterised neuroanatomical structures to provide an in-depth characterisation of the onychophoran brain architecture. We expect that our data will improve the reproducibility and comparability of future neuroanatomical studies.

A multiscale approach reveals elaborate circulatory system and intermittent heartbeat in velvet worms (Onychophora)

“…Thus, an anterior aorta might have been present in the last common ancestor of Onychophora and Arthropoda, but its shape and relative position to the brain might have changed in either lineage. This is not surprising, given the extensive and most likely independent reorganizations of the head during cephalization processes in different panarthropod lineages 69 , 84 – 88 .…”

“…While the anterior aortas of onychophorans and arthropods are likely homologous 8 , 41 , the afferent dorsal vessel and the efferent ventral channel associated with the protocerebral antenna of onychophorans is unlikely to be homologous with the circulatory system of the deutocerebral antenna of mandibulates, as these specialized cephalic appendages belong to different head segments 69 , 84 , 87 , 89 , 90 . Whether or not the antennal artery, the ventral antennal channel and the antennal ring channels associated with the onychophoran antennae were also present in the last common ancestor of Onychophora and Arthropoda is unclear, as the organization of the circulatory system in the anterior appendages of Cambrian outgroup taxa, such as † Aysheaia pedunculata 91 , † Onychodictyon ferox 69 and † Antennacanthopodia gracilis 45 , is unknown.…”

“…The original terminology of the OArCS database was amended and adapted for studies of Onychophora (Table 1 and Supplementary Table 1 ). The terminology and abbreviations for neural structures follow the nomenclature of Martin et al 84 .…”

Developmental and genomic insight into the origin of the tardigrade body plan

“…The model of segment homology discussed above supports a one‐to‐one alignment of the anteriormost segments across Panarthropoda, with the tardigrade head aligning to the protocerebral segment of arthropods and the frontal appendage segment of onychophorans (Figure 3a, hypothesis 1) (Smith & Goldstein, 2017; Smith et al, 2018). Anatomical studies of extant and extinct panarthropods support the one‐to‐one model of segment alignment (Martin et al, 2022; Mayer, Kauschke, et al, 2013; Ortega‐Hernández et al, 2017; Park et al, 2018). However, recently two new models of panarthropod segment homology suggest that the tardigrade head is homologous to more than a single segment of arthropods or onychophorans.…”

Serial Homology and Segment Identity in the Arthropod Head

“…It is worth reiterating that the anteriormost unit, the protocerebral segment, is in itself made up of two distinct units, so the arthropod brain might also be described as “quadripartite.” However, we prefer to maintain the conventional terminology of a tri-partite brain and anterior head, following the expression of three stripes of hedgehog and other segmental genes. Also worth noting is that the two-segment brain of Onychophora represents a convergent expansion of the ancestrally protocerebral brain under any scenario ( Martin et al. 2022 ).…”