The head of arthropods is a specialised anterior body region, which is distinguished by fused segments and several pairs of modified appendages [1
]. These appendages serve for swimming, feeding, defence, or sensory perception, and their movements are coordinated by a complex brain situated within the head. Despite over a century of intense research in this area, the ancestral composition of the arthropod head remains obscure and is one of the most controversial topics in zoology [2
]. Fossils have contributed much to our knowledge [1
], but their limited preservation constrains definitive conclusions about the degree of cephalisation in the last common ancestor of Panarthropoda (Onychophora + Tardigrada + Arthropoda).
The extant Onychophora are a key group when considering this issue, since they are close relatives of arthropods and resemble Cambrian lobopodians [9
], while their internal anatomy and embryology are accessible for detailed examination. As in various lobopodians, the onychophoran "head" is not clearly delineated from the trunk, but shows three pairs of modified appendages: sensory antennae, jaws situated within the mouth cavity, and slime papillae, which are used for defence and capturing prey organisms (Figure ). These modified appendages have been assigned to each body segment by studying embryogenesis, which revealed that the antennae belong to the first (ocular) body segment, the jaws to the second, and the slime papillae to the third segment [14
]. Most importantly, these studies have provided no evidence of any additional vestigial cephalic segments [21
] in Onychophora. This is supported by the expression data of segment polarity genes in onychophoran embryos [25
], which show only three domains anterior to the leg-bearing segments, corresponding to the three cephalic segments (Figure ).
Figure 1 Head composition and homology of cephalic appendages in Onychophora and Arthropoda. (A) Ventral view of onychophoran "head" showing three pairs of modified appendages: antennae (at), jaws (jw), and slime papillae (sp). Scanning electron micrograph. Scale (more ...)
Based on various studies of embryology [14
], including the expression data of the anterior Hox genes labial
], the onychophoran "head" appendages can therefore be aligned with the corresponding appendages of arthropods (Figure ). According to this alignment, the onychophoran antennae are either serial homologues of the arthropod labrum or, alternatively, the corresponding pair of appendages may have been lost in arthropods - an issue that is still controversial [5
]. (It has also been argued that the arthropod labrum is a modified appendage of the third body segment [30
]. However, the Hox gene expression data referred to above, together with the common expression of the anterior marker six3
in the insect labrum and onychophoran antenna [26
], speak against this possibility.) Since the onychophoran antennae belong to the anterior-most body segment bearing the eyes [19
], they cannot be homologised with the chelicerae of chelicerates or the (first) antennae of crustaceans, insects, and myriapods, which belong to the second body segment [2
]. The chelicerae and the (first) antennae of arthropods are instead serially homologous to the onychophoran jaws (Figure ). The onychophoran slime papillae are, in turn, serially homologous to the pedipalps of chelicerates and to the second antennae of crustaceans whereas the corresponding pair of appendages was lost in hexapods and myriapods [review [2
This alignment of head segments is reflected in the organisation of the central nervous system. Three major brain regions are generally recognised in arthropods (Figure ): the protocerebrum (forebrain), the deutocerebrum (midbrain), and the tritocerebrum (hindbrain), corresponding to the three anterior-most body segments [2
]. Such an organisation has also been suggested for the Onychophora, based on studies of adult brain anatomy and its neuropilar structure [21
]. However, an alternative view [36
] suggests that the onychophoran brain or "cerebral ganglion" [38
] is bipartite and does not include the region homologous to the arthropod tritocerebrum.
Figure 2 Subdivision of arthropod brain and alternative possibilities for the position of neuronal cell bodies innervating the third pair of cephalic appendages in Onychophora. (A) Position of protocerebral (yellow), deutocerebral (red) and tritocerebral structures (more ...)
One feature that has previously been used to determine the segmental organisation of the brain in Onychophora is the position and number of transverse neuropils in the adult [31
]. Three major neuropils have been identified, leading to the conclusion that the onychophoran brain is tripartite. However, this rests on the assumption that each neuropil arises from a separate segment during development - an issue, which has not been clarified thus far. An additional feature that could be used to identify the degree of segmentation of the onychophoran brain is the position of neuronal cell bodies innervating the head appendages. If the cell bodies of neurons innervating the tritocerebrum were found to lie within the brain (Figure ), the hypothesis of tripartite organisation [31
] would be supported. In contrast, a position of these neuronal cell bodies found outside the brain (Figure ) would speak against the existence of the tritocerebrum in Onychophora.
To clarify the segmental composition of the onychophoran brain, we combined two approaches. First, we studied brain development to determine the embryonic origin of transverse neuropils. Second, we analysed the position of neuronal cell bodies innervating the cephalic appendages. Our results show that the major transverse neuropils of the onychophoran brain arise from only one (the anterior-most) body segment, and that only the antennae and jaws are innervated by the brain. These findings suggest that the onychophorans show a lower degree of cephalisation in relation to their brain organisation than the arthropods and that the tritocerebrum was not integrated into the brain in the last common ancestor of Onychophora and Arthropoda.