Abstract
As one of the closest relatives of arthropods, Onychophora plays an important role in understanding the evolution of arthropod body plans. Currently there is controversy surrounding the evolution of the brain among the ecdysozoan clades, which shows a collar-shaped, circumoral organization in cycloneuralians but a ganglionic architecture in panarthropods. Based on the innervation pattern of lip papillae surrounding the mouth, the onychophoran brain has been interpreted as a circumoral ring, suggesting that this organization is an ancestral feature of Ecdysozoa. However, this interpretation is inconsistent with other published data. To explore the evolutionary origin of the onychophoran mouth and to shed light on the evolution of the ecdysozoan brains, we analyzed the innervation pattern and morphogenesis of the oral lip papillae in the onychophoran Euperipatoides rowelli using DNA labeling, immunocytochemistry, and neuronal tracing techniques. Our morphogenetic data revealed that the seven paired and one unpaired oral lip papillae arise from three anterior-most body segments. Retrograde fills show that only the first and the third nerves supplying the lip papillae are associated with cell bodies within the brain, whereas the second nerve exclusively receives fibers from somata of peripheral neurons located in the lip papillae. According to our anterograde fills and immunocytochemical data, the first nerve supplies the anterior-most pair of lip papillae, whereas the second and the third nerves are associated with the second to fifth and second to eighth lip papillae, respectively. These data suggest that the lip papillae of E. rowelli are mainly innervated by the proto- and deutocerebrum, whereas there are only a few additional cell bodies situated posterior to the brain. According to these findings, the overall innervation pattern of the oral lip papillae in E. rowelli is incompatible with the interpretation of the onychophoran brain as a modified circumoral ring.
Highlights
There are two major types of brain among ecdysozoans or molting animals (Figure 1)
Based on the innervation pattern of lip papillae surrounding the mouth, the onychophoran brain has been interpreted as a circumoral ring, suggesting that this organization is an ancestral feature of Ecdysozoa
This suggests that onychophorans have a bipartite brain, which consists of the proto- and deutocerebrum, whereas the tritocerebrum evolved in the arthropod lineage (Mayer et al, 2010)
Summary
There are two major types of brain among ecdysozoans or molting animals (Figure 1). Representatives of priapulids, kinorhynchs, nematodes and allies possess a circumoral, collarshaped brain, with anterior and posterior rings of perikarya separated by a ring-like neuropil, the name Cycloneuralia for the clade including these taxa (Bullock and Horridge, 1965; Ahlrichs, 1995; Nielsen, 2012). The onychophoran head comprises three segments, each with a pair of modified appendages (antennae, jaws and slime papillae), localization of the neuronal somata supplying these appendages has demonstrated that the region innervating the slime papillae is not differentiated as part of the brain, but rather belongs to the nerve cord (Figures 2A,B). This suggests that onychophorans have a bipartite brain, which consists of the proto- and deutocerebrum, whereas the tritocerebrum evolved in the arthropod lineage (Mayer et al, 2010)
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