Abstract
BackgroundAlthough molecular analyses have contributed to a better resolution of the animal tree of life, the phylogenetic position of tardigrades (water bears) is still controversial, as they have been united alternatively with nematodes, arthropods, onychophorans (velvet worms), or onychophorans plus arthropods. Depending on the hypothesis favoured, segmental ganglia in tardigrades and arthropods might either have evolved independently, or they might well be homologous, suggesting that they were either lost in onychophorans or are a synapomorphy of tardigrades and arthropods. To evaluate these alternatives, we analysed the organisation of the nervous system in three tardigrade species using antisera directed against tyrosinated and acetylated tubulin, the amine transmitter serotonin, and the invertebrate neuropeptides FMRFamide, allatostatin and perisulfakinin. In addition, we performed retrograde staining of nerves in the onychophoran Euperipatoides rowelli in order to compare the serial locations of motor neurons within the nervous system relative to the appendages they serve in arthropods, tardigrades and onychophorans.ResultsContrary to a previous report from a Macrobiotus species, our immunocytochemical and electron microscopic data revealed contralateral fibres and bundles of neurites in each trunk ganglion of three tardigrade species, including Macrobiotus cf. harmsworthi, Paramacrobiotus richtersi and Hypsibius dujardini. Moreover, we identified additional, extra-ganglionic commissures in the interpedal regions bridging the paired longitudinal connectives. Within the ganglia we found serially repeated sets of serotonin- and RFamid-like immunoreactive neurons. Furthermore, our data show that the trunk ganglia of tardigrades, which include the somata of motor neurons, are shifted anteriorly with respect to each corresponding leg pair, whereas no such shift is evident in the arrangement of motor neurons in the onychophoran nerve cords.ConclusionsTaken together, these data reveal three major correspondences between the segmental ganglia of tardigrades and arthropods, including (i) contralateral projections and commissures in each ganglion, (ii) segmentally repeated sets of immunoreactive neurons, and (iii) an anteriorly shifted (parasegmental) position of ganglia. These correspondences support the homology of segmental ganglia in tardigrades and arthropods, suggesting that these structures were either lost in Onychophora or, alternatively, evolved in the tardigrade/arthropod lineage.
Highlights
Molecular analyses have contributed to a better resolution of the animal tree of life, the phylogenetic position of tardigrades is still controversial, as they have been united alternatively with nematodes, arthropods, onychophorans, or onychophorans plus arthropods
Among representatives of Panarthropoda (Onychophora + Tardigrada + Arthropoda), segmental ganglia occur only in arthropods and tardigrades, whereas somata-free connectives and segmental ganglia are lacking in onychophorans, which instead show a medullary organisation of their ventral nerve cords [8,26,27,28]
The question arises of whether segmental ganglia evolved convergently in tardigrades and arthropods, or whether they are homologous structures (Figure 1B–H). If they are homologous, they might either have been present in the last common ancestor of Panarthropoda or even Ecdysozoa, or they might represent a synapomorphy uniting the tardigrades and arthropods [8]
Summary
Molecular analyses have contributed to a better resolution of the animal tree of life, the phylogenetic position of tardigrades (water bears) is still controversial, as they have been united alternatively with nematodes, arthropods, onychophorans (velvet worms), or onychophorans plus arthropods. Depending on the hypothesis favoured, segmental ganglia in tardigrades and arthropods might either have evolved independently, or they might well be homologous, suggesting that they were either lost in onychophorans or are a synapomorphy of tardigrades and arthropods To evaluate these alternatives, we analysed the organisation of the nervous system in three tardigrade species using antisera directed against tyrosinated and acetylated tubulin, the amine transmitter serotonin, and the invertebrate neuropeptides FMRFamide, allatostatin and perisulfakinin. The question arises of whether segmental ganglia evolved convergently in tardigrades and arthropods, or whether they are homologous structures (Figure 1B–H) If they are homologous, they might either have been present in the last common ancestor of Panarthropoda or even Ecdysozoa (albeit reduced in Onychophora [12]), or they might represent a synapomorphy uniting the tardigrades and arthropods [8]
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