The nervous and visual systems of onychophorans and tardigrades: learning about arthropod evolution from their closest relatives

Abstract

Understanding the origin and evolution of arthropods requires examining their closest outgroups, the tardigrades (water bears) and onychophorans (velvet worms). Despite the rise of molecular techniques, the phylogenetic positions of tardigrades and onychophorans in the panarthropod tree (onychophorans + tardigrades + arthropods) remain unresolved. Hence, these methods alone are currently insufficient for clarifying the panarthropod topology. Therefore, the evolution of different morphological traits, such as one of the most intriguing features of panarthropods-their nervous system-becomes essential for shedding light on the origin and evolution of arthropods and their relatives within the Panarthropoda. In this review, we summarise current knowledge of the evolution of panarthropod nervous and visual systems. In particular, we focus on the evolution of segmental ganglia, the segmental identity of brain regions, and the visual system from morphological and developmental perspectives. In so doing, we address some of the many controversies surrounding these topics, such as the homology of the onychophoran eyes to those of arthropods as well as the segmentation of the tardigrade brain. Finally, we attempt to reconstruct the most likely state of these systems in the last common ancestors of arthropods and panarthropods based on what is currently known about tardigrades and onychophorans.

Low resolution vision in a velvet worm (Onychophora)

“…Onychophorans and tardigrades possess a pair of simple lateral eyes (Greven, 2007;Mayer, 2006;Martin et al, 2017). However, tardigrades are microscopic animals (Gross et al, 2015), which makes it challenging to study their behaviour.…”

“…To date, the homology of their eyes with the visual systems of arthropods has not been resolved. Tardigrade eyes might be innovations specific to their own lineage (Greven, 2007;Martin et al, 2017), although an orthologue of the visual r-opsins (rhabdomeric opsins) of arthropods has been identified in the tardigrade Hypsibius dujardini (Hering and Mayer, 2014). In contrast, onychophorans are predators of one to several centimetres in length, inhabiting humid, terrestrial environments (Mayer et al, 2015).…”

Brain and eyes of Kerygmachela reveal protocerebral ancestry of the panarthropod head

“…Among these, the origin of the labrum has been much debated 3 – 5 . The recent discovery of an anomalocaridid with the brain preserved suggests a protocerebral innervation of the frontal appendages in stem-group euarthropods, and a homology between the frontal appendage and the labrum 1 ; however, this interpretation remains contested 6 , 7 . Furthermore, it has recently been proposed that a subdivision of the protocerebrum into prosocerebrum and archicerebrum occurred through the fusion of two appendage-bearing segments, in which the eyes are modified appendages of the archicerebral segment 2 , 3 , 8 .…”

Evaluation of contrasting techniques for X‐ray imaging of velvet worms (Onychophora)

“…This can be credited to their ancient origin, conserved morphology, and key phylogenetic position as closely related to the arthropods – the world's largest and most diverse animal group (e.g. Mayer et al ., ; Mayer, ; Martin et al ., ). In particular, onychophorans are pivotal for understanding intricate evolutionary processes underlying the successful radiation of arthropods, such as arthropodisation (evolution of jointed limbs), arthrodisation (evolution of body sclerotisation), tagmatisation (fusion of body segments into functional units) and establishment of a specialised ganglionated nervous system (Martin et al ., ).…”

“…Mayer et al ., ; Mayer, ; Martin et al ., ). In particular, onychophorans are pivotal for understanding intricate evolutionary processes underlying the successful radiation of arthropods, such as arthropodisation (evolution of jointed limbs), arthrodisation (evolution of body sclerotisation), tagmatisation (fusion of body segments into functional units) and establishment of a specialised ganglionated nervous system (Martin et al ., ). Even though onychophorans have never been investigated comprehensively by CT techniques, recent studies suggested that this method is promising for studying their anatomy and may eventually help to shed light on evolutionary questions that remain unanswered (Mayer et al ., ; Müller et al ., ).…”