The sea spider Pycnogonum litorale overturns the paradigm of the absence of axial regeneration in molting animals

Abstract

Regenerative abilities and their evolution in the different animal lineages have fascinated generations of biologists. While some taxa are capable of restoring entire individuals from small body fragments, others can regrow only specific structures or lack structural regeneration completely. In contrast to many other protostomes, including the segmented annelids, molting animals (Ecdysozoa) are commonly considered incapable of primary body axis regeneration, which has been hypothesized to be linked to the evolution of their protective cuticular exoskeleton. This holds also for the extraordinarily diverse, segmented arthropods. Contradicting this long-standing paradigm, we here show that immatures of the sea spider Pycnogonum litorale reestablish the posterior body pole after transverse amputation and can regrow almost complete segments and the terminal body region, including the hindgut, anus, and musculature. Depending on the amputation level, normal phenotypes or hypomeric six-legged forms develop. Remarkably, also the hypomeric animals regain reproductive functionality by ectopic formation of gonoducts and gonopores. The discovery of such complex regenerative patterns in an extant arthropod challenges the hitherto widely assumed evolutionary loss of axial regeneration during ecdysozoan evolution. Rather, the branching of sea spiders at the base of Chelicerata and their likely ancestral anamorphic development suggests that the arthropod stem species may have featured similar regenerative capabilities. Accordingly, our results provide an incentive for renewed comparative regeneration studies across ecdysozoans, with the aim to resolve whether this trait was potentially even inherited from the protostome ancestor.

Epimorphic development in tropical shallow-water Nymphonidae (Arthropoda: Pycnogonida) revealed by fluorescence imaging

“…[ 76 – 79 ]). But only recently, they have been exploited in first pycnogonid studies [ 65 , 80 , 81 ]. Beyond the preservation-dependent application evaluated here, these studies demonstrate the suitability of this inexpensive, non-invasive method to complement SEM or microCT-based eidonomic documentation of any pycnogonid material, including historical samples held in museum collections.…”

Investigating the developmental onset of regenerative potential in the annelid Capitella teleta

“…Younger larvae of M. alaskensis are five times more likely to regenerate than older larvae following amputation (Moss, 2018). In Ecdysozoa, the other protostome clade, regeneration ability is generally restricted to appendages, rather than along the main body axis (Brenneis et al, 2023). However, recent work shows that immature instars of the sea spider Pycnogonum litorale can regenerate the midgut and gonads as well as appendages following bisection.…”

“…However, recent work shows that immature instars of the sea spider Pycnogonum litorale can regenerate the midgut and gonads as well as appendages following bisection. Adult counterparts of P. litorale cannot regenerate and do not even survive the amputations, suggesting that regeneration ability is restricted to the immature instar stages (Brenneis et al, 2023).…”

The salamander blastema within the broader context of metazoan regeneration

“…Protostomes are typically divided into two major groups, the Ecdysozoa, containing the arthropods, nematodes and their closest relatives, and Spiralia, which contains annelids, mollusks, and Platyhelminthes amongst others ( Aguinaldo et al, 1997 ; Stechmann and Schlegel, 1999 ; Giribet, 2008 ) . Within Ecdysozoa, several arthropods have been documented to regenerate appendages ( Bely and Nyberg, 2010 ; Suzuki et al, 2019 ; Brenneis et al, 2023 ). Arthropod limb regeneration appears to depend on migratory progenitor cells, and the formation of a proliferative blastema at the tip of the regenerating limb, though, interestingly, the outward morphological manifestation arthropod blastemas conforms to the molt cycle ( Suzuki et al, 2019 ).…”