Systematics, evolution and phylogeny of Annelida – a morphological perspective

Abstract

Purschke, G., Bleidorn, C. and Struck, T. 2014. Systematics, evolution and phylogeny of Annelida -a morphological perspective . Memoirs of Museum Victoria 71: 247-269.Annelida, traditionally divided into Polychaeta and Clitellata, is an evolutionary ancient and ecologically important group today usually considered to be monophyletic. However, there is a long debate regarding the in-group relationships as well as the direction of evolutionary changes within the group. This debate is correlated to the extraordinary evolutionary diversity of this group. Although annelids may generally be characterised as organisms with multiple repetitions of identically organised segments and usually bearing certain other characters such as a collagenous cuticle, chitinous chaetae or nuchal organs, none of these are present in every subgroup. This is even true for the annelid key character, segmentation. The first morphology-based cladistic analyses of polychaetes showed Polychaeta and Clitellata as sister groups. The former were divided into Scolecida and Palpata comprising Aciculata and Canalipalpata. This systematisation definitely replaced the old concept of dividing polychaetes into Errantia and Sedentaria, whereas the group Archiannelida had already been abandoned. The main critics came from a contradicting hypothesis relying on scenario based on plausibility considerations regarding Clitellata as highly derived annelids nesting within polychaetes and rendering the latter paraphyletic. In this hypothesis the absences of typical polychaete characters were regarded as losses rather than as primary absences. However, to date attempts to unambiguously identify the sister group of Clitellata on the basis of morphological characters have failed. Thus, two hypotheses on the last common annelid ancestor have been put forward either being an oligochaete-like burrowing animal or a parapodia-bearing epibenthic worm. These attempts to understand the major transitions in annelid evolution are reviewed and discussed in the light of new morphological evidence such as photoreceptor cell and eye evolution as well as the evolution of the nervous system and musculature. We also discuss the plausibility of these scenarios with regard to recent advances in molecular phylogenetic analyses.

Ammonia excretion in the marine polychaeteEurythoe complanata(Annelida)

“…Likewise, the epidermis and cuticle are always thinner than in other parts of the body. It should be noted that the annelid cuticle is a soft and flexible, rather than tight, border and is typically traversed by numerous microvilli (Hausen, 2005;Purschke et al, 2014). Mostly, annelid branchiae are supplied with efferent and afferent vessels, which give rise to some kind of connecting vessel and often blind-ended blood spaces extending deeply into the epidermal cells.…”

Breaking the ladder: Evolution of the ventral nerve cord in Annelida

“…In addition, these are usually found in highly derived positions in the phylogenetic tree. Yet, such a body plan of ground-dwelling annelids is now found to be highly derived [22] and the subepidermal position of their ventral nerve cord may either be a protective adaptation to the mechanic stress during burrowing or related to the necessity of a well-developed system of circular muscle fibers. Notably, in species with an intraepidermal VNC, the ventral longitudinal muscle bundles are usually separated from each other by the VNC and true circular musculature forming closed rings of fibers is absent [86,87].…”

“…Nonetheless, the annelid VNC shows a great diversity in number and position of neurite bundles and localization either within or beneath the epidermis [1,4,5,7,20,21]. Accordingly, the hypothesis that the ladder-like VNC is ancestral was often questioned [21][22][23][24] and challenged repeatedly, e.g., by a hypothesis regarding a pentaneuralian arrangement of the neurite bundles in the annelid VNC as ancestral [4, 5; rejected in 25] and by the finding of an unpaired mid-ventral nerve cord in numerous taxa [15,21,24,[26][27][28]. Recent, well-supported phylogenomic analyses [29][30][31][32][33] revealed that previous profound investigations into annelid neuroanatomy unfortunately focussed on representatives of derived annelid subgroups, now united as Pleistoannelida [4,5,21].…”

Developmental architecture of the nervous system in Themiste lageniformis (Sipuncula): New evidence from confocal laser scanning microscopy and gene expression

“…Annelids (bristle worms, earthworms, and leeches) are a spiralian taxon with segmented body plans and a predominant VNC with variable composition (Hejnol & Lowe, ; Müller, ; Purschke, Bleidorn, & Struck, ). Within Annelida, the ancestral nervous system was historically inferred to include a rope‐ladder‐like ventral cord (Bullock & Horridge, ; Orrhage & Müller, ; Purschke, ), with bilateral pairs of iterated ganglia joined by longitudinal connectives and transverse commissures (Richter et al, ).…”

“…Within Annelida, the ancestral nervous system was historically inferred to include a rope‐ladder‐like ventral cord (Bullock & Horridge, ; Orrhage & Müller, ; Purschke, ), with bilateral pairs of iterated ganglia joined by longitudinal connectives and transverse commissures (Richter et al, ). However, recent work has highlighted a diversity of neural arrangements among adult annelids, including species in some taxa with medullary cords and others with ventral cords containing intraepidermal neurons (Helm et al, ; Purschke, ; Purschke et al, ). And within the last decade, a series of phylogenomic studies (Andrade et al, ; Helm et al, ; Struck et al, , ; Weigert et al, ; Weigert & Bleidorn, ) have produced new hypotheses for alternative clade arrangements, followed by subsequent ancestral character state reconstructions of annelid VNC architecture suggesting that rope‐ladder‐like arrangements may have evolved more than once, through convergence (Helm et al, ).…”