From egg to “no-body”: an overview and revision of developmental pathways in the ancient arthropod lineage Pycnogonida

Abstract

BackgroundArthropod diversity is unparalleled in the animal kingdom. The study of ontogeny is pivotal to understand which developmental processes underlie the incredible morphological disparity of arthropods and thus to eventually unravel evolutionary transformations leading to their success. Work on laboratory model organisms has yielded in-depth data on numerous developmental mechanisms in arthropods. Yet, although the range of studied taxa has increased noticeably since the advent of comparative evolutionary developmental biology (evo-devo), several smaller groups remain understudied. This includes the bizarre Pycnogonida (sea spiders) or “no-bodies”, a taxon occupying a crucial phylogenetic position for the interpretation of arthropod development and evolution.ResultsPycnogonid development is variable at familial and generic levels and sometimes even congeneric species exhibit different developmental modes. Here, we summarize the available data since the late 19th century. We clarify and resolve terminological issues persisting in the pycnogonid literature and distinguish five developmental pathways, based on (1) type of the hatching stage, (2) developmental-morphological features during postembryonic development and (3) selected life history characteristics. Based on phylogenetic analyses and the fossil record, we discuss plausible plesiomorphic features of pycnogonid development that allow comparison to other arthropods. These features include (1) a holoblastic, irregular cleavage with equal-sized blastomeres, (2) initiation of gastrulation by a single bottle-shaped cell, (3) the lack of a morphologically distinct germ band during embryogenesis, (4) a parasitic free-living protonymphon larva as hatching stage and (5) a hemianamorphic development during the postlarval and juvenile phases. Further, we propose evolutionary developmental trajectories within crown-group Pycnogonida.ConclusionsA resurgence of studies on pycnogonid postembryonic development has provided various new insights in the last decades. However, the scarcity of modern-day embryonic data – including the virtual lack of gene expression and functional studies – needs to be addressed in future investigations to strengthen comparisons to other arthropods and arthropod outgroups in the framework of evo-devo. Our review may serve as a basis for an informed choice of target species for such studies, which will not only shed light on chelicerate development and evolution but furthermore hold the potential to contribute important insights into the anamorphic development of the arthropod ancestor.

The (not very) typical protonymphons of Pycnogonum litorale

“…This number rarely corresponds directly with the number of postocular segments. We believe that only animals from superfamily Phoxichiloidea display this trait (Brenneis et al, ). In other groups segments outnumber the appendages (Alexeeva et al, ; Brenneis et al, , ; Dogiel, ; Morgan, ). Trophic type and size at hatching (used by Dogiel (), Bain (), and Burris ()).…”

“…The diversity of pycnogonid larval types is impressive. As a rule, sea spiders hatch as six‐legged protonymphons, but there are various modified lecithotrophic larvae as well (for review see Brenneis, Bogomolova, Arango, & Krapp, ).…”

“…Based on external morphology, these larvae were classified as “typical protonymphons,” together with larvae of Tanystylum orbiculare , Achelia alaskensis , Achelia laevis , Achelia sawayai , and N. brevirostre (Bain, ). This last species in particular is seen as an exemplar of typical protonymphons (Bain, ; Brenneis et al, ).…”

Phylogenomic resolution of sea spider diversification through integration of multiple data classes

“…The lack of a robust sea spider phylogeny has hindered inferences of major macroevolutionary trends in the group, such as latitudinal biogeographic patterns, larval developmental mode, and the evolution of appendages, body plans, and neuroanatomical structures [15][16][17]. While phylotranscriptomic approaches have proven remarkably effective for resolving relationships of numerous chelicerate groups [18,19], the inaccessibility of rare sea spider lineages has obviated RNA-Seq-based approaches, as cryptic and small-bodied species are often not identified in ethanol-preserved samples until weeks to years after their initial collection.…”

Why the term “larva” is ambiguous, or what makes a larva?

“…Most sea spiders hatch with only four body segments (Brenneis, Bogomolova, Arango, & Krapp, ). These protonymphon stages differ markedly from the adult (morpho‐larva s.l.)…”