Ancestral Patterning of Tergite Formation in a Centipede Suggests Derived Mode of Trunk Segmentation in Trilobites

Abstract

Trilobites have a rich and abundant fossil record, but little is known about the intrinsic mechanisms that orchestrate their body organization. To date, there is disagreement regarding the correspondence, or lack thereof, of the segmental units that constitute the trilobite trunk and their associated exoskeletal elements. The phylogenetic position of trilobites within total-group Euarthropoda, however, allows inferences about the underlying organization in these extinct taxa to be made, as some of the fundamental genetic processes for constructing the trunk segments are remarkably conserved among living arthropods. One example is the expression of the segment polarity gene engrailed, which at embryonic and early postembryonic stages is expressed in extant panarthropods (i.e. tardigrades, onychophorans, euarthropods) as transverse stripes that define the posteriormost region of each trunk segment. Due to its conservative morphology and allegedly primitive trunk tagmosis, we have utilized the centipede Strigamia maritima to study the correspondence between the expression of engrailed during late embryonic to postembryonic stages, and the development of the dorsal exoskeletal plates (i.e. tergites). The results corroborate the close correlation between the formation of the tergite borders and the dorsal expression of engrailed, and suggest that this association represents a symplesiomorphy within Euarthropoda. This correspondence between the genetic and phenetic levels enables making accurate inferences about the dorsoventral expression domains of engrailed in the trunk of exceptionally preserved trilobites and their close relatives, and is suggestive of the widespread occurrence of a distinct type of genetic segmental mismatch in these extinct arthropods. The metameric organization of the digestive tract in trilobites provides further support to this new interpretation. The wider evolutionary implications of these findings suggest the presence of a derived morphogenetic patterning mechanism responsible for the reiterated occurrence of different types of trunk dorsoventral segmental mismatch in several phylogenetically distant, extinct and extant, arthropod groups.

Fuxianhuiid ventral nerve cord and early nervous system evolution in Panarthropoda

“…Within the context of extant representatives, the postcephalic CNS of C. kunmingensis exhibits notable similarities with the thoracic VNC of the notostracan Triops cancriformis, which consists of a homonymous series of separate ganglia linked by short connectives that become progressively smaller toward the posterior end (1, 3). The overall morphology of T. cancriformis further resembles C. kunmingensis-and generally other fuxianhuiids-in the presence of dorsoventral trunk segmental mismatch expressed as appendage polypody (23,25,26). A similarly unspecialized VNC is also found in crustaceans typified by a trunk region with undifferentiated limb-bearing segments, such as the remipedes (5, 7) (Fig.…”

“…S2 A and B and S3). This organization reflects the notable dorsoventral segmental mismatch that typifies the fuxianhuiid trunk (23,25).…”

The morphology and affinities of Skania fragilis (Arthropoda) from the middle Cambrian Burgess Shale

“…These appendages were reported as attaching to the anterior anchor-shaped ridge (Glaessner 1980), unlike any known arthropod, which instead typically show considerable antero-posterior alignment of appendages and segments (Ortega-Hernández & Brena 2012), as seen in Skania and non-Precambrian "parvancorinomorphs". Such patterning is caused by antero-posterior gene expression domains that show little or no relative lateral displacement (Ortega-Hernández & Brena 2012). This also weakened likely relationships between arthropods and taxa possessing glide reflection symmetry such as Vendia, and Praecambridium (Ivantsov 2001).…”

The embryoid development of Strigamia maritimaand its bearing on post-embryonic segmentation of geophilomorph centipedes

“…Given my introduction of new early stages and the inconsistency of previous descriptions, I have decided to use the known term 'peripatoid' for the longer stage preceding the foetus stage, in accord with [27].…”

“…Once detached, this exuvia shows the entire ectoderm pattern associated with the stage 7 embryo, including the undifferentiated ectoderm covering the surface dorsal to the hemitergites (htb in Figure 1C1), which have not yet extended to complete dorsal closure. Once joined, the left and right hemitergites will give rise to the full tergite, as seen in the proembryoid I (t in Figure 1D) (see [27] for full description).…”