Investigating the Oral–Pharyngeal Structure of Early Panarthropods in Hallucigenia

Hallucigenia sparsa（圖片來源：Jose manuel canete，採用 CC BY-SA 4.0 授權）

In evolutionary terms, the phyla Arthropoda, Onychophora, Tardigrada, Nematoda, Nematomorpha, Loricifera, Kinorhyncha, and Priapulida all belong to the broader clade Ecdysozoa. In most ecdysozoans, the oral–pharyngeal region contains tooth-like elements formed from hardened cuticular structures arranged around the mouth, together with circumoral elements forming a ring-like organization. These structures have long been proposed as a potential shared derived trait of Ecdysozoa.

Modern representatives of the phylum Onychophora, such as velvet worms, present an intriguing contrast. Their oral–pharyngeal region lacks these tooth-like elements, and the surrounding tissues appear blister-like in structure (Fig. 1). This unusual morphology has prompted researchers to question how the oral–pharyngeal anatomy of onychophorans relates evolutionarily to that of other ecdysozoans.

(Figure 1) Ventral view of the head of Peripatus capensis (圖片來源：After Sedgwick，CC0 1.0 公共領域)

Two main evolutionary scenarios have therefore been proposed. The first suggests that early ecdysozoans originally possessed tooth-like structures and circumoral elements, but that these features were gradually lost after the lineage leading to onychophorans emerged. The second proposes the opposite: that early ecdysozoans initially lacked these structures, and that the different descendant lineages independently evolved similar oral armatures through convergent evolution, with onychophorans being the only group that never evolved them.

To determine whether the ancestors of onychophorans possessed tooth-like elements and circumoral structures, scientists examined the head regions of several exceptionally preserved fossils of Hallucigenia sparsa.

The genus Hallucigenia belongs to the stem group of Onychophora. These animals were small, measuring roughly 0.1–0.5 cm in length, and possessed ten pairs of appendages. The first three pairs were slender and lacked claws; they were flexible and capable of reaching the mouth, suggesting that they functioned as tentacles used to capture food. The middle five pairs were similar in length, each ending in two claws. The final two pairs near the tail were shorter and bore a single claw each. These seven posterior pairs of appendages were used for locomotion. Along the back ran a series of soft-tissue protrusions connected to seven pairs of spines that curved slightly backward.

Within the fossils, distinct carbon-rich traces were found surrounding the interior of the oral–pharyngeal region. In front of the eyes, small arc-shaped arrangements of structures were identified, which are likely circumoral elements. Behind the eyes, linear arrays interpreted as tooth-like structures extended toward the middle and posterior portions of the foregut (Fig. 2). These observations indicate that Hallucigenia, representing the stem lineage of Onychophora, still possessed both tooth-like elements and circumoral structures.

(Figure 2) Left-side cross-section of a Hallucigenia head（水也佑繪）

To further explore the evolutionary implications, researchers reconstructed an ecdysozoan phylogeny using the Fitch parsimony method (Fig. 3). The resulting tree suggests that the hardened cuticular structures forming the oral–pharyngeal apparatus were already present in the earliest ecdysozoans, supporting the idea that these structures are homologous across the group. The phylogeny also indicates that some true arthropods lack circumoral elements, implying that these features were subsequently lost in certain lineages.

(Figure 3) Phylogenetic tree of Ecdysozoa (感謝Martin R. S & Jean-Bernard Caron提供)

Apart from their defining characteristic of periodic molting, ecdysozoans exhibit relatively few obvious morphological similarities across their diverse lineages. By examining the morphology of the oral–pharyngeal region, this study provides new insight into the evolutionary relationships within Ecdysozoa.

Author: Shui Ye-You

Reference:

Smith, M. R. & Caron, J. B. (2015). Hallucigenia's head and the pharyngeal armature of early ecdysozoans. Nature.