Facivermis yunnanicus reinterpreted as a tube-dwelling Early Cambrian Lobopodian.

Lobopodians are an evolutionary grade that encompasses the stem groups to the three Panarthropod phyla; Arthropoda, Onychophora, and Tardigrada. Cambrian Konservat-Lagerstätten, such as the Chengjiang Biota, Sirius Passet, Burgess Shale, nd Emu Bay Shale, yield the majority of Lobopodian material (though isolated elements also occur as microfossils), and a mosaic of Panarthropod characters are mapped across the various taxa. As such, Cambrian Lobopodians are crucial to interpreting the early evolution and deep genealogical relationships of Panarthropods, as they yield uniquely informative character combinations in phylogenetic analyses. First described in 1989, Facivermis yunnanicus is an enigmatic Worm-like animal from the early Cambrian Chengjiang Biota of Yunnan Province, China. It is asmall (under 10 cm) Bilaterian with five pairs of spiny anterior arms, an elongated body, and a swollen posterior end. The unusual morphology of Facivermis has prompted a history of diverse taxonomic interpretations, and it has been included among the Annelids (segmented Worms), Lophophorates (animals which feed using a filter called a lophophore, such as Brachiopods and Bryozoans), and Pentastomids (an enigmatic group of parasitic Crustaceans commonly known as Tongue Worms). However, in other studies, Facivermis is thought to be intermediate between Cycloneuralian Worms (Kinorhynchans, Loriciferans, Priapulids, Nematodes, and Nematomorphs) and Lobopodians. Facivermis has therefore been suggested to represent an early endobenthic-epibenthic Panarthropod transition and to provide crucial insights into the origin of paired appendages. However, the systematic affinity of Facivermis was poorly supported in a previous phylogeny, partially due to incomplete understanding of its morphology. Therefore, the evolutionary significance of Facivermis remains unresolved.

In a paper published in the journal Current Biology on 28 February 2020, Richard Howard of the International Joint Laboratory for Palaeobiology and Palaeoenvironment at Yunnan University, the Centre for Ecology and Conservation at the University of Exeter, and the Department of Earth Sciences at the Natural History Museum, Xianguang Hou, also of the International Joint Laboratory for Palaeobiology and Palaeoenvironment, and of the Yunnan Key Laboratory for Palaeobiology at Yunnan University, Gregory Edgecombe, again of the International Joint Laboratory for Palaeobiology and Palaeoenvironment at Yunnan University, and of the Department of Earth Sciences at the Natural History Museum, Tobias Salge of the Imaging and Analysis Centre, at the Natural History Museum, Xiaomei Shi, again of the International Joint Laboratory for Palaeobiology and Palaeoenvironment, and Yunnan Key Laboratory for Palaeobiology at Yunnan University, and Xiaoya Ma, again of the International Joint Laboratory for Palaeobiology and Palaeoenvironment, and Yunnan Key Laboratory for Palaeobiology at Yunnan University and Centre for Ecology and Conservation at the University of Exeter, re-examine Facivermis from new material and the holotype (original specimen), leading to the discovery of several new morphological features, and a reinterpretation of both its lifestyle and phylogenic placement.

Facivermis yunnanicus has three body regions: the anterior, middle, and posterior. The anterior comprises head and setose lobopods (five pairs). A pair of simple ocellus-like eyes is positioned dorso-laterally on the head. The middle comprises a greatly elongated and limbless portion of the trunk. The trunk is adorned with papillae and short, curved spines/setae. The posterior comprises a pear-shaped terminal swelling with two or three rings of hooks and a terminal anus. The body is enclosed within a tube.

The head is 1–2.5 mm in length. Ovoid in overall shape, with paired dorsolateral simple ocellus-like eyes preserved as dark pigment spots. The fine structure of the mouth and pharynx (i.e., any radial elements characteristic of ecdysozoans) is not visible. The mouth is terminal, appearing to bend downward slightly. Preocular appendages appear to be present in one specimen (YKLP 11378), but fidelity of preservation is insufficient to confirm whether they are comparable to the antenniform appendages of Luolishania longicruris and Collinsium ciliosum. A cephalic sclerite (plate), as in that of Luolishania longicruris, Collinsium ciliosum, and the Emu Bay Shale Luolishaniid, is absent. 

Holotype and New Material of Facivermis (A) Specimen (NIGPAS 108720) (holotype), dorsal orientation. (B) Specimen (YKLP 11378), lateral orientation, showing trunk spines/setae on dorsal and ventral trunk. (C) Specimen (YKLP 11403), in possible dorsal orientation. (D) Drawing of specimen (NIGPAS 108720). (E) Drawing of Specimen (YKLP 11378). (F) Drawing of specimen (YKLP 11403). Abbreviations: ant?, possible antenniform appendages; ca, circular attachments; h, head; m, mouth; pap, papillae; phx, pharynx; ts, trunk spines. The alimentary canal is highlighted in orange where visible, with the surrounding body cavity in dashed lines. Scale bars, (A) and (B) 2.5 mm; (C) 2 mm. Howard et al. (2020).

Behind the head the amterior portion of Facivermis yunnanicus has five pairs of slender, annulated lobopods located ventro-laterally on the anteriormost trunk. Size ranging from around 3.5 mm in length in smaller specimens (e.g. YKLP 11375) to 4 to 5 mm in larger specimens (e.g. NIGPAS 108720). The lobopods are conical in overall shape, as indicated by circular bases. Characteristic Luolishaniid setae in a double row attach ventrally with a broader base. Observed setae range in length from 0.198 to 0.335 mm in (YKLP 11375) and from 1.162 to 1.844 mm in (YKLP 11380). An average interspace of about 0.34mmfrom seta base to base is recorded from the best preserved example (YKLP 11380).

 Head and Ocular Structures of Facivermis and Luolishania. (A) Close up of the anterior region of Facivermis yunnanicus, showing the head (NIGPAS 108720). White triangles point to the simple ocellus-like eyes. (B) Close up of the anterior region of Luolishania longicruris, showing the head (YKLP 11272). White triangles point to the eyes. (C) Drawing of the anterior region of Facivermis yunnanicus (NIGPAS 108720). Eyes are highlighted in blue. (D) Drawing of the anterior region of Luolishania longicruris (YKLP 11272). Eyes are highlighted in blue. Abbreviations: ds, dorsal sclerites; s, setae. Scale bars (A) 0.5 mm; (B) 0.3 mm. Howard et al. (2020).

The swollen posterior of Facivermis yunnanicus is pear shaped and present in three specimens studied by Howard et al. (YKLP 11374, 11375, and 11403). (YKLP 11374) shows the terminal anus and (YKLP 11403) shows the rows of hooks.

New Material of Facivermis. (A) (YKLP 11377), tube-bearing specimen in possible ventral orientation. (B) Specimen (YKLP 11374), lateral orientation, showing posterior swelling and terminal anus.\(C) Specimen (YKLP 11375a), lateral orientation, showing posterior swelling. (D) Drawing of (YKLP 11377). (E) Drawing of (YKLP 11374). (F) Drawing of (YKLP 11375a).
Abbreviations: an, annuli; g, gut; l1–5 and r1–5, left/right lobopods 1–5; ph, posterior hooks; ps, posterior swelling; t, tube; ta, terminal anus. The alimentary canal is highlighted in orange where visible, with the surrounding body cavity in dashed lines. Scale bars (A) and (B) 5 mm; (C) 3 mm. Howard et al. (2020).

A through gut runs between a terminal mouth and anus of Facivermis yunnanicus, with no diverticula. The gut is narrow, preserved as black carbonaceous film, occasionally with sediment infills.

Additional Facivermis specimens. (A) Specimen (YKLP 11376), showing partial head and lobopods (unknown perspective), trunk and partial posterior. (B) Drawing of specimen (YKLP 11376), showing partial lobopods. (C) Specimen (YKLP 11381), lateral. (D) Drawing of specimen (YKLP 11381). (E) Specimen (YKLP 11379), showing head, lobopods (unknown perspective), and anterior trunk. (F) Drawing of specimen (YKLP 11379). Abbreviations: an, annuli; ant?, possible antenniform appendages; att, lobopod attachments; g, gut; l5 and l4, left lobopod 5 and 4; 1–5, unknown perspective lobopods 3–5. Scale bars: (A), (C) 5 mm, (E) 2.5 mm. Howard et al. (2020).

The tube is preserved as flat and oblong, but presumably cylindrical in life. The cuticle and soft tissues of Facivermis are preserved in a range of reds and purples, whereas the tube obscures the trunk morphology and is clearly distinguishable as a brown rusty color with a coarse texture and a straight and rigid margin. Only two specimens exhibit the tube out of 30 known specimens. (YKLP 11377) shows the trunk, lobopods, and head extending from the tube, whereas (YKLP 1379) shows only the lobopods extending from the tube. 

Fine detail of morphological features. (A) Specimen (YKLP 11381), lateral, partial tube-bearing specimen, with body withdrawn. (B) Anterior of specimen (YKLP 11374), showing circular lobopod attachments. C) Anterior of specimen (YKLP 11375a), showing lobopod setae. (D) Lobopod of specimen (YKLP 11380), showing the broad seta bases. (F) Posterior of specimen (YKLP 11374), showing potential hook row. (G) Body margin of specimen (YKLP). Abbreviations: att, lobopod attachment; lob, lobopods; ph?, possible posterior hook row; l1 and r1–5, left and right lobopods 1-5; sb,seta base; t, tube; ts, trunk spine. Scale bars: (A) 5 mm, (B) 0.3 mm, (C) 0.875 mm, (D) 1.75 mm, (E) 1 mm, (F) 0.25 mm. Howard et al. (2020).

A previous study of Facivermis yunnanicus reported occasional parapodia-like structures extended out from the trunk, which was not observed in any of Howard et al.'s specimens. However, Howard et al. do observe fine spines/setae along the annulations, which appear comparable to cuticular elements of Collinsium ciliosum. These spines are not equivalent to the metameric sclerotized armament seen in other Luolishaniids, Hallucigeniids, Onychodictyon, etc.

The new morphological and phylogenetic work presented by Howard et al. supports a Lobopodian affinity for Facivermis, as suggested by some earlier studies, and refutes an Annelid, Lophophorate, or Pentastomid affinity.

A number of Lobopodian features are identifiable in Facivermis. The head bears paired, dark spots in a dorso-lateral position. Howard et al. interpret these as ocular structures based on the presence of consistent structures in the coeval Lobopodian, Luolishania longicruris, which were interpreted as eyes preserved as residual carbon-rich visual pigments in elemental mapping analyses. The positional consistency of these structures (i.e., paired, symmetrical, and located dorso-laterally on the head) between Facivermis and Luolishania, as well as numerous other Lobopodians, supports this. These visual organs contradict a Pentastomid or Lophophorate affinity.

The appendages of Facivermis have been compared to the five pairs of head tentacles in Nereid Polychaetes to support an Annelid affinity. However, they are not consistent in position with those of Nereids, which are all on the head, unlike the metameric sequence of Facivermis’ appendages on the anterior part of the trunk. An Annelid affinity is inconsistent with the structure of Facivermis’ appendages, which exhibit circular attachments to the trunk in a ventro-lateral position. This indicates that the lobopods were conical structures rather than parapodia, which typically comprise both a dorsal notopodium and ventral neuropodium. Such circular attachments are widely documented in Lobopodians in Burgess Shale-type preservation, e.g., Paucipodia, and Aysheaia. Another study recognized the similarity of Facivermis’ appendages to the anterior lobopods of Luolishania, and Facivermis has been resolved as outgroup to Luolishaniidae (albeit with low support). Howard et al.'s study corroborates these interpretations of Facivermis as a Lobopodian.

The unique aspects of Facivermis compared to other Lobopodians are its elongated Worm-like (vermiform) body lacking posterior appendages, its hook-bearing posterior, and its dwelling tube. Combined with the suspension-feeding function of the anterior setose lobopods, Howard et al. predict that Facivermis was most likely similar to extant (but only distantly related) Feather Duster Worms, which are also tube dwelling, and suspension feed using anterior setose food-gathering appendages. Howard et al.'s interpretation contradicts previous hypotheses that Facivermis was an ambush-style predator, but endorses the idea that the appendages were not used for locomotion and that the posterior hooks represent an anchoring mechanism.

Although the dwelling tube fits the morphological adaptations exhibited by Facivermis, the tube’s rarity presents a puzzling preservation aspect. As it is unknown whether the tube was biogenic or built from sediment, it is possible that the tube had a lower preservation potential than the rest of the body. An alternative explanation is that specimens of the tube lacking a body fossil association would not have been recognized as Facivermis previously, indicating that Facivermis may have been relatively mobile (e.g., if tubes were discarded periodically).

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