Over the past century the discoveries of numerous Cambrian Lagerstätten (such as the Burgess Shale and Chengjiang biotas) have given us remarkable insights into the functional anatomy, development, lifestyles and behaviour of the earliest Metazoan Animals. However, their reproductive anatomy and behaviour, for the most part remains unknown. Indeed, examples of reproductive behaviour from the entire Palaeozoic Era are rare, comprising a few strands and clusters of eggs, some scattered examples of brooding in Arthropods, and the possible embrio-structures seen in Orsten-type deposits from the Cambrian of Siberia and China.
The Ecdysozoa is the single largest group of Animals today, comprising the vast Arthropod clade, plus worms such as the Nematoids and Scalidophorans (the group which includes the Priapulids). In Cambrian faunas this group seems to have been equally important, with Ecdysozoan Worms having apparently been a major part of all benthic communities, playing significant roles as bioturbators, predators and recyclers. The Scalidophorans are particularly well represented in the Burgess Shale, Chengjiang, and Qingjiang biotas.
Selkirkiid Worms are known from the Cambrian of North America, South China, and Greenland, and are probably stem group Priapulids (Worms more closely related to Priapulids than to any other living group, but which lived before the most recent common ancestor of all living Priapulids, or which are descended from such Worms but not the most recent common ancestor). They share several important morphological features with extant Priapulids, and other fossil Scalidophoran Worms, such as an eversible introvert lined with scalid rows and a circum-oral pharyngeal structure bearing teeth. However, Selkirkiids differ from Priapulids and other Scalidophorans in the presence of a conical tube, which with numerous, evenly spaced annuli, is open at both ends, encase the whole trunk, and presumably represents a cuticular structure secreted and renewed by underlying epidermal tissues. There are currently three named genera of Selkirkiids, Selkirkia from North America, Paraselkirkia from China, and Sullulika from Greenland, although it is likely that Paraselkirkia is a junior synonym of Selkirkia (i.e. these Worms should be placed in the same genus, and Paraselkirkia, having been used first, takes precedence and is the name which should be used.
In a paper published in the journal Geoscience Frontiers on 21 May 2021, Xiao-yu Yang of the Key Laboratory for Paleobiology and MEC International Joint Laboratory for Paleoenvironment at Yunnan University, Jean Vannier of the Université Claude Bernard Lyon 1, Jie Yang, also of the Key Laboratory for Paleobiology and MEC International Joint Laboratory for Paleoenvironment at Yunnan University, Deng Wang, also of the Université Claude Bernard Lyon 1, and of the Shaanxi Key Laboratory of Early Life and Environments and State Key Laboratory of Continental Dynamics at Northwest University, and Xi-guang Zhang, once again of the Key Laboratory for Paleobiology and MEC International Joint Laboratory for Paleoenvironment at Yunnan University, describe strucures which they interpret as eggs within the body cavities of the Selkirkiid Worm Paraselkirkia sinica, from the Early Cambrian Xiaoshiba Lagerstätte.
The fossils were collected from the Xiaoshiba section of the Hongjingshao Formation, roughly 3.7 km to the southeast of the village of Ala, in Kunming, Yunnan Province, and are dated to the Cambrian Stage 3 (known locally as the Canglangpuan), making them about 514 million years old.
Paraselkirkia sinica is common in both the Chengjiang and Xiaoshiba biotas, being found at many locations in China, often in dense aggregations. Yang et al. collected about 200 specimens, all preserved as two-dimensional compressions, with pellet-like gut contents; this is fairly typical for Paraselkirkia sinica specimens from the Xiaoshiba, Chengjiang and Qingjiang Lagerstätten. Both internal features (such as the gut tract) and external features (such as the introvert, pharynx, and tube) have an underlying brownish, reddish or yellowish colouration, caused by iron oxide derived from the weathering of pyrite, which in turn was deposited on the organic tissues by the action of sulphate-reducing bacteria under anaerobic conditions. This is a reasonably common feature of Cambrian Lagerstätten, seen in deposits such as the Chengjiang of South China, and the Fezouata of Morocco.
Oocyte-bearing Paraselkirkia sinica from the Cambrian Stage 3 Xiaoshiba Lagerstätte. (a), (b) YKLP 12089: (a) incomplete specimen showing partly preserved introvert, digestive tract and oocytes; (b) close-up (see location in (a)) showing oocytes within possible tubular ovaries. (c)–(e) YKLP 12350: (c) nearly complete specimen showing partly preserved introvert; (d) interpretative drawing; (e) fluorescence image (close-up, see location in (c)) showing oocytes. (f, g) YKLP 12351: (f) incomplete specimen (introvert missing) with oocytes within the tube; (g) close-up (see location in (f)) showing the egg cluster. (h), (i) YKLP 12352: (h) complete tube showing oocytes; (i) close-up (see location in (h)) showing up to 30 eggs seemingly organised in longitudinal rows. Abbreviations: ann, annulation; ct, cuticular conical tube; dt, digestive tract; gc, gut contents; in, introvert; oo, oocytes; ph, pharynx; sc, scalid; tr, trunk. Scale bar: 1 mm (a), (c), (d), (f), and (h) and 500 μm (b), (e), (g), and (i). Yang et al. (2021).
Some of the 200 specimens collected by Yang et al. were empty tubes, but many showed the remains of soft parts. Notably, eleven had clusters of ovoid elements below the midline of the trunk, with relatively sharp rounded outline. These ovoid elements often appear as conspicuous dark spots, between 300 and 450 μm in diameter. In some cases these elements clearly lie on top of the intestine and are overprinted by the annulated pattern of the tube, which Yang et al. take to indicate that they were located within the interspace between the digestive tract and the inner body wall. These objects are not randomly scattered within the body cavity, but instead, form relatively coherent clusters, in some cases spread out in elongate clusters; in some cases these appear to be arranged on either side of the gut, though in others they are clearly only on one side.
Yang et al. believe that the consistent location, shape and size of these elements strongly point towards these being eggs carried within the body cavities of female worms. Element mapping of these clusters revealed the presence of carbon, aluminium, and silicon, as well as iron and phosphorus. Micro-computerised tomography revealed exquisite details of the scalids and digestive tract, but yielded no useful information on the clustered elements. However, when one cluster was subjected to fluorescence imaging this revealed possible external envelope, which was weekly fluorescent and had sharp external margins, and an inner core, which was more strongly fluorescent, and appeared to be detached from the outer envelope.
Twenty two of the two hundred specimens have a single Brachiopod, either a Lingulate or a Kutorginate, attached to one side of the posterior end of the tube. This is consistent enough to suggest there may have been some form of symbiotic association in life. As far as Yang et al. know, the only example of epibiontic symbiosis recorded from the Xiaoshiba Lagerstätte, although such associations have been documented from other Cambrian Lagerstätten.
Yang et al. interpret the clusters of rounded objects observed in Paraselkirkia as eggs within the body cavities of female individuals, based on their consistent location, shape and size, which are comparable to the positioning of eggs within extant Priapulids. There is no evidence that these structures are attached to the tissues of the body cavity, which would be expected in a parasite infection, and they are clearly different from the gut contents, which can be seen as elongated pellet-like elements. The elemental composition analysis revealed a similar composition to that seen in the brooded eggs of Cambrian Bivalved Arthropods from other locations, such as Waptia from the Burgess Shale and Chuandianella from the Chengjiang Lagerstätte. The carbon presnt probably represents underlying thin carbon patches or particles of organic origin. The innability of micro-computed tomography probably also reflects their chemical make-up, and could be indicative of a low concentration in iron oxides compared with that seen in other features of these fossils. The structures shown by fluorescence imaging appear to be an external envelope surrounding an interior core made of a different substance, possibly a yolk or nucleus.
In modern Priapulids, such as Priapulus caudatus and Maccabeus tentaculatus, the gonads (ovaries in females and testes in males) are paired structures located in the posterior part of the trunk, which is a similar position to the structures seen in Paraselkirkia. These gonads can reach large sizes, compared to the rest of the body, and in mature females often occupy a major part of the primary body cavity. In macrobenthic species fertilisation is external with males and females releasing gametes (i.e. sperm and eggs) into the water. Females typically release thousands of oocytes (unfertilised eggs) at a time, through paired urogenital ducts opening on either side of the anus. External sexual dimorphism is rare in Priapulids.
Macrobenthic (large, bottom-dwelling) Priapulids such as Priapulus caudatus and Halicryptus spinulosus typically produce thousands of oocytes with diameters of up to 60-80μm, from ovaries which consist of a large number of ovarial sacs suspended between the gonoduct and a muscular strand. Meiobenthic (small, bottom-dwelling) species, however, produce smaller numbers of oocytes from simple tubular ovaries, although these tend to be larger. For example, Meiopriapulus fijiensis typically produces eight oocytes, but these are up to 250 μm in diameter, Tubiluchus corallicola produces about 20 oocytes reaching about 80 μm in diameter, and Maccabeus tentaculatus produces eight eggs, about 100 μm in diameter.
Comparative diagrams showing female reproductive organs in extant Priapulid Worms and early Cambrian Paraselkirkia. (a) Macrobenthic Priapulid Priapulus caudatus. (b) Meiobenthic Priapulid Tubiluchus corallicola. (c) Early Cambrian Paraselkirkia sinica. (simplified reconstruction). (d) Outline of the three forms represented at the same scale (from left to right: Priapulus, Tubiluchus and Paraselkirkia). (e) Mature oocytes of the three forms at the same scale. Primary body cavity in light blue, ovaries in dark blue, oocytes in yellow, muscular tissues in light red (around pharynx), digestive tissues in light orange, cuticle in grey. Retractor muscles may be present in Paraselkirkia but are not represented. Abbreviations: rm, retractor muscle; s, solenocytes; others as above. Yang et al. (2021).
Like modern Priapulids, the Cambrian Selkirkid Paraselkirkia sinica shows no sign of external sexual dimorphism, and there is nothing to indicate that fertilisation would have been internal in this species, and it is therefore presumed likely that egg fertilisation and embryonic dervelopmet would have been external. This would imply that the structures seen in Paraselkirkia sinica, which are 300–450 μm in diameter, are non-fertilised oocytes, not developing embryos. A maximum of only about 30 eggs is seen in any individual examined, sugesting that Paraselkirkia sinica follows the small-number-of-large-eggs strategy seen in modern meiobenthic Priapulids, although it would quite clearly be considered a macrobenthc were it alive today.
The oocyte clusters retain an cohesive appearance, suggesting that they were retained in an ovarian sac, prior to being released through the urogenital ducts. In meiobenthic Priapulids today the mature oocytes are held in place by the ovarian basal lamina, although these supporting structures such as this tend to decay rapidly after death. If similar structures were present in Paraselkirkia sinica, then they may have helped to prevent the dispersal of the oocytes throughout the body cavity, The structures revealed within the oocytes by fluorescence imaging are comparible with the nucleus of the oocytes of Priapulus caudatus, which is to say about 40% of the diameter.
Selkirkiid Worms have been interpreted variously as burrowers that possibly lived vertically embedded in sediment, or possibly epibenthic tubicolous Worms. This makes them difficult to compare directly to modern Priapulids, which are almost exclusively active infaunal burrowers. One known modern example of a tube-dwelling Priapulid does exist, Maccabeus tentaculatus, however this species reaches a maximum size of 3 mm, and forms a flimsy cylindrical tube from agglutinated plant fragments, a structure quite different from the rigid, annulated, cuticular tube of Paraselkirkia sinica. The sedentary meiobenthic Maccabeus tentaculatus uses a crown of tentacles (which are modified scalids) to catch vagile microbenthic prey such as Copepods, its tube being essentially a camouflaging device. Paraselkirkia sinica does not appear to have been particularly sedentary; it was probably less motile than non-tubicolous forms, but had a well-developed introvert, suggesting an ability to move and possibly penetrate soft sediment. It is possible that its scalids and tube annulations were anchoring features used during locomotion and excursions into the sediment, and its tube appears to have been a primarily defensive structure.
The presence of Brachiopod epibionts living on Paraselkirkia sinica also suggests a predominantly epibenthic lifestyle. Brachipods feed by filtering food from circulating water with lophophoral cilia, making it impossible for them to feed in buried in the sediment. Assuming that Cambrian Brachiopods fed in a similar way to their modern counterparts (and there is no reason to believe otherwise), then they would have been highly unlikely to regularly form a close association with an infaunal Animal. Yang et al. therefore conclude that Paraselkirkia sinica was a semi-sedentary epibenthic Animal that occasionally explored the most superficial layers of the sediment. It is possible that external fertilisation took place within the sediment.
Assumed lifestyle and reproductive mode of Paraselkirkia. (a) Living at the water-sediment interface with a juvenile Brachiopod attached near the posterior end of the tube via a short pedicle. (b) Moving slightly below the water-sediment interface for feeding or protection (e.g. possibly during moulting). (c) External fertilisation; oocytes and spermatozoids presumably emitted within sediment. (d) In-situ development of larvae. Yang et al. (2021).
Modern Brachiopods have free-swimming larvae which settle om a range of hard substrates, including the shells of many groups of invertebrates, and metamorphose into a settled form which remains attached to the same surface for the remainder of its life. Research into the Brachiopods of the Middle Cambrian Burgess Shale strongly suggests that the Brachiopods present there had already adopted this strategy, adhering to the hard tissues of Sponges in order to survive in an environment dominated by soft muds. The Brachiopods of the Xiaoshiba Lagerstätte are about six million years older than those of the Burgess Shale, and again appear to already be preferentially attaching to hard substrates in a muddy environment.
The Brachiopods attached to the Selkirkiid Worm tubes of the Xiaoshiba Lagerstätte are small, typically about 1 mm in diameter, suggesting these were either exceptionally small species, or early stages in the development of larger Brachiopods. Yang et al. favour the latter explanation, and suggest that larger Brachiopods are absent as Paraselkirkia sinica was actually a rather poor host, moving about and interacting with sediments in ways which made it unlikely a Brachiopod settling on its tube would survive to maturity.
It is unclear whether the relationship between Paraselkirkia sinica and the Brachiopods had any benefit to the Worm (i.e. was it true mutualism rather than simply commensalism). The preference of Brachiopods for a position close to the posterior opening of the tube is also enigmatic, with Yang et al. suggesting that such a position may have given the Brachiopod access to 'food particles' produced by the anus of the Worm.
Although fairly large for a Priapulid, Paraselkirkia sinica appears to show a mode of reproduction seen only in meiobenthic species (which seldom exceed 1 mm in length) today. Meiobenthic Priapulids invest a comparatively high amount in each offspring, ensuring each has a good chance of reaching maturity, Macrobenthic species today, however, produce a large number of offspring, but invest little in them as individuals, making it less likely that each individual will reach maturity, but more likely that some of them will. This later strategy makes more sense if the offspring have a high chance of being killed by things against which the adults cannot protect them, such as predation or physical damage from the environment. Adult Selkirkiid Worms do not appear to have a close ecological match today, but the similarity in reproductive styles with modern meiobenthic Priapulids does enable us to make some assumptions about the ecological pressures facing the species' juveniles.
The similarity between the basic organisation of the reproductive system in Paraselkirkia sinica and modern Priapulid Worms suggests that this organisation originated early in the history of the group. Possible embryonic and early post-embryonic Selkirkiid Worms have been suggested from the very base of the Cambrian. These are also quite large, comparable to the large oocytes seen in Paraselkirkia sinica, potentially suggesting that similar reproductive strategies may have originated by then.
Modern Animals show a very wide range of reproductive modes, which may have appeared independently in different groups Ecdysozoans are the largest single subdivision of the Metazoa today and were already an important and diverse group in the Early Cambrian. The discovery of a reproductive system in Paraselkirkia sinica brings the number of Ecdysozoans from the Early Palaeozoic where we know something about their reproductive systems to three. In Early Cambrian Waptid Arthropods egg clusters have been found carried symmetrically on either side of the female's body, which suggests paired gonads as in Paraselkirkia sinica. Copulatory organs have been preserved in Ostracods from the Early Silurian Herefordshire Lagerstätte, which suggest that these Arthropods had developed internal fertilisation by this stage.
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