Cambrian Chordates and Vetulicolians

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Review Cambrian Chordates and Vetulicolians

Mark A. S. McMenamin

Department of Geology and Geography, Mount Holyoke College, South Hadley, MA 01075, USA; [email protected]; Tel.: +1-413-538-2280

Received: 26 June 2019; Accepted: 9 August 2019; Published: 11 August 2019

Abstract: Deuterostomes make a sudden appearance in the fossil record during the early Cambrian. Two bilaterian groups, the chordates and the vetulicolians, are of particular interest for understanding early deuterostome evolution, and the main objective of this review is to examine the Cambrian diversity of these two deuterostome groups. The subject is of particular interest because of the link to vertebrates, and because of the enigmatic nature of vetulicolians. Lagerstätten in China and elsewhere have dramatically improved our understanding of the range of variation in these ancient animals. Cephalochordate and vertebrate body plans are well established at least by Cambrian Series 2. Taken together, roughly a dozen chordate genera and fifteen vetulicolian genera document part of the explosive radiation of deuterostomes at the base of the Cambrian. The advent of deuterostomes near the Cambrian boundary involved both a reversal of gut polarity and potentially a two-sided retinoic acid gradient, with a gradient discontinuity at the midpoint of the organism that is reflected in the sharp division of vetulicolians into anterior and posterior sections. A new vetulicolian (Shenzianyuloma yunnanense nov. gen. nov. sp.) with a laterally flattened, polygonal anterior section provides significant new data regarding vetulicolians. Its unsegmented posterior region (‘tail’) bears a notochord and a gut trace with diverticula, both surrounded by myotome cones.

Keywords: chordates; vetulicolians; cephalochordates; vertebrates; tunicates; Cambrian; Banﬃa; Vetulicolia; Myllokunmingia; Metaspriggina; Shenzianyuloma; agnathans; notochord; gut diverticula; myomeres; deuterostomes; all-trans-retinoic acid (ATRA); segmentation clock; morphogen gradients

1. Introduction In his 1888 book The Geological Evidences of Evolution, Angelo Heilprin, Curator of Invertebrate Paleontology and the Philadelphia Academy of Natural Sciences, made the following prediction [1]:

“Looking at the animal kingdom broadly ... we find that of the two great divisions into which that kingdom is divided, the backboned or vertebrate animals, like the fish, reptile, amphibian, and quadruped, and those without backbone, the Invertebrata, like the coral, starfish, crab, etc., only the latter is represented in the earliest period, the Cambrian, in which indisputable animals remains have been found. Not a vestige of any of the higher forms has here been met with. But let me warn you against this non-appearance. It is by no means impossible, or indeed unlikely, that backboned animals already lived during this period of time, and that their remains will still someday be discovered.”

Heilprin’s prediction [1] concerning the discovery of Cambrian vertebrates was vindicated one hundred and eleven years later with the description of Myllokunmingia in 1999. In a debate over the number of phyla in the Cambrian, S. J. Gould [2] said of the enigmatic Burgess Shale form Banﬃa (classiﬁed here as a vetulicolian):

“Consider Banﬃa, namesake of the more famous national park adjoining Yoho and the Burgess Shale. Walcott’s ‘worm’ ... is almost surely a weird wonder.”

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Gould was correct to consider Banﬃa a weird wonder, in other words, a member of a previously unknown phylum. This conclusion was problematic for Burgess Shale researchers such as Derek Briggs and Richard Fortey, who believe that there were not nearly as many Cambrian phyla [3] as inferred by Gould [2]. Gould’s interpretation, however, gained additional credence with recognition of the early Cambrian phylum Vetulicolia [4]. Phylum Vetulicolia, plus newly recognized early Cambrian chordates, lend weight to the concept of a sudden, rather than muted and long-drawn-out, Cambrian Explosion [5–7].

2. Chinese Breakthrough Two developments in paleontology were to have great impact on both the study of Proterozoic-Cambrian paleobiology and Cambrian chordates. Continuing early Western interest in Chinese Proterozoic and Cambrian strata and fossils [8,9], modern paleontological analysis of the boundary interval began in the late 1970s and early 1980s [10–12]. A critical subsequent event was the discovery in the mid-1980s of the Chengjiang Lagerstätte of the Yunnan Province, China, dated to Cambrian Series 2 [13]. Apart from Pikaia, which had long been known from the Burgess Shale (but not recognized as a chordate until 1979), the soft-bodied preservation of the Chengjiang fossils, colorfully preserved in iron oxides, has provided an astonishing glimpse at the soft-bodied early Cambrian fauna, such as the giant sclerite-lacking lobopodian Paucipodia inermis. Other examples of exceptional fossil preservation include ﬁve genera of scleroctenophores (skeletonized comb jellies) recently described from Chengjiang [14]. Discoveries from the Wulongqing Formation (Guanshan Biota; Cambrian Series 2, Stage 4) of Yunnan, China, have ampliﬁed this signal [15], as have even more recent discoveries from the Qingjiang biota [16]. Included in this suite of fossils are the oldest known chordates.

3. Cambrian Chordates A major impediment to the study of Cambrian chordates (including the phyla/subphyla Cephalochordata, Urochordata [tunicates] and Vertebrata) is that, for many forms, the most taxonomically diagnostic features (with the exceptions, fortunately, of myomeres and the notochord) tend to be the ones most prone to rapid decay, thus leading to the potential absence of key apomorphies. This results in ‘stemward slippage,’ in other words, a fossil specimen appearing more primitive than it actually is because the key derived characters are not preserved [17]. Described or reported genera of Cambrian chordates are as follows.

3.1. Cathaymyrus Assigned to the Cephalochordata [18,19], Cathaymyrus includes two, possibly synonymous, species, C. diadexus and C. haikoensis. Some researchers consider the genus to be ”a chordate of uncertain aﬃnity” [13], with D. Shu calling it “an amphioxus-like creature” [4]. The animal is remarkable for its elongate, narrowly tapered body divided by S-shaped myomeres. A notochord and a discontinuous gut trace may be present [20]. The animal may possess a notochord but lacks a well-deﬁned cranial region. Cathaymyrus is possibly synonymous with Zhongxiniscus [13].

3.2. Cheungkongella Cheungkongella is an attached, spindle-shaped sessile suspension-feeding animal that is thought to be either an early tunicate [21] or a cambroernid (an extinct non-chordate deuterostome clade that includes forms such as the eldoniids, Phlogites and Herpetogaster [22]). D. Shu [4] considers Cheungkongella to be the oldest known urochordate. Geosciences 2019, 9, 354 3 of 24

3.3. Haikouichthys GeosciencesThis 2019 agnathan, 9, x FOR ﬁsh PEER (Figure REVIEW1) was described from the Eoredlichia Zone, Qiongzhusi Formation3 nearof 23 Ercaicun, Yunnan, China [23]. Sense organs and associated structures tentatively identiﬁed in this thischordate chordate include include eyes, nasal eyes, sacs, nasal and otic sacs, capsules and [ otic4]. Possibly capsules synonymous [4]. Possibly with Myllokunmingia synonymous with[13]. Myllokunmingia [13].

Figure 1. Haikouichthys ercaicunensis. Animals are approximately 2.5 cm in length. Image credit: Talifero. Figure 1. Haikouichthys ercaicunensis. Animals are approximately 2.5 cm in length. Image credit: Used here per CC BY-SA 3.0. Talifero. Used here per CC BY-SA 3.0. 3.4. Haikouella 3.4. Haikouella This early chordate and possible agnathan [24] is represented by two species, Haikouella lanceolata and H.This jianshanensis early chordate[25]. and Filamentous possible agnathan gills are present [24] is thatrepresented are similar by totwo those species, of Yunnanozoon Haikouella lanceolata. In some andspecimens, H. jianshanensis the gill filaments [25]. Filamentous coming from gills the are gill present structure that appear are similar to be paired. to those Fin of rays Yunnanozoon are present. In in Haikouellasome specimens, as are, W-shaped the gill filaments (zigzag) coming myomeres. from Tiny the (100 gill micron)structure structures appear to that be are paired. likely Fin pharyngeal rays are presentteeth are in among Haikouella the, first as are such W- structuresshaped (zigzag) recorded myomeres. in the deuterostome Tiny (100 micron) fossil structures record. The that presence are likely of pharyngealthese teeth serve teeth toare distinguish among theHaikouella first suchas structures an agnathan recorded chordate in the as opposeddeuterostome to the fossil otherwise record. similar The presenceCambrian of hemichordate these teeth serveYunnanozoon to distinguish[24–29]. Haikouella Interestingly, as anHaikouella agnathanis interpretedchordate as to opposed have had to both the otherwisea ventral and similar a dorsal Cambrian nerve chord hemichordate [4]. Yunnanozoon [24–29]. Interestingly, Haikouella is interpreted to have had both a ventral and a dorsal nerve chord [4]. 3.5. Metaspriggina 3.5. Metaspriggina The first appearance of gill bar structures (pharyngeal gills) occurs in the Middle Cambrian fossil fromThe the Burgessfirst appearance Shale Metaspriggina of gill bar structures walcotti (Figure (pharyngeal2). Initially gills) thought occurs in to the be relatedMiddle to Cambrian the Ediacaran fossil fromecdysozoan the Burgess genus Spriggina Shale Metaspriggina, Metaspriggina walcottiis now (Fig knownure 2). to Initially be a notochord-bearing thought to be related chordate to with the Ediacaranfeatures such ecdysozoan as eyes and genus pharyngeal Spriggina bars, Metaspriggina that are comparable is now knownto those to of be fish a [30 notochord,31]. In addition,-bearing chordatethe myomeres with offeaturesMetaspriggina such as haveeyes aand distinct pharyngeal dorsal curvebars that and are W-shaped comparable pattern to those formed ofby fish an [30,31]. added Inchevron addition, in the the ventral myomeres region. of Metaspriggi Although possiblyna have due a distinct to homoplasy, dorsal curve this myomere and W-shaped configuration pattern formedstrongly by resembles an added the chevron fish pattern, in the suggesting ventral region. that Metaspriggina Although possiblymight very due well to homoplasy, be ancestral this to myomerethe gnathostomatans. configuration strongly resembles the fish pattern, suggesting that Metaspriggina might very well be ancestral to the gnathostomatans.

Figure 2. Metaspriggina walcotti.. Length Length of of animal 1010 cm.cm. PaleoArtPaleoArt credit: Nobu Nobu Tamura Tamura.. Used here per CC BY-SABY-SA 4.0.4.0.

3.6. Myllokunmingia The most ancient putative vertebrate is Myllokunmingia fengjiaoa from the Lower Cambrian Eoredlichia Zone, Qiongzhusi Formation near Ercaicun, Yunnan, China [13,19,32]. Its assignment to

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3.6. Myllokunmingia The most ancient putative vertebrate is Myllokunmingia fengjiaoa from the Lower Cambrian Geosciences 2019, 9, x FOR PEER REVIEW 4 of 23 Eoredlichia Zone, Qiongzhusi Formation near Ercaicun, Yunnan, China [13,19,32]. Its assignment to the vertebrates is is supported by by its its filamentous filamentous gills, gills, dorsal dorsal fin, fin, W W-shaped-shaped myomeres myomeres and and especially, especially, by what appear toto bebe pairedpaired sensesense organs organs in in the the head head region. region. Fin Fin rays rays are are present present in inMyllokunmingia Myllokunmingia, as, asare are W-shaped W-shaped (zigzag) (zigzag) myomeres. myomeres.Myllokunmingia Myllokunmingiais is possibly possibly synonymous synonymous with withHaikouichthys Haikouichthys[13 [13].]. 3.7. Pikaia 3.7. Pikaia Pikaia gracilens (Figure3) was initially described as a polychaete worm [ 33,34] in early descriptions Pikaia gracilens (Figure 3) was initially described as a polychaete worm [33,34] in early of soft-bodied forms from the Burgess Shale (Middle Cambrian, Bathyuriscus-Elrathina Zone). Pikaia descriptions of soft-bodied forms from the Burgess Shale (Middle Cambrian, Bathyuriscus-Elrathina eventually became famously known as the earliest described Cambrian chordate [2]. In a definitive Zone). Pikaia eventually became famously known as the earliest described Cambrian chordate [2]. In breakthrough that initiated the study of Cambrian chordates, Simon Conway Morris, in 1979, noted a definitive breakthrough that initiated the study of Cambrian chordates, Simon Conway Morris, in the similarity of Pikaia to the living cephalochordates Amphioxus and Branchiostoma, and thus extended 1979, noted the similarity of Pikaia to the living cephalochordates Amphioxus and Branchiostoma, and the geological range of Chordata back to the Middle Cambrian [35]. thus extended the geological range of Chordata back to the Middle Cambrian [35].

Figure 3. Pikaia gracilens. Length of animal 4 cm. Jellyfish in the background is a scyphozoan. PaleoArt Figure 3. Pikaia gracilens. Length of animal 4 cm. Jellyfish in the background is a scyphozoan. PaleoArt credit: Nobu Tamura. Used here per CC-BY SA 4.0. credit: Nobu Tamura. Used here per CC-BY SA 4.0. The previous most ancient chordate fossils were latest Cambrian to Cambro-Ordovician dermal The previous most ancient chordate fossils were latest Cambrian to Cambro-Ordovician dermal plates of ‘ostracoderm’ fishes such as Anatolepis, Sacabambaspis, Arandaspis and Astraspis, the latter best plates of ‘ostracoderm’ fishes such as Anatolepis, Sacabambaspis, Arandaspis and Astraspis, the latter known from the Middle Ordovician Harding Sandstone, Cannon City, Colorado, USA [36–38]. best known from the Middle Ordovician Harding Sandstone, Cannon City, Colorado, USA [36–38]. Recent analyses of Pikaia have placed it as a basal chordate [39,40], and indeed chordate Recent analyses of Pikaia have placed it as a basal chordate [39,40], and indeed chordate affinity affinity seems plausible but other possibilities, such as assignment to a new higher taxon, cannot seems plausible but other possibilities, such as assignment to a new higher taxon, cannot be dismissed be dismissed considering that Pikaia may have formed a cuticle (as occurs in some nonvertebrate considering that Pikaia may have formed a cuticle (as occurs in some nonvertebrate cephalochordates) cephalochordates) [41]. [41]. Large specimens of Pikaia reach 4 cm in length. Originally thought [35] to bear a notochord, Large specimens of Pikaia reach 4 cm in length. Originally thought [35] to bear a notochord, the the structure running along the animal’s back is now called the ‘dorsal organ’, and a notochord and/or structure running along the animal’s back is now called the ‘dorsal organ’, and a notochord and/or notochord plus nerve cord may occur in a position ventral to the dorsal organ [42]. True notochords notochord plus nerve cord may occur in a position ventral to the dorsal organ [42]. True notochords of course do occur in modern Amphioxus and Branchiostoma. Unique features of Pikaia include short of course do occur in modern Amphioxus and Branchiostoma. Unique features of Pikaia include short appendage-like structures possibly attached to the gill slits, and hagfish-like tentacles at the anterior appendage-like structures possibly attached to the gill slits, and hagfish-like tentacles at the anterior end of the animal. end of the animal. An analysis of swim mechanics in Pikaia concluded that it must have been a slow swimmer because An analysis of swim mechanics in Pikaia concluded that it must have been a slow swimmer it lacked the fast-twitch fibers that allow rapid motion in modern fish and other living chordates [42]. because it lacked the fast-twitch fibers that allow rapid motion in modern fish and other living chordates [42].

3.8. Shankouclava Known only from the Lower Cambrian Maotianshan Shale at Anning, Kunming, South China, Shankouclava anningense (Figure 4) is widely regarded as the oldest known tunicate, thanks to its apparent similarity to an individual zooid of the living, colonial aplousobranch tunicate Clavelina [43]. A stolon-bearing, club-shaped animal, Shankouclava reaches 4 cm in length. In addition to its branchial basket, a possible endostyle occurs on the fossil.

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3.8. Shankouclava Known only from the Lower Cambrian Maotianshan Shale at Anning, Kunming, South China, Shankouclava anningense (Figure4) is widely regarded as the oldest known tunicate, thanks to its apparent similarity to an individual zooid of the living, colonial aplousobranch tunicate Clavelina [43]. A stolon-bearing, club-shaped animal, Shankouclava reaches 4 cm in length. In addition to its branchial Geosciencesbasket, a 2019 possible, 9, x FOR endostyle PEER REVIEW occurs on the fossil. 5 of 23

Figure 4. Cambrian tunicate Shankouclava anningense. The animal is 4 cm in height. Image credit: Apokryltaros. Used here per CC BY-SA 3.0.

3.9. Undescribed Shankouclava-like Form A new fossil tunicate strongly resembling Shankouclava, but bearing tentacles, awaits description [13].

3.10. Yunnanozoon

The debate regarding the chordate [27,28], hemichordate [29] or even vetulicolian affinities of Figure 4. Cambrian tunicate Shankouclava anningense. The animal is 4 cm in height. Image credit: Figure 4. Cambrian tunicate Shankouclava anningense. The animal is 4 cm in height. Image credit: YunnanozoonApokryltaros. lividum Used (Fig hereure per 5) CC has BY-SA underscored 3.0. the challenges in interpreting this early chordate- like aniApokryltaros.mal. One of Used the heremost per strikingly CC BY-SA beautiful 3.0. members of the Chengjiang biota (occurring at both Chengjiang3.9. Undescribed area Shankouclava-likeand in Haikou), Yunnanozoon Form , has been variously assigned to the cephalochordates, 3.9. Undescribed Shankouclava-like Form stem-Abilaterians, new fossil tunicate stem-deuterostomes, strongly resembling stem-Shankouclavaambulacrarians,, but bearing stem-chordates, tentacles, awaits stem-hemichordates, description [13]. crownA new hemichordates, fossil tunicate cristozoans, strongly resembling vetulicolians Shankouclava and craniates,, but bearing with tentacles, one group awaits of researchersdescription concluding[13].3.10. Yunnanozoon that it is best considered at present “as a bilaterian of uncertain affinity” [13]. Known from hundreds of specimens ranging from 2–6 cm in length, Yunnanozoon differs from The debate regarding the chordate [27,28], hemichordate [29] or even vetulicolian affinities of the3.10 otherwise. Yunnanozoon comparable Haikouella by having pharyngeal teeth that are an order of magnitude Yunnanozoon lividum (Figure5) has underscored the challenges in interpreting this early chordate-like larger (1 mm) and yet, ironically, Yunnanozoon has a stomach that is not as large. Seriation occurs in animal.The Onedebate of theregarding most strikingly the chordate beautiful [27,28], members hemichordate of the [29] Chengjiang or even biotavetulicolian (occurring affinities at both of Yunnanozoon as indicated by multiple (13!) paired gonads. As in Haikouella lanceolata, in some YunnanozoonChengjiang area lividum and in(Fig Haikou),ure 5) hasYunnanozoon underscored, has the been challenges variously in assigned interpreting to the this cephalochordates, early chordate- specimens, the gill filaments coming from the gill arch appear to be paired. Although there exists no likestem-bilaterians, animal. One of stem-deuterostomes, the most strikingly beautiful stem-ambulacrarians, members of the stem-chordates, Chengjiang biota stem-hemichordates, (occurring at both clear evidence for a notochord nor myomeres in Yunnanozoon, filamentous structures attached to Chengjiangcrown hemichordates, area and in cristozoans, Haikou), Yunnanozoon vetulicolians, andhas craniates,been variously with one assigned group ofto researchersthe cephalochordates, concluding body-axis-parallel rods occur on both sides of the anterior end of the animal. It seems evident that stemthat it-bilaterians, is best considered stem-deuterostomes, at present “as a stem bilaterian-ambulacrarians, of uncertain stem affinity”-chordates, [13]. stem-hemichordates, the filamentous arches functioned as gills. crown hemichordates, cristozoans, vetulicolians and craniates, with one group of researchers concluding that it is best considered at present “as a bilaterian of uncertain affinity” [13]. Known from hundreds of specimens ranging from 2–6 cm in length, Yunnanozoon differs from the otherwise comparable Haikouella by having pharyngeal teeth that are an order of magnitude larger (1 mm) and yet, ironically, Yunnanozoon has a stomach that is not as large. Seriation occurs in YunnanozFigureoon 5. Yunnanozoonas indicated lividum by multiple. Animal is (13!) 6 cm paired in length. gonads. PaleoArt As credit: in Haikouella Cyrus Theedishman. lanceolata, Used in some Figure 5. Yunnanozoon lividum. Animal is 6 cm in length. PaleoArt credit: Cyrus Theedishman. Used specimenshere per, the CC gill BY-SA filaments 3.0. coming from the gill arch appear to be paired. Although there exists no clearhere evidence per CC forBY - aSA notochord 3.0. nor myomeres in Yunnanozoon, filamentous structures attached to bodyKnown-axis-parallel from hundredsrods occur of on specimens both sides ranging of the anterior from 2–6 end cm of in the length, animal.Yunnanozoon It seems evidentdiffers from that 3.11the filamentous. otherwise Zhongjianichthys comparable arches functionedHaikouella as gills.by having pharyngeal teeth that are an order of magnitude largerThis (1 mm)slender and eel yet,-like ironically, creature,Yunnanozoon 1.1 cm in length,has ahas stomach a thick that integument is not as [26]. large. No Seriation myomeres occurs are visiblein Yunnanozoon in the fossilas indicatedbut these bymay multiple be masked (13!) by paired its thick gonads. skin in As the in uniqueHaikouella holotype. lanceolata Th,ought in some by somespecimens, [13] to the be a gill preservational filaments coming variant from of Myllokunmingia the gill arch appear, Zhongjianichthys to be paired. is Althoughconsidered there here existsto be ano valid, clear distinct evidence genus, for a although notochord possibly nor myomeres synonymous in Yunnanozoon with Cathaymyrus, filamentous [13]. If structuresmyomeres attached are indeed to

Figure 5. Yunnanozoon lividum. Animal is 6 cm in length. PaleoArt credit: Cyrus Theedishman. Used here per CC BY-SA 3.0.

Geosciences 2019, 9, 354 6 of 24 body-axis-parallel rods occur on both sides of the anterior end of the animal. It seems evident that the ﬁlamentous arches functioned as gills.

3.11. Zhongjianichthys This slender eel-like creature, 1.1 cm in length, has a thick integument [26]. No myomeres are visible in the fossil but these may be masked by its thick skin in the unique holotype. Thought by some [13] to be a preservational variant of Myllokunmingia, Zhongjianichthys is considered here to be a valid,Geosciences distinct 2019, 9 genus,, x FOR PEER although REVIEW possibly synonymous with Cathaymyrus [13]. If myomeres are indeed6 of 23 absent, there may be a parallel between Zhongjianichthys and a genetically altered zebrafish (Danio) absent,that shows there normal may be development a parallel between of fast muscleZhongjianichthys striations butand nevera genetically develops altered myotomes zebrafish due to(Danio gene) that shows normal development of fast muscle striations but never develops myotomes due to gene knockouts (tbx6−, her1−, her7−) that stop the segmentation clock [44]. These knockouts also lead to - - - knockoutsdeformed vertebrae(tbx6 , her1 (scoliosis,, her7 ) etc.)that butstop the the mutant segmentation fish is nevertheless clock [44]. able These to swim, knockouts the biomechanical also lead to deformeddemands being vertebrae less in (scoliosis, an aquatic etc.) environment but the mutant than for fish tetrapods is nevertheless on land. Zhongjianichthys able to swim, may the biomechanicalrepresent an early demands chordate being with an less altered in an segmentation aquatic environment clock and no than myotomes, for tetrapods but nevertheless, on land. withZhongjiani an abilitychthys to may swim. represent Putative an anterior early sensory chordate structures with an include altered eyes, segmentation nasal sacs clockand a andcurious no ‘anterior-dorsalmyotomes, but lobe’nevertheless [4] that, may with have an ability performed to swim. a sensory Putative function. anterior sensory structures include eyes, nasal sacs and a curious ‘anterior-dorsal lobe’ [4] that may have performed a sensory function. 3.12. Zhongxiniscus 3.12. Zhongxiniscus Zhongxiniscus (Figure6) is a slender cephalochordate-like animal known from Haikou, Kunming, ChinaZhongxiniscus [20]. Although (FigZhongxiniscusure 6) is ahas slender along its cephalochordate dorsal margin,-like triangular animal fins, known the genus from appears Haikou, to Kunming,lack both fin China rays [20]. and Although W-shaped Zhongxiniscus myomeres, developing has along insteadits dorsal S-shaped, margin, narrowtriangular (140–145 fins, the microns genus width)appears myomeres to lack both as infinCathaymyrus rays and W.-shaped myomeres, developing instead S-shaped, narrow (140– 145 microns width) myomeres as in Cathaymyrus.

Figure 6. Zhongxiniscus. Length Length of of animal animal 1 cm. PaleoArt PaleoArt credit: Cyrus Cyrus Theedishman. Used here per CC BY BY-SA-SA 3.0. 4. Vetulicolians 4. Vetulicolians These enigmatic creatures, typified by the eponymous genus Vetulicola, have the general appearance These enigmatic creatures, typified by the eponymous genus Vetulicola, have the general of a segmented tadpole. They were originally identified as arthropods due to the apparently segmented appearance of a segmented tadpole. They were originally identified as arthropods due to the character of the ‘tail’ in some genera, but the complete absence of jointed appendages plus the apparently segmented character of the ‘tail’ in some genera, but the complete absence of jointed recognition of a series of five pairs of gill structures [45] in the anterior part of the animal led to a revised appendages plus the recognition of a series of five pairs of gill structures [45] in the anterior part of placement with the deuterostomes. They are best known from Lagerstätten such as Chengjiang [13] and the animal led to a revised placement with the deuterostomes. They are best known from Lagerstätten have recently been reported from the newly discovered Qingjiang biota [16]. such as Chengjiang [13] and have recently been reported from the newly discovered Qingjiang biota The overall shape of vetulicolians is somewhat reminiscent of bivalved crustaceans, but any [16]. resemblance to anterior tagmosis of crustaceans is superficial. The lateral line in vetulicolians represents The overall shape of vetulicolians is somewhat reminiscent of bivalved crustaceans, but any a potential plane of flexure and this may be a characteristic of their unusual body plan. resemblance to anterior tagmosis of crustaceans is superficial. The lateral line in vetulicolians Diego García-Bellido and his coauthors [46] concluded that “the common ancestor of the Vetulicolia represents a potential plane of flexure and this may be a characteristic of their unusual body plan. + Tunicata include distinct anterior and posterior body regions—the former being non-fusiform and used Diego García-Bellido and his coauthors [46] concluded that “the common ancestor of the for filter feeding and the latter originally segmented—plus a terminal mouth, absence of pharyngeal Vetulicolia + Tunicata include distinct anterior and posterior body regions—the former being non- bars, the notochord restricted to the posterior body region, and the gut extending to the end of the tail.” fusiform and used for filter feeding and the latter originally segmented—plus a terminal mouth, Two informal groups of vetulicolians are recognized here, the “soft shell vetulicolians” and the absence of pharyngeal bars, the notochord restricted to the posterior body region, and the gut “hard shell vetulicolians”. Soft shell vetulicolians lack segmentation in their posterior section or tail; extending to the end of the tail.” lack a prominent constriction between the anterior and posterior portions of the body; and have a very Two informal groups of vetulicolians are recognized here, the “soft shell vetulicolians” and the “hard shell vetulicolians”. Soft shell vetulicolians lack segmentation in their posterior section or tail; lack a prominent constriction between the anterior and posterior portions of the body; and have a very blunt, rectangular anterior. Hard shell vetulicolians have a segmented posterior section, and may have a tuberculate anterior section, at least as juveniles.

4.1. Banffia Banffia constricta (Figure 7), the first described putative vetulicolian, is a common constituent of the Middle Cambrian Burgess Shale biota. Banffia can attain a length of 10 cm. Originally assigned to the annelids, a lack of appendages has proved to be an insurmountable obstacle for assigning Banffia to Arthropoda.

Geosciences 2019, 9, 354 7 of 24 blunt, rectangular anterior. Hard shell vetulicolians have a segmented posterior section, and may have a tuberculate anterior section, at least as juveniles.

4.1. Banffia Banffia constricta (Figure7), the first described putative vetulicolian, is a common constituent of the Middle Cambrian Burgess Shale biota. Banffia can attain a length of 10 cm. Originally assigned to the annelids, a lack of appendages has proved to be an insurmountable obstacle for assigning Banffia toGeosciences Arthropoda. 2019, 9, x FOR PEER REVIEW 7 of 23

Figure 7. Banffia constricta. Length of animal 10 cm. PaleoArt credit: Apokryltaros. Used here per CC Figure 7. Banffia constricta. Length of animal 10 cm. PaleoArt credit: Apokryltaros. Used here per CC BY-SA 3.0. BY-SA 3.0. As is characteristic for vetulicolians, Banffia is divided into an anterior part and a posterior part. As is characteristic for vetulicolians, Banffia is divided into an anterior part and a posterior part. The posterior has a characteristic twist and numerous (40–50) narrow segments. There is a “crossing The posterior has a characteristic twist and numerous (40–50) narrow segments. There is a “crossing pattern” twisted section at the constriction between the anterior and posterior sections. The anus is pattern” twisted section at the constriction between the anterior and posterior sections. The anus is at the end of the posterior section and occurs in the center of a forked structure called the caudal at the end of the posterior section and occurs in the center of a forked structure called the caudal notch [47]. The anterior section or ‘carapace’ is elongate pill-shaped and largely smooth. The anterior notch [47]. The anterior section or ‘carapace’ is elongate pill-shaped and largely smooth. The anterior tip of the animal bears a corona-like structure of concentric rings or ‘circlets’. The structure is presumed tip of the animal bears a corona-like structure of concentric rings or ‘circlets’. The structure is to be the mouth of the animal. presumed to be the mouth of the animal. Fine anastomosing ridges on Banffia, identified as “micro-ichnofossils” [47], are in fact part of Fine anastomosing ridges on Banffia, identified as “micro-ichnofossils” [47], are in fact part of the structure of the animal and may represent vascular canals of some type. Comparable features the structure of the animal and may represent vascular canals of some type. Comparable features occur on Vetulicola longbaoshanensis [15]. No ‘gill slits’ are present in Banffia, and this has impeded occur on Vetulicola longbaoshanensis [15]. No ‘gill slits’ are present in Banffia, and this has impeded comparisons with other vetulicolians. J.-B. Caron [47] sees the “presence of mid-gut diverticulae in comparisons with other vetulicolians. J.-B. Caron [47] sees the “presence of mid-gut diverticulae in Banffia” to represent a possible link to protostomes. Banffia” to represent a possible link to protostomes. Banffia episoma of Utah has a considerably diminished anterior section [48]. Banffia confusa from Banffia episoma of Utah has a considerably diminished anterior section [48]. Banffia confusa from Chengjiang has gill slits on its anterior section and is thus securely placed in the Vetulicolia [47]. Chengjiang has gill slits on its anterior section and is thus securely placed in the Vetulicolia [47]. 4.2. Beidazoon 4.2. Beidazoon Beidazoon venustum is considered a ‘dwarf vetulicolian’ reaching only 8–14 mm in length [49]. TuberclesBeidazoo occurn venustum on the anterior is considered section. aThus, ‘dwarf the vetulicolian’ possibility thatreaching the fossil onlymay 8–14 represent mm in length a juvenile [49]. cannotTubercles be excluded.occur on theBeidazoon anterioris section. one of the Thus ‘hard, the shell’ possibility vetulicolians that the [49 fossil]. may represent a juvenile cannot be excluded. Beidazoon is one of the ‘hard shell’ vetulicolians [49].

4.3. Bullivetula Bullivetula variola is considered here to possibly be synonymous with (a juvenile of) Beidazoon venustum. Pronounced tubercles and pits occur on the anterior section [50].

4.4. Didazoon Somewhat resembling Pomatrum, Didazoon haoae (Figure 8) has an anterior section divided into six segments, a posterior section divided into seven segments, and a creased junction between the two [51]. Didazoon is one of the ‘soft shell’ vetulicolians [49]. Five gill ports have been identified on either side of the anterior section. The tail section is advanced dorsally.

Geosciences 2019, 9, 354 8 of 24

4.3. Bullivetula Bullivetula variola is considered here to possibly be synonymous with (a juvenile of) Beidazoon venustum. Pronounced tubercles and pits occur on the anterior section [50]. Geosciences 2019, 9, x FOR PEER REVIEW 8 of 23 4.4. Didazoon Somewhat resembling Pomatrum, Didazoon haoae (Figure8) has an anterior section divided into six segments, a posterior section divided into seven segments, and a creased junction between the two [51]. Didazoon is one of the ‘soft shell’ vetulicolians [49]. Five gill ports have been identiﬁed on

Geoscienceseither side 2019 of, 9 the, x FOR anterior PEER section.REVIEW The tail section is advanced dorsally. 8 of 23

Figure 8. Didazoon haoae. PaleoArt credit: Stanton F. Fink. Used here per CC BY-SA 2.5.

4.5. Heteromorphus Heteromorphus confusus was originally assigned to Banffia, and the possibility exists that more genera and species will need to be described with ongoing study of these morphologically variable fossils [50]. Heteromorphus is one of the ‘soft shell’ vetulicolians [49]. Figure 8. DidazoonDidazoon haoae haoae.. PaleoArt PaleoArt credit: credit: Stanton Stanton F. F. Fink. Fink. Used Used here here per per CC CC BY BY-SA-SA 2.5. 4.6. Heteromorphus Subtype New Species Form A 4.54.5.. Heteromorphus Heteromorphus This undescribed form is a ‘soft shell’ vetulicolian with an apparently unsegmented posterior Heteromorphus confusus confusus waswas originally assigned assigned to to BanffiaBanffia,, and and the the po possibilityssibility exists that more region (‘tail’) that is “covered with numerous wrinkles” [49]. The rather thick tail is thought to be genera and species will need to be described with ongoing study of these morphologically variable either an extension of both the dorsal and ventral partitions of the anterior section, or, more probably, fossils [50]. [50]. HeteromorphusHeteromorphus isis one one of of the the ‘soft ‘soft shell’ shell’ vetulicolians [49]. [49]. only an extension of the dorsal part of the anterior section [49]. 4.6. Heteromorphus Subtype New Species Form A 4.6. Heteromorphus Subtype New Species Form A 4.7. Nesonektris This undescribed form is a ‘soft shell’ vetulicolian with an apparently unsegmented posterior This undescribed form is a ‘soft shell’ vetulicolian with an apparently unsegmented posterior regionNesonektris (‘tail’) that aldridgei is “covered (Figure with 9) is numerous a vetulicolian wrinkles” described [49]. in The 2014 rather from thick the Cambrian tail is thought Emu to Bay be region (‘tail’) that is “covered with numerous wrinkles” [49]. The rather thick tail is thought to be Shaleeither anKonservat extension-Lagerstätte of both the of dorsal Kangaroo and ventral Island, partitions Australia. of the It has anterior a rather section, rectangular or, more probably, anterior either an extension of both the dorsal and ventral partitions of the anterior section, or, more probably, portiononly an extension and a laterally of the dorsal flattened, part of the paddle anterior-like section posterior [49]. section. Narrow, diamond-shaped only an extension of the dorsal part of the anterior section [49]. intersegmental membranes occur between posterior section segments. Gill structures are not evident on4.7. the Nesonektris anterior section, but a lateral groove appears on both right and left sides of the anterior section 4.7. Nesonektris alongNesonektris the line where aldridgei one would(Figure expect9) is a to vetulicolian find gill structures described [46]. in 2014 from the Cambrian Emu Bay Nesonektris aldridgei (Figure 9) is a vetulicolian described in 2014 from the Cambrian Emu Bay ShaleThe Konservat-Lagerstätte animal attained a of length Kangaroo of 1.7 Island, cm. An Australia. “axial, It rod has-like a rather structure rectangular in the anterior posterior portion body Shale Konservat-Lagerstätte of Kangaroo Island, Australia. It has a rather rectangular anterior region,”and a laterally filling flattened,much of the paddle-like “tail cavity,” posterior has been section. interpreted Narrow, as diamond-shaped a notochord [46], intersegmental thus lending portion and a laterally flattened, paddle-like posterior section. Narrow, diamond-shaped supportmembranes to the occur deuterostome between posterior interpretation section segments.of vetulicolians. Gill structures An alternate are not interpretation evident on the is that anterior the intersegmental membranes occur between posterior section segments. Gill structures are not evident thicksection, rod but structure a lateral represents groove appears a wide onposterior both right gut region, and left although sides of thean alimentary anterior section tract interpretation along the line on the anterior section, but a lateral groove appears on both right and left sides of the anterior section wouldwhere onebe difficult would expectto reconcile to find with gill fragmentation structures [46]. of this linear structure into segments intepreted as notochordalalong the line discs where [46]. one would expect to find gill structures [46]. The animal attained a length of 1.7 cm. An “axial, rod-like structure in the posterior body region,” filling much of the “tail cavity,” has been interpreted as a notochord [46], thus lending support to the deuterostome interpretation of vetulicolians. An alternate interpretation is that the thick rod structure represents a wide posterior gut region, although an alimentary tract interpretation would be difficult to reconcile with fragmentation of this linear structure into segments intepreted as notochordal discs [46].

Figure 9. Nesonektris aldridgei Figure 9. Nesonektris aldridgei. Image. Image credit: credit: Modified Modified from from D. GarcD. Garcíaía-Bellido.-Bellido. Used Used here perhere CC per BY-SA CC BY 4.0.- SA 4.0.

4.8. Ooedigera Ooedigera’s relatively large size (up to 42 mm) and tuberculate ornamentation on its anterior section sets it apart from other vetulicolians. Ooedigera (Figure 10) is known from the lower Cambrian Figure 9. Nesonektris aldridgei. Image credit: Modified from D. García-Bellido. Used here per CC BY- Sirius Passet Lagerstätte of Greenland [52]. If the tuberculate ornamentation is considered a juvenile SA 4.0. trait, as in the possible juveniles Beidazoon and Bullivetula, then Ooedigera might be considered to be a neotenous form. 4.8. Ooedigera

Ooedigera’s relatively large size (up to 42 mm) and tuberculate ornamentation on its anterior section sets it apart from other vetulicolians. Ooedigera (Figure 10) is known from the lower Cambrian Sirius Passet Lagerstätte of Greenland [52]. If the tuberculate ornamentation is considered a juvenile trait, as in the possible juveniles Beidazoon and Bullivetula, then Ooedigera might be considered to be a neotenous form.

Geosciences 2019, 9, 354 9 of 24

The animal attained a length of 1.7 cm. An “axial, rod-like structure in the posterior body region,” ﬁlling much of the “tail cavity,” has been interpreted as a notochord [46], thus lending support to the deuterostome interpretation of vetulicolians. An alternate interpretation is that the thick rod structure represents a wide posterior gut region, although an alimentary tract interpretation would be diﬃcult to reconcile with fragmentation of this linear structure into segments intepreted as notochordal discs [46].

4.8. Ooedigera Ooedigera’s relatively large size (up to 42 mm) and tuberculate ornamentation on its anterior section sets it apart from other vetulicolians. Ooedigera (Figure 10) is known from the lower Cambrian GeosciencesSirius Passet 2019, Lagerstätte9, x FOR PEER of REVIEW Greenland [52]. If the tuberculate ornamentation is considered a juvenile9 of 23 trait, as in the possible juveniles Beidazoon and Bullivetula, then Ooedigera might be considered to be a Geosciencesneotenous 2019 form., 9, x FOR PEER REVIEW 9 of 23

Figure 10. Ooedigera. Length of animal 4.2 cm. PaleoArt credit: Apokryltaros. Used here per CC BY- SA 3.0. Figure 10. Ooedigera. Length of animal 4.2 cm. PaleoArt credit: Apokryltaros. Used here per CC BY-SA 3.0. Figure 10. Ooedigera. Length of animal 4.2 cm. PaleoArt credit: Apokryltaros. Used here per CC BY- 4.94.9.. Pomatrum PomatrumSA 3.0.

4.9. PomatrumPomatrum ventralis ventralishas has a typical a typical overall overall vetulicolian vetulicolian body body form, form,with a withchicken-egg-shaped a chicken-egg- anteriorshaped anteriorportion andportion a ﬂattened, and a flat beaver-tail-liketened, beaver-tail posterior-like posterior section section or ‘tail’. orPomatrum ‘tail’. Pomatrum(Figure (Fig 11)ure is one 11) is of one the ‘softof the shell’Pomatrum ‘soft vetulicolians shell’ ventralis vetulicolians [ 49has]. Pomatrum a typical [49]. isPomatrum overall remarkable vetulicolian is for remarkable its circlet body mouth for form, its consisting circlet with a mouth chicken of concentric consisting-egg-shaped zones of anterior portion and a flattened, beaver-tail-like posterior section or ‘tail’. Pomatrum (Figure 11) is one concentricof 30 or more zones plates. of 30 Five or gillmore structures plates. Five (G1–G gill5) arestructures present (G on1– eitherG5) are side present of the on anterior either portionside of [the49]. anteriorofThe the anterior ‘soft portion shell’ section [49]. vetulicolians is smoothThe anterior apart [49]. sectionfrom Pomatrum some is smooth transverseis remarkable apart grooves. from for its someThe circlet posterior transverse mouth region grooves. consisting has ten The orof posteriorconcentricmore segments, region zones with hasof 30ten the or or anterior-most more more plates. segments, partitionsFive withgill structures becomingthe anterior (G fainter-1most–G5) and arepartitions present more closely becoming on either spaced fainterside [49 of]. andthe moreanterior closely portion spaced [49]. [49]. The anterior section is smooth apart from some transverse grooves. The posterior region has ten or more segments, with the anterior-most partitions becoming fainter and more closely spaced [49].

Figure 11. PomatrumPomatrum.. Stanton Stanton F. F. Fink. Fink. Used Used here here per per CC CC BY BY-SA -SA 2.5. 4.10. Skeemella 4.10. Skeemella Figure 11. Pomatrum. Stanton F. Fink. Used here per CC BY-SA 2.5. Skeemella, one of the strangest animals assigned to the vetulicolians, occurs in Middle Cambrian Skeemella, one of the strangest animals assigned to the vetulicolians, occurs in Middle Cambrian 4.10strata. Skeemella of Utah, USA [53]. Skeemella has a relatively small anterior section and a highly elongated posterior strata of Utah, USA [53]. Skeemella has a relatively small anterior section and a highly elongated section that is divided into dorsal and ventral plates or half-rings. A telson-like, double-pointed or posteriorSkeemella section, one that of theis divided strangest into animals dorsal assigned and ventral to the plates vetulicolians, or half-rings. occurs A in telson Middle-like, Cambrian double- forked posterior tip occurs at the end of the vermiform posterior section. This structure is presumed pointedstrata of or Utah, forked USA posterior [53]. Skeemella tip occurs has at the a relatively end of the small vermiform anterior posterior section section. and a h Thisighly structure elongated is Banffia presumedposteriorhere to be section homologoushere to thatbe homologous is to divided the caudal into to the notch dorsal caudal of and notch ventral. of Banffia plates. or half-rings. A telson-like, double- Skeemella’s placement in the Vetulicolia is controversial. Skeemella has a general morphology pointedSkeemella’s or forked placement posterior in tip the occurs Vetulicolia at the isend controversial. of the vermiform Skeemella posterior has a general section. morphology This structure that is ispresumedthat similar is similar to here theto to7– the8be stage homologous 7–8 Sytox stage green Sytox to the fluorescence green caudal fluorescence notch nuclear of Banffia- nuclear-stainedstained. embryo of embryo the millipede of the millipedeStrigamia Strigamia [54], and the resemblence may not be entirely superficial if both Skeemella and Strigamia had [54], Skeemella’sand the resemblence placement mayin the not Vetulicolia be entirely is controversial. superficial if bothSkeemella Skeemella has a andgeneral Strigamia morphology had dorsal that engrailed Skeemella expressionisdorsal similar expression to of the the 7 –segment8 of stage the segmentSytox polarity green polaritygene fluorescence engrailed gene . Skeemella nuclear. - isstained nevertheless embryois nevertheless considered of the millipede considered here to Strigamia be both here deuterostome[54], and the resemblence and vetulicolian, may notwith be the entirely dorsal -superficialventral partition if both in Skeemella the post anderior Strigamia region, with had ‘lateraldorsal line’expression partition of the between segment them polarity on both gene sides engrailed of the. Skeemella animal, is representingnevertheless consideredan extension here of tothe be ‘gill’ both- bearingdeuterostome lateral and line vetulicolian, structure seen with on the the dorsal anterior-ventral end partition of vetulicolians. in the post Someerior typeregion, of withHox- related‘lateral geneticline’ partition modification between has themevidently on both led to sides caudal of theextension animal, of representingthe vetulicolian an lateral extension line ofin Skeemellathe ‘gill’-. bearing lateral line structure seen on the anterior end of vetulicolians. Some type of Hox-related 4.11genetic. Vetulicola modification has evidently led to caudal extension of the vetulicolian lateral line in Skeemella.

4.11. TheVetulicola type species of the genus is Vetulicola cuneata [50], and it remains the best known species in the genus. Vetulicola (Figure 12) is one of the ‘hard shell’ vetulicolians [49]. Vetulicola has a ‘quadrate carapace’The type [55] species with aof ventral the genus keel, is Vetulicola a pointed cuneata dorsal [50], fin, and and it remains a segmented, the best dorsally known advancedspecies in arthropodthe genus.- Vetulicolalike posterior (Figure section. 12) is one Spindle of the-shaped ‘hard shell’ gill structuresvetulicolians are [49]. present, Vetulicola showing has a ‘quadrate what are interpretedcarapace’ [55] as with gill pouches, a ventral gill keel, filaments, a pointed and dorsal gill slits fin, [4,15,49]. and a segmented, Up to three dorsally orders advanced of faint annulationsarthropod-like occur posterior on the section.anterior Spindlebody section.-shaped Seven gill segments structures are are seen present, on the sh posteriorowing what section. are interpreted as gill pouches, gill filaments, and gill slits [4,15,49]. Up to three orders of faint annulations occur on the anterior body section. Seven segments are seen on the posterior section.

Geosciences 2019, 9, 354 10 of 24 to be both deuterostome and vetulicolian, with the dorsal-ventral partition in the posterior region, with ‘lateral line’ partition between them on both sides of the animal, representing an extension of the ‘gill’-bearing lateral line structure seen on the anterior end of vetulicolians. Some type of Hox-related genetic modiﬁcation has evidently led to caudal extension of the vetulicolian lateral line in Skeemella.

4.11. Vetulicola The type species of the genus is Vetulicola cuneata [50], and it remains the best known species in the genus. Vetulicola (Figure 12) is one of the ‘hard shell’ vetulicolians [49]. Vetulicola has a ‘quadrate carapace’ [55] with a ventral keel, a pointed dorsal ﬁn, and a segmented, dorsally advanced arthropod-like posterior section. Spindle-shaped gill structures are present, showing what are interpreted as gill pouches, gill ﬁlaments, and gill slits [4,15,49]. Up to three orders of faint annulationsGeosciences 2019, occur 9, x FOR on PEER the REVIEW anterior body section. Seven segments are seen on the posterior section.10 of 23 Vetulicola rectangulata has a relatively slender posterior region (Figure 12) but it is otherwise similar to V.Vetulicola cuneata .rectangulataVetulicola longbaoshanensis has a relatively fromslender the posterior Gushan Biotaregion has (Fig moreure 12) elaborate but it is gill otherwise structures similar [15], somewhatto V. cuneata resembling. Vetulicola those longbaoshanensis of an undescribed from the new Gushan taxon ofBiota vetulicolian has more from elaborate the Qingjiang gill structures Biota ([[15],16], Supplementarysomewhat resembling Materials). those of an undescribed new taxon of vetulicolian from the Qingjiang Biota ([16], Supplementary Materials).

Figure 12. VetulicolaVetulicola rectangulata (top(top specimen) specimen) and and VetulicolaVetulicola cuneata (center(center and and bottom bottom specimens). specimens). NoteNote,, thethe wedgewedge beakbeak in inVetulicola Vetulicola cuneata cuneata. PaleoArt. PaleoArt credit: credit: Apokryltaros. Apokryltaros. Used Used here here per per CC CC BY-SA BY- 3.0.SA 3.0. 4.12. Vetulicolian gen. et sp. Indet. A 4.12. ThisVetulicolian vetulicolian, gen. et 28sp. mmIndet. in A length, has a posterior section that is similar to Ooedigera peeli but “with a broader ﬂattened area ventrally than dorsally” [52]. The single known specimen has a relatively This vetulicolian, 28 mm in length, has a posterior section that is similar to Ooedigera peeli but smooth surface. “with a broader flattened area ventrally than dorsally” [52]. The single known specimen has a 4.13.relatively Xidazoon smooth surface.

4.13. XidazoonXidazoon [56] is a possible junior synonym of Pomatrum.

4.14.Xidazoon Yuyuanozoon [56] is a possible junior synonym of Pomatrum.

4.14. KnownYuyuanozoon only from the holotype, Yuyuanozoon magnificissimi (Figure 13) is another vetulicolian from Chengjiang [43]. Its anterior section is ovoid and comparatively smooth, with five pairs of gill structuresKnown arranged only from in a chain-likethe holotype, array Yuyuanozoon on either side magnificissimi of the anterior (Fig sectionure 13) of the is another animal. Yuyuanozoonvetulicolian reachesfrom Chengjiang over 20 cm [43]. in length.Its anterior As typical section for is ovoid vetulicolians, and comparatively its posterior smooth, section with is divided five pairs into of seven gill segments.structures The arranged posterior in section a chain is-like cylindrical, array on rather either than side being of flattened the anterior as in some section other of vetulicolians. the animal. TheYuyuanozoon anterior sectionreaches has over six 20 segments. cm in length. As typical for vetulicolians, its posterior section is divided into seven segments. The posterior section is cylindrical, rather than being flattened as in some other vetulicolians. The anterior section has six segments. The large mouth region [57,58] suggests that Yuyuanozoon may have been well suited to filter feeding strategies similar to those of a modern salp or doliodid, although any similarities are likely to be superficial. An unidentified modern doliolid (possibly genus Doliolum) bears resemblance to the anterior section of Yuyuanozoon magnificissimi [Figure 13], which might imply a filter feeding lifestyle for the latter.

Geosciences 2019, 9, 354 11 of 24 Geosciences 2019, 9, x FOR PEER REVIEW 11 of 23

Geosciences 2019, 9, x FOR PEER REVIEW 11 of 23

Figure 13. Yuyuanozoon magnificissimi with smaller Vetulicola rectangulata swimming behind. PaleoArt Figure 13. Yuyuanozoon magnificissimi with smaller Vetulicola rectangulata swimming behind. PaleoArt credit: Apokryltaros. Used here per CC BY-SA 3.0. credit: Apokryltaros. Used here per CC BY-SA 3.0. The large mouth region [57,58] suggests that Yuyuanozoon may have been well suited to filter 5.feeding Shenzianyuloma strategies similar nov. gen. to those of a modern salp or doliodid, although any similarities are likely to be superficial.A new species An unidentified of vetulicolian modern (Shenzianyuloma doliolid (possibly yunnanense genus nov.Doliolum gen.) bearsnov. sp. resemblance) from the to early the Figure 13. Yuyuanozoon magnificissimi with smaller Vetulicola rectangulata swimming behind. PaleoArt Cambriananterior section Chengjiang of Yuyuanozoon Biota (Burgess magnificissimi Shale[Figure-Type (BST)13], which deposit; might Maotianshan imply a filter Shale, feeding 518 lifestyle Ma), credit: Apokryltaros. Used here per CC BY-SA 3.0. representsfor the latter. the earliest example of ‘angelfish’ body form in a nectobenthic deuterostome (Figures 14– 24). Although the exact locality of the holotype is unknown, a specimen of the brachiopod Diadonga 5. Shenzianyuloma5. Shenzianyuloma nov.nov. gen. gen. pista occurs on the same slab (Figure 14), in accordance with matrix characteristics (yellow shale), indicatingA newA new speciesthat species the ofspecimen of vetulicolian vetulicolian is indeed ( (ShenzianyulomaShenzianyuloma derived from the yunnanense yunnanense Maotianshannov. nov. Shale. gen. gen.nov. nov. sp.) sp.) from from the the early early CambrianCambrianThe Chengjiangfossil Chengjiang was acquiredBiota Biota (Burgess (Burgess in February Shale-Type Shale - 2019Type (BST) from (BST) deposit; a deposit;crystal Maotianshan and Maotianshan fossil Shale, vendor 518 Ma), Shale, located represents 518 inMa), representsLianyungang,the earliest the example earliest Jiangsu, ofexample ‘angelfish’China. ofThis ‘angelfish’ body online form purchase in body a nectobenthic form rescued in a an deuterostomenectobenthic important specimen (Figuresdeuterostome 14 that–24 ).was (Fig Although ature risks 14 – 24).ofthe Although being exact lostlocality the to exact science of the locality holotype by vanishing of isthe unknown, holotype into a aprivate is specimen unknown, collection. of the a specimen brachiopod The specimen ofDiadonga the (IGMbrachiopod pista 5008)occurs isDiadong now on a pistaavailablethe occurs same slabforon studythe (Figure same by 14the ),slab inpaleontological accordance(Figure 14), with researchin matrixaccordance community. characteristics with matri (yellowx characteristics shale), indicating (yellow that shale) the , indicatingspecimen that isindeed the specimen derived is from indeed the Maotianshan derived from Shale. the Maotianshan Shale. TheThe fossil fossil was acquired acquired in February in February 2019 from 2019 a crystalfrom a and crystal fossil vendor and fossil located vendor in Lianyungang, located in Lianyungang,Jiangsu, China. Jiangsu, This onlineChina. purchase This online rescued purchase an important rescued specimen an important that was specimen at risk of that being was lost at to risk science by vanishing into a private collection. The specimen (IGM 5008) is now available for study by of being lost to science by vanishing into a private collection. The specimen (IGM 5008) is now the paleontological research community. available for study by the paleontological research community.

Figure 14. Shenzianyuloma yunnanense nov. gen. nov. sp. Holotype. Sample 1 of 6/25/2019; IGM 5008. B, Epifaunal brachiopod Diadonga pista. Scale bar 1 cm.

Geosciences 2019, 9, 354 12 of 24

Shenzianyuloma yunnanense nov. gen. nov. sp. is preserved as a compression fossil in yellow Chengjiang shale. The perimeter/margins of the fossil seem to be intact, suggesting that the animal in life had a slender profile as viewed from the front or back. The proximal part of the tail and midpoint of the flanks experienced minor deformation that led to displacement of some of the gill structures and, significantly,Geosciences 2019 de-nesting, 9, x FOR PEER of REVIEW one or more of the myomere cones. The gill structures have the shape12 of of 23 ovoid capsules, and one of these may have split apart, allowing gill filament-like structures to project downwardIn spite (Figures of the 17 central and 18 ). disturbance, the fossilized animal is largely intact and gives a good representationIn spite of of the the central shape disturbance, of the creature. the fossilizedShenzianyuloma animal yunnanense is largely nov. intact gen. and nov. gives sp. ais good not a representationdecayed or mutilated of the shape specimen of the of creature.a known Shenzianyulomataxon. yunnanense nov. gen. nov. sp. is not a decayedThe or rock mutilated sample specimen bearing of the a known fossil has taxon. dimensions 12 cm × 7.8 cm, and is 1.4 cm thick. The preservedThe rock length sample of bearingthe animal the fossilis 5 cm, has with dimensions an anterior 12 cm body7.8 region cm, and 4 iscm 1.4 deep cm thick. (Figure Thes preserved14 and 15). × lengthIt has ofa thedorsal animal fin (Fig is 5 cm,ure with14 and an 15) anterior with bodya saw region tooth 4margin. cm deep The (Figures anterior 14 and of the 15). animal It has ais dorsal blunt, finwith (Figures a ventral 14 and beak. 15) with a saw tooth margin. The anterior of the animal is blunt, with a ventral beak. AlthoughAlthough its its posterior posterior is is not not segmented, segmented,Shenzianyuloma Shenzianyuloma yunnanense yunnanensenov. nov. gen. gen. nov. nov. sp. sp. has has four four clearlyclearly defined defined segments segments in in the the ventral ventral part part of of its its anterior anterior portion, portion, whereas whereas the the dorsal dorsal part part of of the the anterioranterior section section where where the the dorsal dorsal fin fin attaches attaches is is smooth, smooth, almost almost domal. domal. SegmentSegment 1 1 ofof thethe ventral anterior anterior forms forms the the ‘mandible’ ‘mandible’ of ofthe the beak. beak. This This does does appear appear to be to a beak be a - beak-likelike structure, structure, as opposed as opposed to being to being some somesort of sort spinose of spinose projecti projection,on, due to due its similarity to its similarity to the ‘wedge to the ‘wedgebeak’ known beak’ known from Vetulicola from Vetulicola cuneata cuneata. Segments. Segments 2–4 increase 2–4 increase in depth in depth in a posterior in a posterior direction, direction, with withsegment segment 4 extending 4 extending downward downward to toform form the the edge edge of of a a ventral ventral keel. keel. The posterior sectionsection seemsseems to to continuecontinue as as an an extension extension of of this this segmented segmented ventral ventral part part of theof the anterior anterior section. section. This This would would be inversebe inverse to theto patternthe pattern proposed proposed for Heteromorphus for Heteromorphussubtype subtype new species new species Form A Form [49], whereA [49], the where posterior the posterior section issection thought is tothought be likely to be an likely extension an extension of the dorsal of the half dorsal of the half anterior of the section.anterior section. TheThe dorsal dorsal part part of of the the anterior anterior section section appears appears to to be be unsegmented, unsegmented, rather rather developing developing a a triangular triangular finfin that that mirrors mirrors the the profile profile of of ventral ventral segments segments 1–4 1 to–4 give to give the angelfishthe angelfish body body shape. shape. The dorsalThe dorsal fin has fin blunthas blunt teeth teeth on its on leading its leading edge edge that that increase increase in size in size in anin an anterior anterior direction. direction. The The base base of of the the dorsal dorsal finfin develops develops a a thin thin dark dark line line that that parallels parallels the the fin fin insertion insertion at at the the top top of of the the animal’s animal’s back back (Figure (Figure 16 16).). TheThe line line is is approximately approximately 0.4 0.4 mm mm from from the the base base of of the the fin. fin.

Figure 15. Shenzianyuloma yunnanense nov. gen. nov. sp. IGM 5008. Line art sketch showing morphology of the specimen. B, wedge beak; D, dorsal ﬁn with denticulate leading margin; g, gill structure;Figure 15.G, presumedShenzianyuloma gut trace; yunnanenseN, notochord. nov. gen. Scale nov. bar 1 sp.cm. IGM Image 5008. Credit: Line Mark art McMenamin. sketch showing morphology of the specimen. B, wedge beak; D, dorsal fin with denticulate leading margin; g, gill structure; G, presumed gut trace; N, notochord. Scale bar 1 cm. Image Credit: Mark McMenamin.

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Figure 16. Shenzianyuloma yunnanense nov. gen. nov. sp. IGM 5008. Dorsal fin detail showing Figure 16. Shenzianyuloma yunnanense nov. gen. nov. sp. IGM 5008. Dorsal fin detail showing denticulate margin and thin ridge that parallels the base of the fin. Photo Credit: Mark McMenamin. denticulate margin and thin ridge that parallels the base of the fin. Photo Credit: Mark McMenamin. Three (of a presumed original five) gill structures are preserved at the interface between the Three (of a presumed original five) gill structures are preserved at the interface between the segmentedThree (of ventral a presumed and smooth original dorsal five) parts gill ofstructures the anterior are sectionpreserved (Figure at the 15 interface). The posterior-most between the segmented ventral and smooth dorsal parts of the anterior section (Figure 15). The posterior-most segmentedreserved gill ventral structure and preservessmooth dorsal paired parts gill of filaments the anterior that trailsection downward (Figure 15). from The the posterior gill structure-most reserved gill structure preserves paired gill filaments that trail downward from the gill structure reserved(Figures 17 gill and structure 18). preserves paired gill filaments that trail downward from the gill structure (Figures 17 and 18).

Figure 17. Shenzianyuloma yunnanense nov. gen. nov. sp. IGM 5008. Detail of ﬁlamentous gill structure. Figure 17. Shenzianyuloma yunnanense nov. gen. nov. sp. IGM 5008. Detail of filamentous gill structure. Photo Credit: Mark McMenamin. Photo Credit: Mark McMenamin.

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FigureFigure 18.18. 18. Shenzianyuloma Shenzianyuloma yunnanense yunnanense nov.nov. nov. gen. gen. nov. nov. sp. sp.IGM IGM IGM 5008. 5008. 5008. Sketch Sketch Sketch of of gill gill of gillstructure structure and and ﬁlamentsfilamentsfilaments in in previous previous image.image. image. Image Image Credit: Credit: Mark Mark McMenamin. McMenamin.

TheThe posterior posterior section section of of Shenzianyuloma Shenzianyuloma yunnanenseyunnanense yunnanense nov.nov. nov. gen.gen. gen. nov. nov. sp. sp.provides provides key key information information aboutabout the the aaffinities ﬃaffinitiesnities ofof of thisthis this creature.creature. creature. The The ‘tail’ ‘tail’ shows shows evidence evidence for forboth both a notochord a notochord and and a distinct a distinct posteriorposterior gutgut gut trace. trace. trace. Both Both Both the the notochord the notochord notochord and and the and gutthe thetrace gut gut aretrace surroundedtrace are aresurrounded surrounded above and above below above and by and anteriorlybelow below by by slantinganteriorlyanteriorly myotomes slanting slanting myotomes (Figures myotomes 19 (Figures– 22(Fig). ure 19–22).s 19–22).

FigureFigure 19.19. 19. Shenzianyuloma Shenzianyuloma yunnanenseyunnanense yunnanensenov. nov. nov. gen. gen. gen. nov. nov. nov. sp. sp. IGM sp.IGM IG 5008. 5008.M 5008. Posterior Posterior Posterior region region region of of animal. animal. of animal. Scale Scale in Scale mm.inin mm. mm. Photo Photo Photo Credit: Credit: Credit: Mark Mark Mark McMenamin. McMenamin. McMenamin.

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Figure 20. Shenzianyuloma yunnanense nov. gen. nov. sp. IGM 5008. Detail of tail region showing Figure 20. Shenzianyuloma yunnanense nov. gen. nov. sp. IGM 5008. Detail of tail region showing notochord and posterior gut trace. Photo Credit: Mark McMenamin. notochord and posterior gut trace. Photo Credit: Mark McMenamin.

The notochord notochord is is preserved preserved as as a alight light-colored-colored band band that that runs runs along along the the dorsal dorsal half half of the of thetail.tail. Its Its widthThe notochord is approximately is preserved 3–4 mmas a light diameter,-colored and band about that 1.3 runs cm along of notochord the dorsal length half of is the preserved tail. Its width is approximately 3–4 mm diameter, and about 1.3 cm of notochord length is preserved (Figures 19(Figures–22). Two 19– 22prominent). Two prominent nodes along nodes its length along its(to lengththe right (to of the center right in of Fig centerure 22 in) Figurelikely represent22) likely 19represent–22). Two notochordal prominent discs nodes [46 along]. its length (to the right of center in Figure 22) likely represent notochordal discs [46].

Figure 21. 21. ShenzianyulomaShenzianyuloma yunnanense yunnanense nov. gen. nov. nov. sp. sp. IGM IGM 5008. 5008. Sketch Sketch of of tail tail region region from from previous previous image.image. GG,, presumed presumed gut gut trace; trace; mm,, myomeres; myomeres; m*m*,, delaminated delaminated myomere; myomere; NN,, notochord. notochord. Image Image Credit: Credit: Mark McMenamin. The gut trace is preserved as a linear structure with 7 mm preserved length. It is approximately The gut trace is preserved as a linear structure with 7 mm preserved length. It is approximately 0.35 mm in width with a distinct, very narrow central canal about 0.05 mm wide. Fine linear structures 0.35 mm in width with a distinct, very narrow central canal about 0.05 mm wide. Fine linear project at high angles to the central tube of the alimentary tract (Figures 22 and 23); these are interpreted structures project at high angles to the central tube of the alimentary tract (Figures 22 and 23); these here as gut diverticula [47]. They are definitely projections from the central gut trace, rather than being are interpreted here as gut diverticula [47]. They are definitely projections from the central gut trace, cracks or fractures of some type in the vicinity of the gut. rather than being cracks or fractures of some type in the vicinity of the gut. The diverticula connect to the main gut trace at a variety of high angles (Figure 23). In Banffia, The diverticula connect to the main gut trace at a variety of high angles (Figure 23). In Banffia, diverticula usually connect with the intestinal trace at approximate right angles, but not infrequently, diverticula usually connect with the intestinal trace at approximate right angles, but not infrequently, are offset at high angles [47] similar to the arrangement seen in Figure 23. are offset at high angles [47] similar to the arrangement seen in Figure 23.

Geosciences 2019 9 Geosciences 2019,, 9,, 354x FOR PEER REVIEW 16 of 2423 Geosciences 2019, 9, x FOR PEER REVIEW 16 of 23 A similar morphology is seen in Pomatrum cf. ventralis, specimen YKLP 10914a [50], where an A similar morphology is seen in Pomatrum cf. ventralis, specimen YKLP 10914a [50], where an alimentaryA similar tract morphology is ventral to is a seenlinear in structure Pomatrum flanked cf. ventralis by “numerous, specimen transverse YKLP 10914a lines” [50], [50] where that may an alimentary tract is ventral to a linear structure flanked by “numerous transverse lines” [50] that may alimentaryvery well represent tract is ventral a notochord to a linear surrounded structure by flanked myotome by “numerous cones. transverse lines” [50] that may very well represent a notochord surrounded by myotome cones. very wellDisturbance represent to athe notochord central part surrounded of the animal by myotome displaced cones. gill structures and caused delamination Disturbance to the central part of the animal displaced gill structures and caused delamination or or deDisturbance-nesting of the to themyotome central cones part ofin the animaltail region displaced (m* in Figgillure structures 21). This and was caused a key occurrence,delamination as de-nesting of the myotome cones in the tail region (m* in Figure 21). This was a key occurrence, as it orit demonstratedde-nesting of the the myotome presence conesof cone in- inthe-cone tail regionmyomere (m* structure in Figure in 21). Shenzianyuloma This was a key yunnanense occurrence, nov. as demonstrated the presence of cone-in-cone myomere structure in Shenzianyuloma yunnanense nov. gen. itgen. demonstrated nov. sp. Connective the presence tissues of werecone- apparentlyin-cone myomere not yet structure as strong inas Shenzianyulomathose in a modern yunnanense fish, allowing nov. nov. sp. Connective tissues were apparently not yet as strong as those in a modern fish, allowing the gen.the delamination nov. sp. Connective to occur. tissues were apparently not yet as strong as those in a modern fish, allowing delamination to occur. the delaminationMuscle fibers to are occur. visible in the myotome immediately posterior to the delaminated myotome, Muscle fibers are visible in the myotome immediately posterior to the delaminated myotome, just toMuscle the right fibers of theare middlevisible min inthe Fig myotomeure 21. immediately posterior to the delaminated myotome, just to the right of the middle m in Figure 21. just to the right of the middle m in Figure 21.

Figure 22. Shenzianyuloma yunnanense nov. gen. nov. sp. IGM 5008. Detail showing notochord and Figure 22. Shenzianyuloma yunnanense nov. gen. nov. sp. IGM 5008. Detail showing notochord and Figureposterior 22. gut Shenzianyuloma trace. Myomeres yunnanense are visible nov. in gen. both nov. the sp. dorsal IGM and 5008. ventral Detail portions showing of notochord the tail. Photo and posterior gut trace. Myomeres are visible in both the dorsal and ventral portions of the tail. Photo posteriorCredit: Mark gut McMenamin.trace. Myomeres are visible in both the dorsal and ventral portions of the tail. Photo Credit: Mark McMenamin. Credit: Mark McMenamin.

Figure 23. ShenzianyulomaShenzianyuloma yunnanense yunnanense nov.nov. gen. gen. nov. nov. sp. sp. IGM IGM 5008. 5008. Deta Detailil of alimentary of alimentary tract tract and andgut Figuregutdiverticula diverticula 23. Shenzianyuloma at the at anterior the anterior endyunnanense of end preserved of preservednov. gen. gut trace.nov. gut trace.sp. Width IGM Width of 5008. view of Deta view700 ilmicrons. 700of alimentary microns. Image Image tractCredit: and Credit: Mark gut diverticulaMarkMcMenamin. McMenamin. at the anterior end of preserved gut trace. Width of view 700 microns. Image Credit: Mark McMenamin.

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Figure 24. 24. Shenzianyuloma yunnanense yunnanense nov.nov. gen. gen. nov. sp., sp., digital reconstruction. reconstruction. This This partial reconstruction omitsomits the the dorsal dorsal ﬁn fin and and any any conjectural conjectural tail /caudaltail/caudal ‘ﬁn,’ ‘fin,’ as the as posterior the posterior tip of thetip animalof the isanimal unknown. is unknown. Image Credit:Image Credit: Mark McMenamin, Mark McMenamin, using Sculptris using Sculptris Alpha 6Alpha by Pixologic, 6 by Pixologic, Inc. Inc.

Vetulicolian Locomotion 5.1. Vetulicolian Locomotion The seemingly awkward body shape of virtually all vetulicolians begs the question of how these The seemingly awkward body shape of virtually all vetulicolians begs the question of how these creatures were able to swim and to maintain their position in the water column. The roughly triangular, creatures were able to swim and to maintain their position in the water column. The roughly angelfish-like body form of angelfish vetulicolian (Shenzianyuloma yunnanense nov. gen. nov. sp.), triangular, angelfish-like body form of angelfish vetulicolian (Shenzianyuloma yunnanense nov. gen. complete with a protruding lower ‘jaw,’ is well known from the freshwater angelfish Pterophyllum, nov. sp.), complete with a protruding lower ‘jaw,’ is well known from the freshwater angelfish the marine angelfish Pomacanthus, and a variety of fossil fishes including Eoplatex papilio and the Pterophyllum, the marine angelfish Pomacanthus, and a variety of fossil fishes including Eoplatex papilio pycnodont Proscinetes. Lacking pectoral fins or their functional equivalents, Shenzianyuloma yunnanense and the pycnodont Proscinetes. Lacking pectoral fins or their functional equivalents, Shenzianyuloma nov. gen. nov. sp. would presumably have been incapable of labriform swimming, and would yunnanense nov. gen. nov. sp. would presumably have been incapable of labriform swimming, and have relied instead on less-efficient tail propulsion. Jets of water from the gill structures may have would have relied instead on less-efficient tail propulsion. Jets of water from the gill structures may also helped to propel angelfish vetulicolian forward. The dorsal fin on the anterior section, as well have also helped to propel angelfish vetulicolian forward. The dorsal fin on the anterior section, as as its denticulate leading margin, imply at least a certain degree of controlled forward motion and well as its denticulate leading margin, imply at least a certain degree of controlled forward motion hydrodynamic stability in the water column. and hydrodynamic stability in the water column. 6. Developmental Biology of Chordate/Vetulicolian Origins 6. Developmental Biology of Chordate/Vetulicolian Origins Several aspects should be mentioned with regard to developmental biology when considering Several aspects should be mentioned with regard to developmental biology when considering the origin of Chordata and related Cambrian animals. For example, the distinction between the tiny the origin of Chordata and related Cambrian animals. For example, the distinction between the tiny pharyngeal teeth of Haikouella and the larger pharyngeal teeth of Yunnanozoon, homologous features [7] pharyngeal teeth of Haikouella and the larger pharyngeal teeth of Yunnanozoon, homologous features between the two genera, represents the range of variation seen in the early chordate anterior scleritome. [7] between the two genera, represents the range of variation seen in the early chordate anterior The body division into two halves in vetulicolians has been invoked as an illustration of Romer’s scleritome. somato-visceral theory [51,59]. It seems reasonable to speculate that a discontinuity in all-trans-retinoic The body division into two halves in vetulicolians has been invoked as an illustration of Romer’s acid (ATRA)-FGF morphogen signaling molecules has occurred at the vetulicolian midline; thus, somato-visceral theory [51,59]. It seems reasonable to speculate that a discontinuity in all-trans- in vetulicolians, the anterior part of the animal and the posterior part of the animal may have been retinoic acid (ATRA)-FGF morphogen signaling molecules has occurred at the vetulicolian midline; dominated by different molecular signaling regimes. For example, a dual retinoic acid gradient is thus, in vetulicolians, the anterior part of the animal and the posterior part of the animal may have involved in down-regulating FGF8 to permit somitogenesis. Interestingly, the gradient is at a minimum been dominated by different molecular signaling regimes. For example, a dual retinoic acid gradient value at the head/tail junction, and reaches a maximum in the anterior section [60]. is involved in down-regulating FGF8 to permit somitogenesis. Interestingly, the gradient is at a The (ATRA)-FGF double-sided retinoic acid gradient signal isolation seems to be particularly minimum value at the head/tail junction, and reaches a maximum in the anterior section [60]. pronounced in Skeemella [53]. Somite/segmentation formation is dramatically favored in the posterior The (ATRA)-FGF double-sided retinoic acid gradient signal isolation seems to be particularly section and more subdued (although still present) in the anterior section, suggesting that the same pronounced in Skeemella [53]. Somite/segmentation formation is dramatically favored in the posterior posterior-generated signaling factor is influencing segmentation in both the posterior (influence strong) section and more subdued (although still present) in the anterior section, suggesting that the same posterior-generated signaling factor is influencing segmentation in both the posterior (influence strong) and anterior (influence weak) sections, with the presumed ATRA gradient dropping off

Geosciences 2019, 9, 354 18 of 24 and anterior (influence weak) sections, with the presumed ATRA gradient dropping off sharply across the anterior–posterior sections division [61]. Here, we see a potential unification of the morphogenetic field and gradient signaling approaches, with a morphogenetic field discontinuity demarcating fields of morphogen signaling factor influence. The serial gene duplications known to have occurred in vertebrates, gnathostomes and teleost fish evidently cannot be linked to the “evolution of complexity in vertebrates” [29].

7. Conclusions Among living chordates, molecular phylogeny shows that tunicates are more closely related to vertebrates (they jointly form the Olfactores) than vertebrates are to lancelets (Cephalochordata [61,62]). Curiously, in the latter analysis, “the monophyly of deuterostomes remained poorly supported” [62]. The reliability of molecular clocks based on these data (“most major lineages of deuterostomes arose prior to the Cambrian Explosion” [61]) is open to question, considering that few if any deuterostome fossils are known from strata deposited before the Cambrian boundary. In any case, the general consensus is that vertebrates first appeared in the Cambrian [63]. A putative exception to this general rule of Cambrian chordate appearance is the identification of Burykhia hunti from Ediacaran strata of the White Sea region, Russia and Ausia fenestrata from the Nama Group in Namibia, as the oldest known ascidians [64]. It seems highly unlikely that members of the Ausiidae are urochordates, considering that their morphology consists of tubes or bags with serial perforations. The presence of a zig-zag medial suture in Burykhia suggests rather that the fossils are more properly allied with frondose ‘vendobiont’ Ediacarans such as Charnia, Rangea, Phyllozoon and Pteridinium. It seems quite plausible that the advent of deuterostomes near the Cambrian boundary involved both a reversal of gut polarity and a two-sided retinoic acid gradient, with a gradient discontinuity at the midpoint of the organism that is reflected in the characteristic division of vetulicolians into morphologically distinct anterior and posterior sections. The posterior section of Shenzianyuloma yunnanense nov. gen. nov. sp. demonstrates that vetulicolians are indeed deuterostomes allied to chordates [65], due to Shenzianyuloma’s notochord (with discs) in a position that is dorsal to an alimentary tract with diverticula, and also due to the presence of myotome cones [66] with preserved muscle fibers. It is now possible to review the current state of knowledge regarding Cambrian chordates, vetulicolians and their affinities. All of these animals are deuterostomes (i.e., the blastopore becomes the anus during early ontogeny), although of course, other deuterostomes are also known from the early Cambrian (cambroernids, echinoderms and hemichordates). Three groups may be recognized among the Cambrian chordates. Urochordates, characterized by the presence of a branchial basket, are represented by Cheungkongella and Shankouclava. Cephalochordates, characterized by a full notochord, are represented by four genera: Cathaymyrus Pikaia (with question), Zhongjianichthys, and Zhongxiniscus. Vertebrates, characterized by a neural crest, are also represented by four genera: Haikouella, Haikouichthys, Metaspriggina and Myllokunmingia. Vetulicolians are characterized by their bipartite body form and by five pairs of gill structures. Two informal groups of vetulicolians can be recognized, the “soft shell vetulicolians” and the “hard shell vetulicolians”. Soft shell vetulicolians lack segmentation in their posterior section or tail; lack a prominent constriction between the anterior and posterior portions of the body; and have a very blunt, rectangular anterior. Hard shell vetulicolians have a segmented posterior section, and may have a tuberculate anterior section, at least as juveniles. Soft shell vetulicolians are represented by: Didazoon, Heteromorphus, Pomatrum and Xidazoon. Hard shell vetulicolians are represented by six genera: Beidazoon, Bullivetula, Nesonektris, Ooedigera, Vetulicola and Yuyuanozoon. Geosciences 2019, 9, 354 19 of 24

Skeemella and Shenzianyuloma are unique, unusual vetulicolians that cannot be placed in either the soft shell or hard shell clade. Yunnanozoan, although surely a bilaterian deuterostome, cannot be conﬁdently placed in either the chordates or the vetulicolians. Taken together, these chordate and vetulicolian genera document an important part of the explosive radiation of deuterostomes at the base of the Cambrian. Although debate is likely to continue, the preponderance of the evidence does suggest that vetulicolians and yunnanozoans are indeed deuterostomes [47,50,52,53,67–71]. Although deuterostomes, the extremely odd character set in vetulicolians also suggests that they may very well represent a higher taxon of phylum rank. Great caution, however, is needed in order to avoid circular reasoning with regard to the use of gross morphology to make such phylogenetic claims. The ﬁve pairs of gill structures in vetulicolians could in fact represent mid-gut glands of some sort, although this seems unlikely. The bizarre carpoids, with (like vetulicolians) a bipartite body division are now considered to be regular echinoderms with no gill slits and a feeding arm with a normal water vascular system [72]. Still, the mythical chimaera-like nature of many of the early deuterostomes suggests that the group may very well require the erection of multiple extinct phylum-level taxa to avoid systematic shoehorning. Aldridge et al. [50] note that although the vetulicolians “appear to form a monophyletic clade, it is premature to accord them phylum rank without resolution of their phylogenetic position.” This remains a cogent observation, for indeed, with Shenzianyuloma yunnanense nov. gen. nov. sp. displaying evidence for conical myomeres surrounding a notochord with discs, the possibility that Shenzianyuloma and other vetulicolians represent stem chordates must be seriously considered.

8. Systematic Paleontology Repository data: IGM, Institute of Geology Museum, Departmento de Paleontología, Cuidad Universitaria, Delegacíon de Coyoacán, 04510, México; YKLP, Key Laboratory for Palaeobiology, Yunnan University, Kunming, China. Kingdom Animalia Superphylum Deuterostomia Phylum Vetulicolia

Genus Shenzianyuloma nov. gen.

Diagnosis: Vetulicolian with a body divided into a broad, laterally flattened anterior section and relatively narrow posterior or tail region. The anterior section is divided into a relatively smooth dorsal part with a denticulate dorsal fin and a segmented or partitioned ventral part. The dorsal fin has a thin ridge that parallels the base of the fin. A wedge beak occurs at the anterior junction of the dorsal and ventral parts. Five gill structures with filaments occur between the dorsal and ventral parts of the anterior section. The dorsal and ventral parts of the anterior section have approximately similar (but inverted relative to one another) profiles. The unsegmented posterior or tail region develops a notochord, a gut trace with diverticula, and at least seven myomeres. The posterior tip of the tail region is unknown. Description: This vetulicolian has an unsegmented posterior section (‘tail’) and anterior section that is segmented only in its ventral part, where four segments occur. Gill structures occur between the dorsal and ventral parts of the anterior section. At the anterior of the animal, a wedge beak forms from segment 1 at the juncture between the dorsal and ventral anterior section parts. The sagittal crest bears a dorsal fin with a denticulate anterior margin. The dorsal fin has blunt teeth on its leading edge that increase in size toward the front of the fin. The base of the dorsal fin shows a thin dark linear ridge that parallels the fin insertion at the top of the animal’s back, at a distance of 0.4 mm from the fin base (Figure 16). A thin keel forms the ventral margin of the anterior section, and the anterior-ventral profile roughly matches that of the main dorsal fin. The dorsal part of the narrow, dorsally advanced posterior section bears three fins, two larger and flap-shaped and a posterior one that is much smaller. Geosciences 2019, 9, 354 20 of 24

The posterior section has both a notochord (with notochordal discs) and distinct gut trace (with diverticula). Both notochord and gut/intestine are surrounded by conical myotomes. Extremely fine lines project at approximate right angles to the central tube of the alimentary tract (Figure 22); these represent gut diverticula [44]. Discussion: The posterior tip of Shenzianyuloma yunnanense nov. gen. nov. sp. is unknown due to breakage in the holotype. The presence of myotomes strongly suggest that Shenzianyuloma yunnanense nov. gen. nov. sp. is both a deuterostome and a chordate. Shenzianyuloma yunnanense nov. gen. nov. sp. resembles “Heteromorphus subtype new species Form A” [46] in being a ‘soft shell’ vetulicolian form that: lacks segmentation in its posterior section or tail; lacks a prominent constriction between the anterior and posterior portions of the body; and has a very blunt, rectangular anterior. Shenzianyuloma yunnanense nov. gen. nov. sp. differs from “Heteromorphus subtype new species Form A” by having: a narrower tail that lacks wrinkles; anteriorly slanting myotome-like structures; a wedge beak; and several flap- or scoop-like fins along the dorsal edge of its posterior section. A gut trace extends to the preserved end of the tail in Shenzianyuloma yunnanense nov. gen. nov. sp. As in Haikouella and Myllokunmingia, gill filaments that proceed from the gill structure in Shenzianyuloma appear to be paired. Sagittal plane expansion and lateral flattening of the anterior section of Shenzianyuloma provides a striking morphological contrast to the dorsal-ventral flattening of the anterior section of the Burgess Shale vetulicolid Banffia constricta (Figure7), thereby expanding our knowledge of the range of form in this important group of early deuterostomes. The dorsal fin in Shenzianyuloma is comparable to the dorsal fin of Myllokunmingia, although Myllokunmingia’s dorsal fin has a comparatively lower profile [4] and lacks the denticles on the leading edge of the fin. Shenzianyuloma yunnanense nov. gen. nov. sp. resembles “Heteromorphus subtype new species Form A” [46] in being a ‘soft shell’ form that: lacks segmentation in its posterior section or tail; lacks a prominent constriction between the anterior and posterior portions of the body; and has a very blunt, rectangular anterior end. Shenzianyuloma yunnanense nov. gen. nov. sp. differs from “Heteromorphus subtype new species Form A” by having: a narrower tail that lacks wrinkles, but has anteriorly slanting myotome-like structures, and a wedge beak. A gut trace extends to the preserved end of the tail in Shenzianyuloma yunnanense nov. gen. nov. sp. As in Haikouella and Myllokunmingia, gill filaments that proceed from the gill structure in Shenzianyuloma appear to be paired. A unique ‘dorsal fin’ in Shenzianyuloma yunnanense nov. gen. nov. sp. mirrors the profile of the ventral cuticular plate. The anterior end of the latter forms a ‘wedge beak’ similar to that described from Vetulicola cuneata. The wedge beak-bearing cuticular plate consists of three articulating sections, implying a dentary-like mobility in what appears to be the earliest beak-like ‘jaw’ structure reported from a deuterostome. Whether or not Shenzianyuloma yunnanense nov. gen. nov. sp. also has a vertical mouth (‘M’ in [46]) as inferred for “Heteromorphus subtype new species Form A” is unknown. If so, Shenzianyuloma may have had a dual oral apparatus, a biting beak at the lower part of the mouth (i.e., jaw with horizontal opening) and a blunt, elongate ‘M’ mouth opening that forms a vertical gape for the purposes of filter feeding. The anteriorly slanting myotome-like structures of Shenzianyuloma yunnanense nov. gen. nov. sp. strongly support the hypothesis that vetulicolians are deuterostomes rather than arthropod-like protostomes. Etymology: The genus name is a neuter noun formed as a combination and rearrangement of the Chinese word for angelfish (Shénxian¯ yú, 神仙鱼) and an anagram of the genus name for the ocean sunfish, Mola.

Shenzianyuloma yunnanense nov. gen. nov. sp.: Figures 14–24

Holotype: Field sample 1 of 6/25/2019; IGM 5008. Description: Same as for genus, by monotypy. Geosciences 2019, 9, 354 21 of 24

Etymology: The trivial name, in honor of Yunnan, China, is rendered here “yunnanense” rather than “yunnanensis” to agree in gender with the neuter noun Shenzianyuloma. Age and Locality Information: Early Cambrian Chengjiang Biota (Burgess Shale-Type (BST) deposit; Maotianshan Shale, 518 Ma).

Supplementary Materials: The following are available online at http://www.mdpi.com/2076-3263/9/8/354/s1, Supplemental file: Statement on provenance of Shenzianyuloma holotype. Video S1: fossil specimen and 3D model reconstruction. Acknowledgments: Thanks to Dianna L. Schulte McMenamin, Jon Tennant and three reviewers for assistance with this research. Conflicts of Interest: The author declares no conflict of interest.

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