[Palaeontology, Vol. 60, Part 2, 2017, pp. 149–157] RAPID COMMUNICATION THE ‘TULLY MONSTER’ IS NOT A VERTEBRATE: CHARACTERS, CONVERGENCE AND TAPHONOMY IN PALAEOZOIC PROBLEMATIC ANIMALS by LAUREN SALLAN1 ,SAMGILES2,ROBERTS.SANSOM3,JOHNT. CLARKE1 , ZERINA JOHANSON4 ,IVANJ.SANSOM5 and PHILIPPE JANVIER6 1Department of Earth & Environmental Science, University of Pennsylvania, Philadelphia, PA USA; [email protected], [email protected] 2Department of Earth Sciences, Oxford University, Oxford, UK; [email protected] 3School of Earth & Environmental Sciences, University of Manchester, Manchester, UK; [email protected] 4Department of Earth Sciences, Natural History Museum, London, UK; [email protected] 5School of Geography, Earth & Environmental Sciences, University of Birmingham, Birmingham, UK; [email protected] 6CR2P, Museum national d’Histoire naturelle, Paris, France; [email protected] Typescript received 18 November 2016; accepted in revised form 19 January 2017 Abstract: The affinity of Tullimonstrum gregarium, a pin- identity and implies that convergence or deeper origins are cer-mouthed, soft bodied bilaterian, has been subject to responsible for vertebrate-like traits. Further, phylogenetic debate since its recovery from Carboniferous coal deposits at placement within vertebrates is only made possible by the Mazon Creek, Illinois. After decades of impasse focused on constraints of a chordate-only dataset with limited outgroups mollusc, arthropod and annelid attributes, two recent, yet and use of selective characters. Long-discussed alternative conflicting, high-profile studies concluded that the ‘Tully placements among molluscs (e.g. heteropod gastropods), Monster’ is a vertebrate, a relative of lampreys or jawed arthropods (e.g. anomalocarids) or elsewhere within non- fishes. Here, we find that structures described as supporting vertebrate deuterostomes are more congruent. Indeed, many vertebrate, and particularly crown vertebrate, affinity face of these lineages independently evolved vertebrate-like traits, significant challenges from biological, functional and tapho- including complex eyes and ‘teeth’. Thus, given the totality nomic perspectives. Problems with comparator choice, inter- of evidence, Tullimonstrum should be excluded from the ver- pretation of taphonomic processes at Mazon Creek and tebrate crown. Potential assignments for aberrant bilaterians, estimation of convergence within the bilaterian tree may common throughout the Palaeozoic fossil record, need to be have misled these recent studies, leading to conclusions considered in light of the number and likelihood of required which do not accommodate current understanding of the exceptions to established schemes. vertebrate record. For example, the absence of taphonomi- cally-expected synapomorphies in Tullimonstrum (e.g. otic Key words: Tullimonstrum, Mazon Creek, lamprey, Car- capsules, body pigment) calls into question vertebrate boniferous, taphonomy, vertebrates. TULLIMONSTRUM GREGARIUM Richardson, 1966 is a well- soft-tissue fossils with divergent morphology and a single known problematic bilaterian that only occurs in concre- documented occurrence in time (Donoghue & Purnell tions recovered from marine Essex fauna deposits within 2009), the affinity of Tullimonstrum was immediately sub- the Carboniferous Francis Creek Shale, most notably at ject to debate. It has been serially attributed to almost Mazon Creek, Illinois (307 Ma; Foster 1979; Shabica & every bilaterian group, including arthropods, molluscs Hay 1997; Sallan & Coates 2014). It is notable for its and ‘worms’ of all sorts (Richardson 1966; Johnson & combination of traits uncommon in fossil and living ani- Richardson 1969; Foster 1979; Beall 1991). Continuing mals, such as long-stalked eyes and an elongate proboscis uncertainty regarding Tullimonstrum’s classification has with a pincer-like mouth (Richardson 1966; Johnson & produced as much interest as the aberrant morphology at Richardson 1969; Foster 1979). Like so many Palaeozoic its source. © The Palaeontological Association doi: 10.1111/pala.12282 149 150 PALAEONTOLOGY, VOLUME 60 Despite thousands of specimens surveyed by dozens of camera-like eye; and (2) the presence of two organelles, workers over the decades, one major bilaterian clade was cylindrical and spheroid melanosomes, in the eye. These never linked to Tullimonstrum: Vertebrata. Vertebrates were taken as evidence for a multilayered retinal pig- were most likely excluded from consideration due to a mented epithelium (RPE), a vertebrate trait (although general absence of evident synapomorphies in Tullimon- presence of the RPE was marked as equivocal in their fig. strum, appearance of conflicting traits such as broad 4). With respect to the vertebrate nature of these charac- superficial segments, and gross dissimilarity with the ters, an alternative interpretation, based on three-dimen- coincident crown cyclostomes and gnathostomes (jawless sionally preserved specimens, is that the eyes are pigment and jawed fishes, respectively) that have well-preserved cup type (Johnson & Richardson 1969), which are far modern morphologies (e.g. Mayomyzon and Myxinikela; more phylogenetically widespread but not found among Gabbott et al. 2016). In fact, when a single twentieth cen- vertebrates (Clements et al. 2016). Second, the distribu- tury study discussed a potential connection with then- tion of pigment cell structures and melanin within the problematic conodonts, it was wholly in the context of a eye has not been well surveyed among other bilaterians, conodont–mollusc clade (Beall 1991). This relationship living or extinct (Lamb et al. 2007; Schoenemann et al. was summarily dismissed by the discoverers of the con- 2009; Clements et al. 2016). This suggests other occur- odont animal while making a case for conodont– rences are possible and limits the current utility of these vertebrate affinity (Aldridge et al. 1993). traits in placing Tullimonstrum. Presence of these two The recent announcements in Nature of a vertebrate melanosome types is variable even among vertebrates: the affinity for Tullimonstrum were therefore unexpected (Cle- RPE, along with the lens and iris, has been lost in extant ments et al. 2016; McCoy et al. 2016). Two simultaneous hagfish (Locket & Jørgensen 1998; Gabbott et al. 2016), studies came to this conclusion on the basis of novel, yet and only spheroid melanosomes are preserved in the eyes distinct, interpretations of previously observed features of the chondrichthyan Bandringa (Clements et al. 2016, (primarily eye pigments and axial structures respectively). extended data fig. 5l). No other vertebrate traits were However, these arguments for vertebrate attribution pre- identified by Clements et al. (2016), yielding two addi- sent major challenges in terms of taphonomy, morphology tional possibilities beyond vertebrate affinity: (1) cylindri- and parsimony, and furthermore contain major inconsis- cal melanosomes and/or the RPE evolved deeper within tencies. McCoy et al. (2016) used the presence of a ‘noto- deuterostomes with genetic prerequisites for RPEs (see chord’ to designate Tullimonstrum as a lamprey, yet noted below; Lamb et al. 2007); or (2) Tullimonstrum belongs that such internal elements are not preserved in definitive to an entirely different group of bilaterians and exhibits Mazon Creek vertebrates. Indeed, Clements et al. (2016) convergent eye structures (Foster 1979). Eye structures found no such structure, but described discrete layers of and characters exhibit high levels of homoplasy, conver- melanosomes in the eye as a vertebrate synapomorphy gence and parallel evolution (Ogura et al. 2004; Serb & (Bardack & Richardson 1977; Gabbott et al. 2016), while Eernisse 2008; Schoenemann et al. 2009; Clements et al. acknowledging the absence of other, expected characters. 2016). While independent gain of this structure (or its Here, we argue that a crown vertebrate, and in particu- loss in proximate crown vertebrate outgroups) may lar a lamprey, identity for Tullimonstrum is unlikely. For appear unparsimonious, this must be balanced against the example, the absence of taphonomically-expected verte- absence of expected vertebrate synapomorphies in Tul- brate synapomorphies in Tullimonstrum (e.g. otic cap- limonstrum, not to mention its incongruous body plan. sules, body pigment; Bardack & Richardson 1977; Janvier In contrast, McCoy et al. (2016) identified a host of 1996; Sallan & Coates 2014; Clements et al. 2016; Gabbott putative vertebrate traits in their description of Tullimon- et al. 2016; McCoy et al. 2016) suggests that convergence strum, which were used to support a lamprey designation. or deeper origins are responsible for vertebrate-like traits. This began with a ‘notochord’ represented by a mid-body Alternative, previously proposed, placements among mol- light-coloured stain or gap in segmentation (Johnson & luscs (e.g. heteropod gastropods; Johnson & Richardson Richardson 1969; Fig. 1A, ax). ‘Notochord’ identity was 1969; Foster 1979; Beall 1991), arthropods (e.g. Johnson assigned in Tullimonstrum only through comparison with & Richardson 1969; Foster 1979) or new attributions else- an indented band in Gilpichthys, a poorly-described puta- where within deuterostomes or chordates are more con- tive chordate mistakenly referred to as a stem-hagfish by gruent for the reasons laid out below. McCoy et al. (2016; see Sansom et al. 2010; Janvier 2015; Janvier & Sansom 2015; Gabbott et al. 2016; Fig. 2B). Notochords are unpreserved