Phylogenetic analysis reveals that Rhabdopleura is an extant graptolite CHARLES E. MITCHELL, MICHAEL J. MELCHIN, CHRIS B. CAMERON AND JO¨ RG MALETZ Mitchell, C.E., Melchin, M.J., Cameron, C.B. & Maletz, J. 2013: Phylogenetic analysis reveals that Rhabdopleura is an extant graptolite. Lethaia,Vol.46,pp.34–56. A phylogenetic analysis of morphological data from modern pterobranch hemichordates (Cephalodiscus, Rhabdopleura) and representatives of each of the major graptolite orders reveals that Rhabdopleura nests among the benthic, encrusting graptolite taxa as it shares all of the synapomorphies that unite the graptolites. Therefore, rhabdopleurids can be regarded as extant members of the Subclass Graptolithina (Class Pterobranchia). Com- bined with the results of previous molecular phylogenetic studies of extant deuterosto- mes, these results also suggest that the Graptolithina is a sister taxon to the Subclass Cephalodiscida. The Graptolithina, as an important component of Early–Middle Palaeo- zoic biotas, provide data critical to our understanding of early deuterostome phylogeny. This result allows one to infer the zooid morphology, mechanics of colony growth and palaeobiology of fossil graptolites in direct relation to the living members of the clade. The Subdivision Graptoloida (nom. transl.), which are all planktic graptolites, is well sup- ported in this analysis. In addition, we recognize the clade Eugraptolithina (nov.). This clade comprises the Graptoloida and all of the other common and well-known grapto- lites of the distinctive Palaeozoic fauna. Most of the graptolites traditionally regarded as tuboids and dendroids appear to be paraphyletic groups within the Eugraptolithina; however, Epigraptus is probably not a member of this clade. The Eugraptolithina appear to be derived from an encrusting, Rhabdopleura-like species, but the available informa- tion is insufficient to resolve the phylogeny of basal graptolites. The phylogenetic position of Mastigograptus and the status of the Dithecoidea and Mastigograptida also remain unresolved. h Biodiversity, Cambrian, Hemichordata, Deuterostomia, Ordovician. Charles E. Mitchell [[email protected]], Department of Geology, University at Buffalo- SUNY, Buffalo, NY 14260, USA; Michael J. Melchin [[email protected]], Department of Earth Sciences, St. Francis Xavier University, Antigonish, NS B2G 2W5, Canada; Chris B. Cameron [[email protected]], De´partement de sciences biologiques, Universite´ de Montre´al, Montre´al QC H2V 2S9, Canada; Jo¨rg Maletz [[email protected]], Institut fu¨r Geologische Wissenschaften, Freie Universita¨t Berlin, Malteserstr. 74-100, D-12249 Ber- lin, Germany; manuscript received on 8 ⁄ 12 ⁄ 11; manuscript accepted on 7 ⁄ 5 ⁄ 12. The small phylum Hemichordata plays a pivotal role Finally, we do not know the relationship among the in our efforts to understand the pattern of relation- tube-building groups: the graptolites and ptero- ships among the three major deuterostome taxa, the branchs. This latter question is the topic of our nature of the deuterostome ancestor and the evolu- study. tionary origin of the chordates (Fig. 1). Historically, Pterobranchs are colonial or pseudocolonial and hemichordates have been divided into four classes: reproduce via short-lived planula larvae and asexual the extant Enteropneusta (acorn worms), Planktosp- budding. They produce a collagenous dwelling struc- haeroidea and Pterobranchia and the extinct Grapto- ture that is commonly called a coenecium in the case lithina (Bulman 1970). The relationship among the of pterobranchs and a rhabdosome in the case of classes is highly uncertain, however, and this con- graptolites. For simplicity’s sake, we will use the term founds efforts to reconstruct deuterostome evolution. tubarium (Lankester 1884) for all of these communal It is not known whether the pterobranchs are a sister domiciles. The two major orders commonly assigned group to the enteropneusts (e.g. Winchell et al. 2002; to the Pterobranchia are the Cephalodiscida and the Cameron 2005) or derived within the enteropneust Rhabdopleurida. Both groups are relatively well clade (e.g. Cameron et al. 2000; Cannon et al. 2009). known from their living representatives, but have It is not known whether the monotypic Planktosp- yielded a fairly sparse fossil record (Rickards et al. haeroidea – rare, large, planktic larvae – represents a 1995). Graptolites, in contrast, have a relatively com- distinct clade of animals or are merely hypertrophied plete and rich fossil record of their skeletal details, tornaria larva of an enteropneust (Spengel 1932). whereas their soft-part anatomy is almost completely DOI 10.1111/j.1502-3931.2012.00319.x Ó 2012 The Authors, Lethaia Ó 2012 The Lethaia Foundation LETHAIA 46 (2013) Phylogeny of living and fossil graptolites 35 Fig. 1. Synthesis of recent molecular analyses of deuterostome phylogeny. Tree topology based on results presented in Winchell et al. (2002), Cameron (2005), Cannon et al. (2009), Delsuc et al. (2006) and Putnam et al. (2008). unknown except for a few poorly preserved remnants graptolites, graptolites were excluded from the Ptero- (Bjerreskov 1978, 1994; Rickards & Stait 1984; Loydell branchia. et al. 2004). In addition, the Middle to Late Cambrian On the other hand, Bulman’s (1970, p. V17) defini- fossil record of graptolites, which encompasses the tion of the Class Graptolithina is ‘The Graptolithina earliest part of their evolutionary history, is much less are colonial, marine organisms, which secreted a scler- complete than for the Ordovician or Silurian periods otized exoskeleton with characteristic growth bands when they became diverse and widespread (Rickards (fuselli) and growth lines. The thecae house individual & Durman 2006). This disparity in the available infor- zooids usually arranged in a single or double row mation for the various hemichordate groups has hin- along the branches (stipes) of the colony (rhabdo- dered a complete understanding of the phylogenetic some), rarely in irregular aggregates. In most orders, relationships between the living and extinct groups thethecaearepolymorphicandinthreetheyare and between different groups of graptolites. clearly related to an internal sclerotized stolon system. The goals of the present study are: (1) to test Rhabdosomes originate by a single bud from the ini- whether Pterobranchia and Graptolithina are mono- tial zooid, housed in a conical sicula, producing sim- phyletic groups and sister taxa as has commonly been ple, branched or rarely encrusting colonies.’ supposed; and, (2) in so doing, create a robust phylo- Cephalodiscid pterobranchs are clearly excluded genetic tree of the major tube-building hemichordate from the Graptolithina, based on this diagnosis, even taxa that can provide a foundation for further palaeo- taking into account recent evidence that their tubari- biological and macroevolutionary studies. um and its spine-like structures show a mode of con- struction similar to that inferred for graptolites (Dilly 1993). In contrast, the only respect in which the rhab- Previous phylogenetic interpretations dopleurid pterobranchs do not fit this diagnosis is in the description of the sicula as a conical structure. The The construction of the collagenous tubarium and bushy dendroid graptolites, however, possess a tubular asexually budded colonial zooids are synapomorphies prosicula (Fig. 2; Kozłowski 1949) and, moreover, of the Pterobranchia (Cameron 2005) and these fea- Epigraptus (and possibly the crustoids) possess a vesic- tures are shared with the graptolites, along with many ular prosicula very similar to that of Rhabdopleura details of the composition and fusellar mode of con- (Kozłowski 1971). struction of the tubarium (Andres 1977; Dilly 1993; Beklemishev (1951, 1970), in contrast, proposed Mierzejewski & Kulicki 2003). Despite these similari- that all of the pterobranchs and graptolites should be ties, Bulman (1970) regarded the Pterobranchia and united in a single Class Graptolithoidea, distinguished Graptolithina as distinct classes. His diagnosis of the by the presence of a sclerotized tubarium constructed Pterobranchia, which matches closely with most with fusellar increments that house a colony of zooids. widely used diagnoses for this group, notes that the This classification has been more recently employed members of the class are colonial (Rhabdopleura) or by Mierzejewski and Urbanek and their co-authors pseudocolonial (Cephalodiscus, where cloned individ- (e.g. Mierzejewski & Kulicki 2002; Mierzejewski & uals detach from one another as adult zooids) and Urbanek 2004; Urbanek 2004). Whereas this system- possess a shared cuticular tubarium, but otherwise atic approach acknowledges the common descent of focuses on the soft tissue anatomy of the organisms. the graptolites and pterobranchs within the Hemi- In the absence of details of the soft tissue structure of chordata, it significantly expands the concept of 36 Mitchell et al. LETHAIA 46 (2013) AB C G D EF Fig. 2. Sicular structure. Prosicula (ps) shaded and boundary with metasicula (ms) marked by x—x. A, B, crustoid? sicula with sac-like prosi- cula and raised primary aperture from which metasicula extended (A–E from Kozłowski 1971; material from Ordovician glacial boulders). C, Epigraptus sp., vesicular prosicula, secondary apertures for metasicula and (b) bitheca. D, Kozlowskitubus erraticus with vase-like prosicula, helical line in distal tubular part and tubular metasicula. E, Dendrograptus communis with entirely tubular prosicula