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And the Implications for the Vertebrate Fossil Decay of Vertebrate Downloaded from rspb.royalsocietypublishing.org on September 8, 2012 Decay of vertebrate characters in hagfish and lamprey (Cyclostomata) and the implications for the vertebrate fossil record Robert S. Sansom, Sarah E. Gabbott and Mark A. Purnell Proc. R. Soc. B 2011 278, 1150-1157 first published online 14 October 2010 doi: 10.1098/rspb.2010.1641 Supplementary data "Data Supplement" http://rspb.royalsocietypublishing.org/content/suppl/2010/10/14/rspb.2010.1641.DC1.h tml References This article cites 47 articles, 15 of which can be accessed free http://rspb.royalsocietypublishing.org/content/278/1709/1150.full.html#ref-list-1 Subject collections Articles on similar topics can be found in the following collections evolution (1278 articles) palaeontology (109 articles) taxonomy and systematics (149 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Proc. R. Soc. B go to: http://rspb.royalsocietypublishing.org/subscriptions Downloaded from rspb.royalsocietypublishing.org on September 8, 2012 Proc. R. Soc. B (2011) 278, 1150–1157 doi:10.1098/rspb.2010.1641 Published online 14 October 2010 Decay of vertebrate characters in hagfish and lamprey (Cyclostomata) and the implications for the vertebrate fossil record Robert S. Sansom, Sarah E. Gabbott* and Mark A. Purnell Department of Geology, University of Leicester, Leicester LE1 7RH, UK The timing and sequence of events underlying the origin and early evolution of vertebrates remains poorly understood. The palaeontological evidence should shed light on these issues, but difficulties in interpret- ation of the non-biomineralized fossil record make this problematic. Here we present an experimental analysis of decay of vertebrate characters based on the extant jawless vertebrates (Lampetra and Myxine). This provides a framework for the interpretation of the anatomy of soft-bodied fossil vertebrates and putative cyclostomes, and a context for reading the fossil record of non-biomineralized vertebrate characters. Decay results in transformation and non-random loss of characters. In both lamprey and hag- fish, different types of cartilage decay at different rates, resulting in taphonomic bias towards loss of ‘soft’ cartilages containing vertebrate-specific Col2a1 extracellular matrix proteins; phylogenetically informa- tive soft-tissue characters decay before more plesiomorphic characters. As such, synapomorphic decay bias, previously recognized in early chordates, is more pervasive, and needs to be taken into account when interpreting the anatomy of any non-biomineralized fossil vertebrate, such as Haikouichthys, Mayomyzon and Hardistiella. Keywords: experimental taphonomy; vertebrate; cyclostomes; decay bias; cartilage evolution 1. INTRODUCTION common ancestor is to be accurately reconstructed [9]. Nearly all vertebrate fossils preserve only biomineralized Furthermore, Early Cambrian fossils identified as ver- skeletal remains, but the comparatively rare specimens tebrates on the basis of non-biomineralized characters that preserve vertebrate soft-tissue characters are among [10–12] provide the best constraints on the minimum the most iconic fossils known. This is especially true of date of divergence of vertebrates from invertebrates, and remains from the early phase of vertebrate evolution, pre- deuterostomes from protostomes [13]. dating the widespread occurrence of phosphatic skeletal Clearly, the remains of non-biomineralized vertebrates tissues. Most vertebrate crown-group apomorphies are have considerable evolutionary significance. This signifi- soft-tissue, ultrastructural and embryological characters cance is entirely dependent upon correct phylogenetic [1,2]. Without fossil remains of early vertebrates and placement of the fossils, which is in turn contingent their soft tissues, we would remain ignorant of the upon robust interpretations of anatomical characters, timing and sequence of character acquisition through yet this is problematic. Although exceptional preservation the vertebrate stem, the base of the gnathostome stem of non-biomineralized animals, including vertebrates, and the cyclostome stem; we would have no temporal or provides evidence of fossil anatomies that would other- ecological context for early vertebrate evolution and the wise remain unknown, post-mortem decay means that assembly of the vertebrate body plan. These are landmark those anatomies are never preserved complete. Determin- events in the history of life that took place against a back- ing whether characters are absent from a fossil because drop of rapid molecular evolution and genome they decayed away or because they had yet to evolve is duplication [3,4]: testing the hypothesis of a causal therefore critical, yet difficult [14]. Decay, and in particu- relationship between increasing genomic and morpho- lar decay-induced collapse, also means that the shape logical complexity requires data from the fossil record and topological relations between characters can [5]. Recent work, for example, has identified the presence change, creating further difficulties for the recognition of two Col2A1 genes (expressed as type 2 collagen— of homologous anatomical characters, especially if Col2a1) in lampreys and hagfish as an important inno- diagenetic stabilization of recalcitrant organic remains vation in vertebrate skeletal development, possibly [15,16] occurs only after considerable decay. The com- linked to genome duplication [6–8]. This work also high- plex interplay of decay and fossilization represents a lighted the need to combine fossil evidence of cartilages in double-edged sword, acting both to enhance preservation early vertebrates with developmental data from extant through bacterial mediation of rapid authigenic mineraliz- homologues if skeletal development in the vertebrate ation, e.g. [17], and to remove and distort anatomical data through collapse and decomposition of morphologi- cal structures. * Author for correspondence ([email protected]). Understanding decay is therefore of paramount Electronic supplementary material is available at http://dx.doi.org/ importance to analysis of non-biomineralized fossils and 10.1098/rspb.2010.1641 or via http://rspb.royalsocietypublishing.org. their characters. Decay data can establish a time line, Received 30 July 2010 Accepted 21 September 2010 1150 This journal is q 2010 The Royal Society Downloaded from rspb.royalsocietypublishing.org on September 8, 2012 Decay of vertebrate characters R. S. Sansom et al. 1151 revealing: (i) characters that are lost so rapidly through decay that they are unlikely ever to become preserved, (ii) characters composed of relatively labile tissues that have the potential to be preserved through rapid authi- genic mineralization, and (iii) recalcitrant characters Myxinoidea Petromyzontida Gnathostomata that have the potential to persist in the geological record as diagenetically stabilized organic biomolecules. Previous Cyclostomata Vertebrata analyses of organismal decay have focused upon trans- Craniata (vertebrates formation of organisms as a whole in terms of general sensu lato) stages of decay [18–22], but we have developed a differ- ent approach: by focusing upon how and when each of the Urochordata phylogenetically informative morphological characters Cephalochordata Chordata (synapomorphies) of an organism decay, we are able to distinguish phylogenetic absence from taphonomic loss, Figure 1. Phylogeny of vertebrates and hierarchical character and recognize partially decayed characters [23]. This classifications. Dashed lines represent alternative resolutions technique, as applied to extant proxies for early chordates (cyclostome monophyly/paraphyly). (cephalochordate and larval lamprey), has revealed syna- pomorphic decay biases: plesiomorphic morphological ecological impact. Individuals were kept overnight in aerated characters were found to be significantly more decay water and transported live to Leicester. Atlantic hagfish resistant than the more phylogenetically informative char- (Myxine glutinosa, 48 individuals, 15–41 g) were collected acters diagnostic of particular chordate clades [23]. The in March 2009, using baited traps in the coastal waters early decay of diagnostic, synapomorphic characters can (depth 100–120 m) off West Sweden, near Tja¨rno¨ Marine result in their non-preservation, and this bias, if unrecog- Biological Laboratory. They were kept overnight in circulat- nized in fossils, will result in their incorrect phylogenetic ing sea water, euthanized in the morning and then placement on the stems of the crown groups to which transported, chilled, to Leicester in under 24 h. they truly belong, and thus distort our reading of the record. All experimental animals were euthanized using an over- Here, we present an experimental investigation of the dose of tricaine methanesulphonate (MS222; 2 mg ml21 decomposition of extant representatives of the jawless with buffer). Some previous studies of decay have used vertebrates, or cyclostomes (lamprey and hagfish). This asphyxia to kill animals, but MS222 treatment does not allows us to characterize the sequences of morphological adversely affect bacterial flora [33] and our previous results decay and loss of synapomorphies, and provide a frame- with Branchiostoma demonstrate that using MS222 has no work for interpretation of character preservation and effect on the patterns or rate of decay [19,23]. loss in non-biomineralized fossil
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