Cells Tissues Organs Published online: May 27, 2011 DOI: 10.1159/000324245 Evolutionary Origins of Animal Skeletal Biomineralization Duncan J.E. Murdock Philip C.J. Donoghue School of Earth Sciences, University of Bristol, Wills Memorial Building, Queen’s Road, Bristol , UK Key Words Introduction Biomineralization ؒ Animal skeleton ؒ Evolution ؒ Fossil record ؒ Cambrian explosion Biomineralogy has long been the focus of materials scientists, chemists and palaeontologists, but it has only recently captured the interest of developmental biologists Abstract [Wilt, 2005] who in short order have begun to address The evolutionary history of biomineralization in animals is some of the fundamental questions in biomineralogy. crucial to our understanding of modern mineralized tissues. Foremost is the question of whether disparate animal lin- Traditional methods of unravelling this history have aimed to eages evolved their mineralized skeletons independently derive a theory of the development of biomineralization or the ability to develop a mineralized skeleton is inher- through evolution by the comparison of mineralized systems ited from a common ancestor. The prospect of a skeleton- in model organisms. This has led to the recognition of the ized universal ancestor of animals has been revived in ‘biomineralization toolkit’ and raised the question of the ho- light of the discovery that orthologous genes and their mology of mineralized tissues versus convergent or parallel encoded proteins are implicated in skeletal development evolution. The ‘new animal phylogeny’ reveals that many of in organisms as diverse as vertebrates, echinoderms, the groups known to biomineralize sit among close relatives molluscs and sponges [Ettensohn et al., 2003; Livingston that do not, and it favours an interpretation of convergent or et al., 2006; Jackson et al., 2007]. Whether this ‘biomin- parallel evolution for biomineralization in animals. In addi- eralization toolkit’ of genes reflects a parallel co-option tion, the fossil record of the earliest mineralized skeletons of a common suite of genes or the inheritance of a skeleto- presents a rapid proliferation of biomineralization across a genic gene regulatory network from a biomineralizing range of animal phyla with fossil representatives of many common ancestor remains an open debate [Livingston et modern biomineralizing phyla. A synthesis of molecular, de- al., 2006; Jackson et al., 2007]. Reconciling these conflict- velopmental, phylogenetic and fossil evidence demonstrates ing interpretations of the data requires knowledge of the the convergent or parallel evolution of biomineralization in phylogenetic distribution of the molecular and skeletal animals at the phylum level. The fossil record of the Cambrian characters in question. These have changed significantly explosion not only provides vital evidence for the evolution in recent years in light of molecular phylogenetics, which of animal mineralized tissues but also suggests a mechanism has radically changed our understanding of the evolu- for its rapid and synchronous convergent origin. tionary relationships among animal phyla. Copyright © 2011 S. Karger AG, Basel © 2011 S. Karger AG, Basel Mr. Duncan J.E. Murdock 1422–6405/11/0000–0000$38.00/0 School of Earth Sciences, University of Bristol Fax +41 61 306 12 34 Wills Memorial Building, Queen’s Road E-Mail [email protected] Accessible online at: Bristol BS8 1RJ (UK) www.karger.com www.karger.com/cto Tel. +44 117 954 5400, E-Mail duncan.murdock @ bristol.ac.uk Biomineralization and the ‘New Animal Phylogeny’ marginally favoured, but this is too simplistic. Rather it has been suggested that, at least between calcium carbon- Mineralized skeletons are found in all of the major divi- ate polymorphs, once a lineage has adapted to using a sions of the animal tree in an astounding range of grades particular system, changes are rare [Porter, 2010]. Mo- of organization, body plan and function. Outside of the lecular dissection of biomineralization indicates other- context of evolutionary history the interpretations of rela- wise: orthologous genes have been co-opted and diversi- tionships between these structures can be misleading. It is fied in parallel among vertebrates and echinoderms [Liv- therefore prudent to examine the phylogenetic context of ingston et al., 2006], molluscs [Jackson et al., 2010] and animal skeletons. The ‘new animal phylogeny’ reveals that bilaterians [Jackson et al., 2010]. many of the groups known to biomineralize are interca- However, since mineralized skeletons of extant organ- lated among relatives that do not. An exemplar case study isms, and the molecular machinery involved in producing is the change in our understanding of deuterostome phy- them, have undergone a significant amount of evolution- logeny. The traditional synthesis resolved deuterostomes ary change since their divergences, they may not be rep- as a clade rich in animals that biomineralize, with several resentative of the ancestral condition. It is therefore neces- candidates for the invertebrate non-chordate origin of the sary to utilize the evidence of the earliest animal skeletons vertebrate skeleton and the assumption that the range of afforded to us by the fossil record, representing a condi- skeletal systems exhibited was derived from a common tion much closer to the deep divergences of animals. biomineralizing ancestor [Moss, 1964]. However, the lophophorate phyla (brachiopods, phoronids and bryozoa) are united with molluscs, annelids and their allies to form Lessons from the Fossil Record the Lophotrochozoa in the modern synthesis, whilst the chaetognaths and nemerteans are allied with the other ma- The preservation potential of mineralized tissues is rel- jor division of protostomes, i.e. Ecdysozoa. The remaining atively good; therefore, were the latest common ancestor mineralized clades, the calcareous Echinodermata and of extant mineralized groups to have been biomineraliz- jawed vertebrates which possess apatite skeletons, have di- ing, we might expect to see remains of these structures in vergences intercalated by the jawless vertebrates, cephalo- the fossil record. By contrast, multiple origins for biomin- chordates, tunicates and hemichordates, all of which prim- eralizing animals would produce a different record, with itively lack skeletal tissues. The primitive vertebrate skel- the fossilized remains of animal skeletons appearing after eton originated as a cartilaginous endoskeleton associated the divergence of their respective groups. The earliest re- with the pharynx, which is known to have mineralized in cord of animal skeletons are the calcareous fossils of the an extinct group of jawless fish (the conodonts) as part of 660-Ma Trezona Formation [Maloof et al., 2010] followed, an oropharyngeal feeding apparatus [Donoghue and San- in the latest Ediacaran period, by the weakly mineralized som, 2002]. The first true mineralized vertebrate skeletons Cloudina ( fig. 3 b), Namacalathus and similar forms evolved in ostracoderms, a group of stem gnathostomes, as [Grotzinger et al., 2000], which have been allied with var- a dermal skeleton independently of the echinoderm skel- ious cnidarian, poriferan and annelid groups. In the Ear- eton [Donoghue and Sansom, 2002]. ly Cambrian the diversity and abundance of shelly fossils If we examine the distribution of biominerals across a dramatically increased, and the fossil record was domi- modern phylum level tree of animals ( fig. 1 ), although nated by the ‘small shelly faunas’ until the end of the Mid- silica as a biomineral is restricted to silica sponges, cal- dle Cambrian [Porter, 2004]. Amongst these are stem (a careous and phosphatic biomineralization occur in all of sister relative outside the living clade) or crown (a clade of the major divisions of the tree. At the simplest level, two living members of a group and all descendants of their competing hypotheses to explain this distribution can common ancestor) representatives of all the modern bio- be erected: either mineralized animal skeletons evolved mineralizing animal phyla, and many orders, as well as once or independently in each case. A strict parsimony many taxa whose biological affinity within the animal approach cannot distinguish between these hypotheses: tree is yet to be constrained [Bengtson, 2005]. This rapid either a single origin with 13 losses (or changes in min- proliferation of fossil diversity, i.e. the Cambrian explo- eral system) or 14 independent gains. If changes between sion, is one of the most intriguing problems in palaeontol- mineral systems (i.e. between calcium carbonate and ogy, and the nature of this record is hotly debated [Run- phosphate) can be achieved with relative ‘ease’ on the negar, 1982]. Is it an explosion of animal diversity or the grounds that the same biochemical machinery can be co- explosion in fossil diversity expected in the parallel evolu- opted into either role [Knoll, 2003], then a single origin is tion of biomineralized animal skeletons? 2 Cells Tissues Organs Murdock/Donoghue Fig. 1. Distribution of biomineralization Acoela Myzostimida Annelida Gastroticha Gnathostomulida Brachiopoda Tardigrada Calcarea Chaetognatha Onychophora Nemertea Bryozoa Arthropoda Nematoda Cnidaria Chordata Platyhelminthes Choanoflagellates Silica sponges Mollusca Hemichordata Echinodermata Xenoturbella Nematomorpha Priapulida Rotifera Phoronida across a phylum level animal tree. Termi- Kinorhyncha nal branches are coded to reflect known fossil or extant representatives