Vol. XLII(4): 2010 THE FESTIVUS Page 43 SHELL MICROSTRUCTURES IN EARLY MOLLUSKS MICHAEL J. VENDRASCO1*, SUSANNAH M. PORTER1, ARTEM V. KOUCHINSKY2, GUOXIANG LI3, and CHRISTINE Z. FERNANDEZ4 1Institute for Crustal Studies, University of California, Santa Barbara, CA, 93106, USA 2Department of Palaeozoology, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden 3LPS, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, 39 East Beijing Road, Nanjing 210008, P.R. China, 414601 Madris Ave., Norwalk, CA 90650, USA Abstract: Shell microstructures in some of the oldest known mollusk fossils (from the early to middle Cambrian Period; 542 to 510 million years ago) are diverse, strong, and in some cases unusual. We herein review our recent work focused on different aspects of shell microstructures in Cambrian mollusks, briefly summarizing some of the major conclusions from a few of our recent publications and adding some new analysis. Overall, the data suggest that: (1) mollusks rapidly evolved disparate shell microstructures; (2) early mollusks had a complex shell with a different type of shell microstructure in the outer layer than in the inner one; (3) the modern molluscan biomineralization system, with precise control over crystal shapes and arrangements in a mantle cavity bounded by periostracum, was already in place during the Cambrian; (4) shell microstructure data provide a suite of characters useful in phylogenetic analyses of mollusks and mollusk-like Problematica, allowing better determination of the magnitude of disparity during the Cambrian as well as understanding of how the body plans of extant phyla were built through time; (5) calcitic semi-nacre, a type of shell microstructure characteristic of brachiopods and bryozoans, occurred in Cambrian mollusks, suggesting a deeper level of homology in the shells of these lophotrochozoan taxa; and (6) laminar shell microstructures, which are the strongest (most fracture resistant) but most energetically expensive and slowest to build, were common in Cambrian mollusks, suggesting predation was a powerful selective force at that time and providing additional evidence that the origin of mobile predators was a contributing cause of the Cambrian diversification event (Cambrian explosion) and the appearance of mineralized skeletons. Introduction lineages towards diverse defensive solutions. The evidence is limited but overall is consistent with this The rapid diversification of animals beginning hypothesis, including the following supporting around 542 million years ago was one of the most observations: (1) the earliest signs of predation occur at significant events in the history of life. This event, the base of the Cambrian or just before (Bengtson & known as the “Cambrian Explosion,” is characterized Zhao, 1992); (2) many different types of fossil evidence by the independent appearance and rapid diversification of predation have been recovered from Cambrian rocks, of shells in many animal lineages (Bengtson & Conway including predatory appendages on fossil arthropods Morris, 1992). The Cambrian explosion is the time (Whittington & Briggs, 1985), drill holes (Conway when most fossilizable phyla first appear in the fossil Morris & Bengtson, 1994), bite marks (Conway Morris, record and when most phyla first develop mineralized 1998), ingested prey preserved in the digestive tract of skeletons. Although there have been significant advances predators (Whittington, 1985), and healed shell scars over the past few decades in our understanding of this (Skovsted et al., 2007); and (3) shells, thought by many interval, we are far from knowing the causes of the to be primarily a tool of defense (Vermeij, 1987), event or its detailed pattern. appeared in many different animal lineages during the One of the more prominent hypotheses about the Cambrian explosion (Bengtson & Conway Morris, Cambrian explosion is that it was caused by the onset of 1992) and were made of diverse components and had predation, which likely drove adaptation in various different microstructures (Bengtson & Conway Morris, *Corresponding author: 14601 Madris Ave., Norwalk, CA 90650, USA. E-mail: [email protected] Page 44 THE FESTIVUS Vol. XLII(4): 2010 1992), and so likely evolved independently in many of these are likely members of extinct phyla, as Gould clades. Nevertheless, in spite of this preliminary suggested, many of these still problematic fossils are support, the hypothesis that predation was a major probably members of a stem lineage of an extant driving force of the Cambrian explosion is still disputed. phylum, and as such are critical in understanding the The Cambrian Period is also characterized by many early evolution of animal morphology (cf. Budd, 2003). problematic taxa (“Problematica” or “Incertae sedis”, The body plans of extant phyla were built in a piecemeal class uncertain) that cannot easily be classified into manner through time, and understanding which fossils modern groups of animals. Gould (1989) emphasized are members of which extinct stem lineages can help us such taxa in his popular book Wonderful Life: The understand how the body plans of extant taxa originated Burgess Shale and the Nature of History, wherein he (Figure 1). Moreover, understanding which of these inferred much higher morphological disparity (i.e., fossils are not members of stem lineages of extant phyla many more phyla, more basic anatomical designs) of will help us better assess the extent of phylum-level animals in the Cambrian than later in Earth history. By disparity in the Cambrian, allowing improved testing of this logic, many of the problematic fossils in the Gould’s (1989) hypothesis of higher Cambrian disparity. Cambrian are members of phyla that went extinct by the end of the Cambrian. The title of the book was a reference to the 1946 movie, It's a Wonderful Life, because Gould (1989) envisioned contingency in the history of life: by his reasoning, if you re-ran the tape of life (i.e., a “do over” in schoolyard speech), different groups of animals would go extinct during the Cambrian, and our planet would have a very different fauna, with perhaps no vertebrates and probably no humans. Conway Morris (1998) strongly objected to Gould’s reasoning, pointing out the commonality of convergent evolution throughout the history of life and suggesting that lineages will be pulled towards certain forms by natural selection. Convergent evolution is the phenomenon where distantly related lineages independently evolve similarities in form as a result of adaptation to similar environments (e.g. torpedo shape with fins in dolphins, sharks, and ichthyosaurs — an extinct group of reptiles). Gould (2001) was unconvinced by Conway Morris’ argument, seeing no inevitability in evolution or the survival of vertebrates or humans, and maintained his opinion on contingency. Meanwhile, Gould’s (1989, 2001) claim of higher disparity during the Cambrian was disputed by researchers who used multivariate morphospace analyses Figure 1. The character states that define the crown group of a taxon to try to quantify disparity in arthropods and priapulids, are likely to have arisen in a piecemeal manner. The crown group is defined as the last common ancestor of all living members of a taxon noting that disparity by these measures was about the of interest (e.g., Mollusca) and all of its descendants. The stem same in the Cambrian as today (Wills, 2001). lineage is comprised of any taxa outside the crown group that are However, Gould (1989) emphasized disparity among, more closely related to the crown group than they are to the most not within, phyla, so it is unclear to what extent the proximal extant outgroup (i.e., the sister group). The basal taxa of a stem lineage would therefore be expected to share only some of the results reported by Wills (2001) bear on Gould’s characters uniting the crown group. They would lack any hypothesis. apomorphies (derived character states) arising in any members more Since the publication of Gould’s Wonderful Life, a closely related to the crown group. (Diagram modified from Budd, number of previously problematic fossils have been 1998.) assigned to the stem lineages (Figure 1) of modern phyla, although numerous fossils from the earliest Mollusks occur in many of the early animal fossil assemblages of animals remain problematic. While some assemblages and clearly began to diversify in the early Vol. XLII(4): 2010 THE FESTIVUS Page 45 Cambrian. Most of the earliest (early Cambrian) shelled shell microstructure (the shape and arrangement of mollusks were univalves with slight coiling but some mineral crystals in the shell) in sub-micrometer detail. had shells with greater coiling and others were bivalves Runnegar showed that coatings on the inner shell surface (Figure 2). The relationships among these earliest of secondary calcium phosphate – probably precipitated mollusks remain controversial because there are so few as a result of bacterial decay shortly after the death of characters that are well known from their fossil shells. the animal (Lucas & Prévôt, 1991) – could preserve Pioneering work by Bruce Runnegar (1985) revealed imprints of shell microstructures in both inner and outer that phosphatic molds of Cambrian mollusks (internal or shell layers (Figure 3). The nature of the shell external coatings of the shell) preserve details of their microstructure contributes to the beauty and strength of Figure 2. Some Cambrian mollusks (1-8) and a mollusk-like problematic