Final Report Summary - MOLLUSC EVOLUTION (Changes in mollusc shell microstructure through time)
This project on molluscan evolution has helped to fill a large gap in our understanding of the early history of the mollusc shell and its relationship to the evolutionary improvements of early oceanic predators. In the course of this project we have discovered and provided exceptionally detailed photographs via scanning electron microscopy (SEM) of more than fifty new cases of remarkably preserved molluscs, some of which are among the oldest known representatives of the Mollusca (from the early Cambrian Period; ~540 million years ago). We also developed a Microsoft ACCESS database of shell microstructures in Paleozoic molluscs in order to better discern spatial and temporal patterns of features of the mollusc shell. In this way we have tested hypotheses about the controls over biomineralization in the early molluscs, for example whether predation or seawater chemistry exerted greater control on the nature and organization of minerals within the shell.
Our new data have revealed that most early and middle Cambrian molluscs appear to have had extensive calcite in their shell, in contrast to modern forms where aragonite is much more common. This pattern reflects the fact that these particular fossil species lived during a time of 'calcite seas' wherein this mineral was favored over aragonite. This correlation is consistent with the hypothesis that seawater chemistry exerted strong influence on the mineral used in constructing the earliest mollusc shells. Cambrian molluscs also tended to have thicker organic components to the shell and thus had a much more flexible shell than most modern molluscs. This may have been because predators at this time lacked hard claws or jaws.
Our work on fossils from the subsequent period, the Ordovician (~450 million years ago), reveals that molluscs by this time had shells with relatively thicker mineral layers. In addition, numerous lineages had the strong but energetically expensive shell microstructure nacre. The predominance of nacre in the Ordovician, and its rare or non-existent occurrence in the Cambrian, is consistent with the hypothesis that mollusc shell strength increased during the Great Ordovician Biodiversification Event as the intensity of predation magnified. A great number of evolutionary innovations in efficiency of predation occurred during the Ordovician as, for example, claws and jaws became stronger and harder, and shell drilling ability improved. The Ordovician also saw a dramatic increase in mobile, efficient predators such as cephalopods and echinoderms.
Our research has also shown that the mollusc shell became essentially modern by the time of the middle to late Paleozoic Era. Exceptionally preserved molluscs from the Pennsylvanian Buckhorn Asphalt (Pennsylvanian; ~310 million years ago) reveal that some lineages of molluscs by this time had thick layers of crossed-lamellar microstructure whereas other groups had extensive nacre. Some species even had a combination of both of these shell microstructures, the two strongest varieties known in invertebrate animals. Thus our data reveal a stepwise increase in the defensive ability of the mollusc shell from the Cambrian to Ordovician and the Ordovician to Carboniferous. Although the mollusc shells of the Mesozoic Era (during the time of numerous, large shell crushing reptiles, fish, and cephalopods) are most famous, our work has shown that by the Carboniferous most mollusc lineages already had strong shell microstructures, giving molluscs a head-start in the acceleration of the evolutionary arms race during the subsequent Mesozoic Era. In addition to high resolution SEM that revealed even ultrastructures within the basic units of shell microstructure (e.g. textures within nacre tablets), we also employed atomic force microscopy to document that the organic inclusions within the nacre still remain even after hundreds of millions of years. This is the oldest known occurrence of such organic inclusions within the shell microstructure of molluscs. We were also successful in characterizing the original crystallographic orientation of the original micro-components of the shell using Electron Backscatter Diffraction (EBSD). We got good data on cephalopods, bivalves, and gastropods in the assemblage, allowing for a detailed comparison of nacre in ancient molluscs. Our work has shown that the Buckhorn Asphalt represents the best preservation of mollusc shell microstructures from the entire Paleozoic Era (~540-250 million years ago).
The detailed preservation of nacre in the Ordovician fossils as imprints in ultra-fine grain calcium phosphate as well as the preservation of original nacre in Carboniferous fossils both allow for a detailed comparison of nacre in the different mollusc groups that had it: gastropods, cephalopods, bivalves, and monoplacophorans. Such comparisons can help test the hypothesis that nacre originated independently in the different groups of molluscs, an idea that contrasts with historical dogma. Our results show clear differences among the molluscs both in the Ordovician as well as Carboniferous. As with modern forms bivalve nacre is distinct from that of gastropods. Cephalopod nacre is more reminiscent to that of gastropods but also is unique in some ways, and monoplacophoran nacre seems intermediate between gastropod and bivalve nacre. In addition monoplacophorans and gastropods from the Ordovician show unusual aragonite tablet growths that are less ordered than in modern nacre. These may be precursors to true nacre. In any case the historical distinctiveness of nacre in the Mollusca is consistent with the hypothesis that nacre originated 3 or 4 times independently in the phylum. This provides even more evidence that increasing predation during the Cambrian-Ordovician must have been influencing the construction of the mollusc shell.
In addition to our work on fossil molluscs, we also examined modern chitons in order to determine the similarity in biomineralization mechanisms between chitons and other molluscs. This work can begin to help resolve the question of whether the shell of chitons is homologous to that of bivalves, gastropods, and other molluscs. The semi-thin sections we made of chitons and transmission electron microscopy (TEM) reveal that the periostracal groove is on the ventral side of the animal, not dorsal as previously believed. Moreover, the fine morphology and mode of formation of the chiton periostracum is quite similar to that of other molluscs (in particular bivalves), but the chiton periostracum also differs from that of bivalves in some key ways. We have also seen that the scales and spines of chitons are remarkably diverse in fine morphology and method of formation. Chitons are often viewed as 'primitive' molluscs, but the biomineralization mechanisms occurring in the girdle that encircles their shell plates are complex and varied.
We have shared the information resulting from this project at 7 international conferences (in the UK, Estonia, Spain, and Switzerland), during an invited talk at the Swedish Museum of Natural History, and during the Andalucía Day of Science. We have two publications finalized and four more are in various stages of preparation that should be published within the next year or so. Once these papers are 'in print' we will make available to the public our Microsoft ACCESS database on Paleozoic shell microstructures. This will allow other researchers to develop and test new hypotheses related to the controls and evolution within the shell of various lineages of ancient mollusc.
Our new data have revealed that most early and middle Cambrian molluscs appear to have had extensive calcite in their shell, in contrast to modern forms where aragonite is much more common. This pattern reflects the fact that these particular fossil species lived during a time of 'calcite seas' wherein this mineral was favored over aragonite. This correlation is consistent with the hypothesis that seawater chemistry exerted strong influence on the mineral used in constructing the earliest mollusc shells. Cambrian molluscs also tended to have thicker organic components to the shell and thus had a much more flexible shell than most modern molluscs. This may have been because predators at this time lacked hard claws or jaws.
Our work on fossils from the subsequent period, the Ordovician (~450 million years ago), reveals that molluscs by this time had shells with relatively thicker mineral layers. In addition, numerous lineages had the strong but energetically expensive shell microstructure nacre. The predominance of nacre in the Ordovician, and its rare or non-existent occurrence in the Cambrian, is consistent with the hypothesis that mollusc shell strength increased during the Great Ordovician Biodiversification Event as the intensity of predation magnified. A great number of evolutionary innovations in efficiency of predation occurred during the Ordovician as, for example, claws and jaws became stronger and harder, and shell drilling ability improved. The Ordovician also saw a dramatic increase in mobile, efficient predators such as cephalopods and echinoderms.
Our research has also shown that the mollusc shell became essentially modern by the time of the middle to late Paleozoic Era. Exceptionally preserved molluscs from the Pennsylvanian Buckhorn Asphalt (Pennsylvanian; ~310 million years ago) reveal that some lineages of molluscs by this time had thick layers of crossed-lamellar microstructure whereas other groups had extensive nacre. Some species even had a combination of both of these shell microstructures, the two strongest varieties known in invertebrate animals. Thus our data reveal a stepwise increase in the defensive ability of the mollusc shell from the Cambrian to Ordovician and the Ordovician to Carboniferous. Although the mollusc shells of the Mesozoic Era (during the time of numerous, large shell crushing reptiles, fish, and cephalopods) are most famous, our work has shown that by the Carboniferous most mollusc lineages already had strong shell microstructures, giving molluscs a head-start in the acceleration of the evolutionary arms race during the subsequent Mesozoic Era. In addition to high resolution SEM that revealed even ultrastructures within the basic units of shell microstructure (e.g. textures within nacre tablets), we also employed atomic force microscopy to document that the organic inclusions within the nacre still remain even after hundreds of millions of years. This is the oldest known occurrence of such organic inclusions within the shell microstructure of molluscs. We were also successful in characterizing the original crystallographic orientation of the original micro-components of the shell using Electron Backscatter Diffraction (EBSD). We got good data on cephalopods, bivalves, and gastropods in the assemblage, allowing for a detailed comparison of nacre in ancient molluscs. Our work has shown that the Buckhorn Asphalt represents the best preservation of mollusc shell microstructures from the entire Paleozoic Era (~540-250 million years ago).
The detailed preservation of nacre in the Ordovician fossils as imprints in ultra-fine grain calcium phosphate as well as the preservation of original nacre in Carboniferous fossils both allow for a detailed comparison of nacre in the different mollusc groups that had it: gastropods, cephalopods, bivalves, and monoplacophorans. Such comparisons can help test the hypothesis that nacre originated independently in the different groups of molluscs, an idea that contrasts with historical dogma. Our results show clear differences among the molluscs both in the Ordovician as well as Carboniferous. As with modern forms bivalve nacre is distinct from that of gastropods. Cephalopod nacre is more reminiscent to that of gastropods but also is unique in some ways, and monoplacophoran nacre seems intermediate between gastropod and bivalve nacre. In addition monoplacophorans and gastropods from the Ordovician show unusual aragonite tablet growths that are less ordered than in modern nacre. These may be precursors to true nacre. In any case the historical distinctiveness of nacre in the Mollusca is consistent with the hypothesis that nacre originated 3 or 4 times independently in the phylum. This provides even more evidence that increasing predation during the Cambrian-Ordovician must have been influencing the construction of the mollusc shell.
In addition to our work on fossil molluscs, we also examined modern chitons in order to determine the similarity in biomineralization mechanisms between chitons and other molluscs. This work can begin to help resolve the question of whether the shell of chitons is homologous to that of bivalves, gastropods, and other molluscs. The semi-thin sections we made of chitons and transmission electron microscopy (TEM) reveal that the periostracal groove is on the ventral side of the animal, not dorsal as previously believed. Moreover, the fine morphology and mode of formation of the chiton periostracum is quite similar to that of other molluscs (in particular bivalves), but the chiton periostracum also differs from that of bivalves in some key ways. We have also seen that the scales and spines of chitons are remarkably diverse in fine morphology and method of formation. Chitons are often viewed as 'primitive' molluscs, but the biomineralization mechanisms occurring in the girdle that encircles their shell plates are complex and varied.
We have shared the information resulting from this project at 7 international conferences (in the UK, Estonia, Spain, and Switzerland), during an invited talk at the Swedish Museum of Natural History, and during the Andalucía Day of Science. We have two publications finalized and four more are in various stages of preparation that should be published within the next year or so. Once these papers are 'in print' we will make available to the public our Microsoft ACCESS database on Paleozoic shell microstructures. This will allow other researchers to develop and test new hypotheses related to the controls and evolution within the shell of various lineages of ancient mollusc.