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2010 Annual Science Report

Massachusetts Institute of Technology Reporting  |  SEP 2009 – AUG 2010

Paleontological Investigations of the Advent and Maintenance of Multicellular Life

Project Summary

This years research has targeted several areas associated with the origin and early diversification of multicellular life. Team member Knoll and colleagues (Harvard) have investigated the molecular basis of complex multicellularity, which developed in a variety of different groups. They have also continued work on the evolution of biomineralization in early eukaryotes. Team member Erwin has continued work on the evolution of developmental gene regulatory networks in early metazoans and, with Jim Valentine (UC Berkeley) completed the manuscript on the Ediacaran-Cambrian diversification of animals.

4 Institutions
3 Teams
15 Publications
0 Field Sites
Field Sites

Project Progress

Paleontological investigations of the advent and maintenance of multicellular life

Team member Knoll completed a longstanding investigation on the comparative biology and paleobiology of complex multicellularity. Simple multicellularity has evolved numerous times within the Eukarya, but complex multicellular organisms belong to only six clades: animals, embryophytic land plants, florideophyte red algae, laminarialean brown algae, and two groups of fungi. Phylogeny and genomics suggest a generalized trajectory for the evolution of complex multicellularity, beginning with the cooptation of existing genes for adhesion. Molecular channels to facilitate cell-cell transfer of nutrients and signaling molecules appear to be critical, as this trait occurs in all complex multicellular organisms but few others. Proliferation of gene families for transcription factors and cell signals accompany the key functional innovation of complex multicellular clades: differentiation cells and tissues for the bulk transport of oxygen, nutrients and molecular signals, thereby circumventing the physical limitations of diffusion. The fossil records of animals and plants document key stages of this trajectory (Knoll, 2010; see also Knoll and Hewitt, 2010, a preliminary study finally published this year).

Caltech postdoctoral fellow Jonathan Wilson and team member Andrew Knoll also published a morphometric analysis of water transport cells within vascular plants, the largest biomass of complex multicellular organisms on Earth. Previous work showed that cell length, diameter, and pit resistance govern the hydraulic resistance of individual conducting cells; thus, Wilson and Knoll were able to use these three parameters as axes for a physiologically explicit morphospace analysis, showing that early seed plants evolved a structural and functional diversity of xylem architectures broader, in some ways, than the range observable in living plants (Wilson and Knoll, 2010).

Team member Knoll also completed two papers on biomineralization by eukaryotic organisms. In one, Knoll and Caltech colleague W.W. Fischer argued that the comings and goings of reef builders and other hypercalcifying organisms in marine environments reflect changes in the saturation level of surface seawater with respect to calcite and aragonite, as modulated by deep ocean redox character. This research is directly relevant to current research on ocean acidification and its biological consequences (Knoll and Fischer, 2010). Knoll and John Raven also completed a study of non-skeletal biomineralization in eukaryotes. Non-skeletal biomineralization by eukaryotic cells, with precipitates retained within the cell interior, can duplicate some of the functions of skeletal minerals, e.g. increased cell density, but not the mechanical and antibiophage functions of extracellular biominerals. However, skeletal biomineralisation does not duplicate many of the functions of non-skeletal biominerals. These functions include magnetotaxis (magnetite), gravity sensing (intracellular barite, bassanite, celestite and gypsum), buffering and storage of elements in an osmotically inactive form (calcium as carbonate, oxalate polyphosphate and sulfate; phosphate as polyphosphate) and acid-base regulation, disposing of excess hydroxyl ions via an osmotically inactive product (calcium carbonate, calcium oxalate) (Raven and Knoll, 2010). In other research, Knoll and Italian colleagues S. Ratti and M. Giordano reported the results of physiological experiments designed to test the hypothesis that seawater sulfate levels have influenced the composition of primary producers in the oceans through time (Ratti et al., in prep.). Finally, Phoebe Cohen, a Harvard graduate student supported by NAI completed her Ph.D. dissertation. Among other things, Dr. Cohen discovered a remarkable new record of eukaryotic microfossils, dramatically increasing the known diversity of protists in later Neoproterozoic oceans (Cohen 2010).

Team member Doug Erwin, in collaboration with Eric Davidson (Cal Tech) continued work on the evolution of metazoan developmental gene regulatory networks (GRNs), based on empirical studies from Davidson’s lab, and on a synthesis of studies on a variety of organisms. One paper examines the evolutionary implications of the fact that changes in transcription factors are haplosufficient. This allows much more rapid evolution of GRNs than would be possible if the mutations had to go to fixation, particularly in marine organisms that produce many larvae. The prediction from this is that rates of certain types of regulatory mutations should be much higher than in other regulatory mutations, or in mutations of structural genes. In a review paper on early eumetazoan evolution, Davidson and Erwin examined the patterns of genetic regulatory and developmental changes associated with the early stages of eumetazoan evolution. In this paper they reconstruct pre-eumetazoan network organization and consider the process by which the eumetazoan regulatory apparatus might have been assembled. A strong conclusion is that the evolutionary process generating the genomic programs responsible for developmental formulation of basic eumetazoan body plans was in many ways very different from the evolutionary changes that can be observed at the species level in modern animals.

Team member Erwin has also completed a book with Jim Valentine (UC Berkeley) on the Ediacaran-Cambrian diversification of animals. This book, to be published in June 2011, reviews and synthesizes current understanding of the geological context, phylogenetic relationships, fossil record, paleoecology, and comparative developmental biology of this major evolutionary event. Erwin and Valentine argue that this event reflected a complex set of causes, with an important role for the modification of the environment by early metazoans, generating a positive feedback process that bootstrapped biodiversity.