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Frontiers in Evolutionary Biology REPORT OF A WORKSHOP PREPARED FOR THE NATIONAL SCIENCE FOUNDATION March 2005 Table of contents Introduction ........................................................................................1 Emerging tools ..................................................................................1 Research themes ...............................................................................2 The evolution of genome structure and function ......................3 Genetics/evolution of adaptation ................................................3 Population divergence and speciation .......................................4 Microevolution of development ...................................................4 Evolution of integrated phenotypes ...........................................5 Microbial systems .........................................................................6 Evolution of conflict and cooperation ........................................6 Large-scale patterns of diversity in time and space .................7 Applied evolution ..........................................................................7 Institutional resources ......................................................................8 Infrastructural needs and opportunities .........................................9 Appendix: Workshop participants .................................................10 INTRODUCTION frontiers of evolutionary research in the coming Support for ecological and evolutionary research decade. As a result, the themes for future at the National Science Foundation expanded research outlined here reflect both new questions substantially during the past decade. To help and new conceptual frameworks, as well as the guide this expansion, in October 1998 the application of new tools to classic questions in Population Biology program at NSF hosted a evolutionary biology. workshop on “Frontiers in Population Biology”. The workshop had four specific goals: The report from that workshop identified and 1) To identify emerging tools essential to illustrated seven research themes of special evolutionary research; interest in population biology, and described how 2) To identify and illustrate research these themes connect to genetics/genomics on themes of particular promise; the one hand and to environmental issues on the 3) To summarize major institutional other. The report has been valuable to officers at resources available to support NSF in shaping their programs and balancing evolutionary research; their grant portfolios. 4) To suggest infrastructural needs and Our understanding of evolutionary biology opportunities for enabling the next has advanced enormously in the past six years. generation of advances in our understanding The explosion of genomic information, rapid of evolution. advances in computer and sensor technology, and the development of sophisticated new statistical and analytical approaches coupled with the EMERGING TOOLS recent reorganization of programs at NSF make Many research frontiers identified in this report this an appropriate time to evaluate progress and are now accessible only because of recent, to identify areas in which new investment is explosive advances in technology, while others warranted. In January 2005 a panel of experts lie at the fringe of current technology. A shared met at NSF to identify areas that represent the feature of many of these advances is the scale at frontiers for evolutionary research in the coming which they are conducted. We can now sequence decade. The scope of this workshop was whole genomes, analyze expression of all genes, somewhat larger than that considered at the 1998 and analyze data with desktop supercomputers. It workshop, reflecting the range of evolutionary is clear that advances in phenotypic analysis research and topics considered by Population and equivalent to those on the genomic and Evolutionary Processes, Ecological and computational side are needed, as these research Evolutionary Physiology, Animal Behavior and frontiers require a variety of high-throughput, related programs at NSF. In addition to high-precision techniques for measurement of identifying nine thematic areas within genetic, physiological, and phenotypic evolutionary biology, the panel considered how characteristics in large numbers of individuals in questions within these areas relate to questions in the field as well as in controlled, laboratory molecular genetics and genomics, systematics, environments. environmental sciences and other areas. • Genomics – The advent of high throughput In reflecting on research frontiers that have DNA sequencing has led to the availability emerged since 1998, two related trends are of whole genome sequences for a broad evident. First, evolutionary approaches and phylogenetic sample of organisms, including perspectives are increasingly an integral part of replicate genome sequences for different all areas of biological research, from molecular individuals of the same species. Microarray biology to macroecology. As a result, we are analyses of gene expression (and similar increasingly able to explore the mechanisms, methods) allow dissection of complex processes and patterns of evolutionary change at genetic networks involved in physiological, multiple levels of biological organization from developmental, and behavioral responses. the gene to the ecosystem. Second, technological Large-scale genetic manipulation allows advances in genomics, computation, and experimental tests of adaptive hypotheses informatics have provided a world of new tools involving particular genes or sets of genes. and information to apply to evolutionary Environmental DNA provides insights into questions. These and similar technical advances the physiological and evolutionary dynamics will continue to be a key factor in pushing the of unculturable microbes. Challenge: to 1 Figure 1: Connections among research frontiers identified in this report. connect sequence-and expression-level data allow them to record corresponding with organismal phenotypes and responses. environmental variables at the scale at which • Analytics – The high-speed computational organisms sense the environment. Wireless resources now available enable complex technologies allow these measurements to statistical analyses and simulation studies be recorded without capturing or relocating faithfully reflecting details of biology that the individuals, and future integration with were previously impossible. Genome, global positioning systems will allow these phylogenetic, and environmental databases data to be integrated with fine-scale climate provide a wealth of information about the and environmental variables. Challenge: to genetic characteristics of organisms, their develop high-throughput methods allowing evolutionary relationships, and the external complex phenotypic measurements to be environment in which they occur. Continued made reproducibly at high frequency on a statistical and computational developments large number of individuals. are paving the way for a reconciliation of historical and cross-sectional analysis of genetic variation. Challenge: to develop RESEARCH THEMES the conceptual framework for large-scale Research questions in evolutionary biology are databases of organismal phenotypes, the highly interrelated. Answering fundamental tools necessary to integrate these disparate questions about organismal adaptation, for databases into a comprehensive resource for example, requires understanding not only the analysis of large-scale patterns in genomic consistency, magnitude, and objects of natural and phenotypic evolution, and the statistical selection but the ways in which genome structure techniques for fine-scale evolutionary (including the structure of gene regulatory analysis of population history. networks) influences the distribution of mutational effects and the response to selection. • Phenomics – Advances in sensor technology enable real-time measurements Moreover, determining how genome structure of many important physiological variables in influences the evolution of integrated phenotypes the field. Advances in sensor design will is vital if we are to understand how individual- 2 level differences in development are related to • What are the extents and rates of changes in mechanisms of species divergence and large- genome structure and size, and what are scale patterns of biotic diversity. their functional consequences for organismal The workshop identified nine interrelated evolution? themes as research frontiers, broad areas where • How do new genes arise and go extinct? existing or foreseeable technology makes great • How does selection act on large-scale advances possible in the next decade (Figure 1). variation in genome structure and organization? The Evolution of Genome Structure and • What are the relative roles of changes in Function structural, regulatory, and non-genic Scope: Evolutionary change requires change in sequences in organismal evolution? the architecture or components of genomes, and • What evolutionary forces determine organismal properties determined by genetic or transposable element activity and number in molecular interaction networks that arise from genomes, and what are the functional the expression of genes. Understanding genomes, consequences of these mobile elements? their components, and the interaction networks • What is the structure of genetic networks, that arise from them is fundamental to a modern how do they evolve and how
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