Frontiers in Evolutionary Biology

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          PREPARED FOR


           March 2005
Table of contents

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
This report was prepared by the participants of the workshop. The workshop was sponsored by the National
Science Foundation through Grant No DEB-0500314, to the University of North Carolina at Chapel Hill. Any
opinions, findings, conclusions, or recommendations expressed in this report are those of the participants and
do not necessarily represent the official views, opinions, or policy of the National Science Foundation.
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

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
•   Phenomics – Advances in sensor                        mutational effects and the response to selection.
    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-

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
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 does network
understanding of the genetic basis of                     topology influence organismal evolution?
evolutionary change.                                  •   What are the evolutionary causes of
Rationale: Genomes are highly complex                     differences in recombination and mutation
molecular assemblages that encompass the                  rates across the genome?
fundamental physical organization of genetic
information in organisms. Fundamentally,              Genetics/evolution of adaptation
genomes are organized to encode the genetic           Scope: Adaptation requires both that organisms
information in discrete units (genes) as well as to   differ in fitness and that those fitness differences
contain sequence elements (e.g., centromeres and      be heritable. Understanding how adaptive traits
telomeres in most eukaryotic systems, ori             evolve requires that we integrate genetic analyses
sequences in bacteria) necessary for the              of phenotypic differences with analyses of the
transmission and maintenance of genetic               performance consequences of phenotypic
information.                                          differences in an ecological context.
     Genomes also have specific architectures         Rationale: Molecular genetic studies have
and components that vary dynamically both             provided a wealth of information on historical
within and among species. We are beginning to         patterns and rates of evolution of particular genes
understand that single-gene approaches to             but have rarely made a connection with
understanding genome structure and function are       particular phenotypes or adaptive value.
insufficient. Individual gene products are            Similarly, a great deal is known about the
embedded in large-scale interaction networks          adaptive value of specific phenotypes in
that represent integrated functional units at the     ecological contexts and rates of phenotypic
molecular genetic level.                              evolution, but little is known about their genetic
     Our understanding of the evolutionary            basis. While connecting these types of studies
dynamics of diversification in genome structures      has been an underlying goal in evolutionary
and their associated molecular genetic networks,      biology since the synthesis of evolutionary
however, remains limited. Moreover, few               theory and genetics, only now has it become
comparative genomic studies are underpinned by        possible to make these connections explicit. New
a clear phylogenetic context. Finally, we lack        genomic, molecular and computational tools
theoretical analyses to inform our understanding      offer the opportunity to link genetic variation at
of how genomes and their associated genetic           the DNA level with phenotypes, even in non-
networks evolve. The revolution in genomics           model organisms. Combined with technological
technologies and resources, including whole           advances and novel theoretical machinery, we
genome sequences, low-cost sequencing,                now have an unparalleled ability to measure
microarray technologies and computational             selection on the genes underlying phenotypic
power, now allow us to begin to address               variation in natural populations. Furthermore,
questions surrounding the evolution of genome         improved understanding of gene functions and
structure and function.                               interactions will allow us to study more fully the
Frontier questions                                    evolution of adaptive phenotypes. Investigations

into the existence of generalities concerning the     architecture of traits that differentiate populations
genetic basis of adaptive evolution will require      and species.
studies in many different organisms over long         Frontier questions
periods of time.                                      • How do gene-genealogies diverge at
Frontier questions                                        speciation?
• What is the molecular basis of adaptation?          • What is the genetic architecture of
• What types of genes are involved in                     behavioral, ecological, physiological and
     adaptation: regulatory or structural?                developmental incompatibilities that cause
• What types of mutations are involved in                 reproductive isolation? How does genetic
     adaptation: non-coding, point, indel,                architecture constrain or promote divergent
     transposable elements?                               selection on such traits?
• What genetic features of adaptive evolution         • Do pre-zygotic incompatibilities evolve
     are convergent?                                      more frequently or less frequently than post-
• To what extent is phenotypic convergence                zygotic incompatibilities in the initial stages
     the result of genetic convergence?                   of divergence?
• How can an understanding of the molecular           • What proportion of the species’ genome is
     bases of adaptation reveal historical patterns       impervious to gene flow? What are the
     of adaptation in natural populations?                consequences of porous species boundaries?
                                                          What is the role of hybridization and
Population divergence and speciation                      genome reorganization in speciation?
Scope: Population divergence and speciation           • Must gene flow be absent for speciation to
are fundamental processes for the generation of           occur? How common are the conditions
biological diversity. They produce the boundaries         under which sympatric speciation can occur?
within which microevolutionary forces act. They           How common is reinforcement?
are manifest by changes in the allelic                • Is the standing genetic variation within
composition of phenotypic variation among both            species the major genetic reservoir for
diverging populations within species and                  speciation?
recently diverged species groups.                     • What can the patterns of variation among
Rationale: New approaches and technologies                taxa tell us about the evolutionary processes
are facilitating unprecedented insights into the          by which they arise?
mechanisms of population divergence and
speciation. The ability to apply these                Microevolution of development
technologies to non-model systems offers the          Scope: All phenotypes in multicellular
opportunity to probe a diversity of speciation        organisms are the result of development. An
patterns and mechanisms. This comparative             emerging understanding of developmental
frontier will enable syntheses of evolutionary        mechanisms coupled with recently developed
forces that cause phenotypic divergence and           genomic tools makes it possible for the first time
speciation, an understanding of genetic               to study the evolutionary mechanisms by which
architectures of diverging traits and populations,    differences in organismal development arise.
and predictions about the extent and direction of     Rationale: The last twenty years of work in
possible gene flow between species. Phenotypes        developmental genetics has generated detailed
of particular interest include those underlying       information regarding shared and divergent
prezygotic incompatibility, such as                   features of the developmental mechanisms that
morphological and behavioral traits involving         underlie phenotypic (primarily morphological)
sexual or ecological isolation, and those             differences among broad taxonomic groups.
underlying postzygotic incompatibility, such as       These studies have revealed the surprising result
developmental or physiological traits causing         that there is a shared set of developmental and
hybrid sterility or inviability. Understanding how    regulatory processes (a shared “developmental
these traits evolve requires that we understand       toolbox”) that serves as the foundation for
the distribution of genetic variation within and      development within plant and animal systems.
among diverging species, the shape and                How can we understand organismal diversity in
topologies of gene genealogies that give              the face of this apparent pattern of conservation?
historical insight into that genetic variation,       Armed with a better grasp of large scale patterns
genome and chromosomal structural variation           of the evolution of development, it is now
between recently formed species, and the genetic      appropriate to turn our attention more fully to the

evolutionary processes that lead to these patterns.   signaling and locomotory performance, but
     Rapid advances in the detailed analysis of       understanding their evolution requires
developmental mechanisms within model taxa            approaches that treat the phenotype as an
coupled with increasing availability of genomic       integrated system rather than as a set of isolated
and functional genomic information now allows         traits.
for detailed studies of variation in developmental    Rationale: New approaches and technologies
processes within populations. These studies           have enabled biologists to measure complex,
include an analysis of molecular variation and        integrated phenotypes and their functional
molecular evolution of developmentally relevant       consequences in increasing detail and
loci, as well as variation in functionally related    sophistication. An individual’s fitness is the
characters such as levels and localization of gene    result of an integrated suite of phenotypic traits
expression. Complementary to the study of             interacting with environmental conditions; and
variation within populations is the examination       many such traits are multi-dimensional functions
of divergence in developmental characters             of age and environmental conditions. However,
among closely related species. The increasing         evolutionary studies often characterize an
availability of genomes of closely related taxa       individual’s phenotype in terms of a small
will facilitate this work. Another exciting area of   number of phenotypic traits, and consider
future research centers on placing this               variation and selection of phenotypes in a simple,
developmental information into an                     atomistic manner. Recent technological advances
environmental and ecological context relevant to      make it possible to pursue a different approach,
the whole organism.                                   to understand variation and selection of
Frontier questions                                    integrated phenotypes and to investigate how this
• How does phenotypic variation arise from            integration changes during evolution. An
     variation during development? How does           important related challenge is to develop the
     selection act on this variation?                 capacity to measure multiple components of
• What are the developmental mechanisms               integrated phenotypes on the large number of
     underlying phenotypic differences among          individuals required for lab and field studies of
     closely related species and how are these        genetic variation, selection, and evolution.
     differences related to variation within-         Frontier questions
     species?                                         • What are the patterns of evolution in
• What is the level of natural variation in                integrated suites of morphological,
     genes affecting different stages of                   behavioral, physiological and other traits?
     development? What are the signatures of               Are there different patterns or rates of
     selection and drift on these genes?                   evolution for different types of traits?
• How do homologous developmental                     • How do we visualize and quantify patterns
     processes generate non-homologous                     of phenotypic and genetic variation in high-
     phenotypes (i.e., what is the developmental           dimensional, integrated phenotypes?
     basis of convergence and parallelism)?           • How modular are integrated phenotypes in a
• How does the structure of developmental                  functional sense? How does functional
     pathways influence the evolution of the               integration emerge during development?
     genetic components of those pathways?            • How modular are integrated phenotypes
• How is adaptive plasticity achieved through              during evolution? How readily are such
     development modulation? What is the                   modules co-opted into new functional roles
     genetic architecture and molecular basis of           during evolution?
     plasticity?                                      • How do behavioral responses affect the
                                                           pattern of selection on morphological,
Evolution of Integrated Phenotypes                         physiological and other traits? How do
Scope: Many diverse characteristics of an                  immune responses and behavior interact to
organism—morphology, physiology, behavior—                 influence their joint evolution?
combine to yield an integrated phenotype that         • What are temporal and spatial patterns of
determines its functioning in some set of                  selection on integrated phenotypes in natural
environmental conditions. The phenotypic                   populations? Are patterns of selection on
characteristics may range from gene expression             integrated phenotypes different than for
profiles and metabolic fluxes to acoustic                  other traits?

•   What are the genetic bases of phenotypic             lineages maintain species cohesion? Can we
    plasticity in integrated phenotypes? How do          develop a species concept for
    differences in the pattern and magnitude of          microorganisms and viruses that captures
    plasticity affect selection and evolutionary         their evolutionary history?
                                                     Evolution of conflict and cooperation
Microbial Systems                                    Scope: Conflict is pervasive in the evolution of
Scope: Evolutionary biologists have devoted          life, and it is the key element of many major
relatively little attention to microbial and viral   transitions in the organization of life.
systems, even though microorganisms make up          Evolutionary conflict occurs in interactions
most of the tree of life. Both systems are           between species, between individuals, or
particularly amenable to experimental evolution      between genetic elements, and is sometimes
and to comparative genomics.                         overcome by cooperation. Understanding how
Rationale: New technologies that allow better        cooperation arises is important in explaining
sampling of both culturable and unculturable         major transitions from the organization of genes
genomes have expanded the tree of life,              in chromosomes, prokaryotes to eukaryotes, and
uncovering a third domain, and have shown us         other major transitions.
the immense diversity in the microbial world.        Rationale: Conflict and cooperation are crucial
Evolutionary experiments using microbes or           drivers of interactions within and between
viruses have enriched our understanding of           species. Between-species interactions include
genetic change in novel environments, of host-       plant-fungus interactions, pollination, host-
pathogen evolution, and of the evolution of          pathogen interactions, and ant-plant, or ant-
conflict and cooperation. Medicine, agriculture      fungus mutualisms. Selection operates on each
and industry are increasingly using evolutionary     partner to maximize their gain, and minimize
approaches to microbial and viral systems to         their cost, which can lead to arms races and
interpret data, track pathogens, improve             resulting rapid evolution.
bioremediation, manage resistance, and design              Within species interactions include male-
molecules and organisms for specific purposes.       female interactions, worker-queen interactions,
Microbial and viral systems are amenable to in       mother-fetus interactions and cell-cell
vivo reconstruction of ancestral genes and their     interactions in chimeric organisms. Since the
smaller genomes make them good candidates for        partners are members of the same species,
evolutionary genomics. These systems also            selection for gain in one partner can favor genes
provide a new testing ground for theories            that are detrimental when expressed in the other
developed for animals and plants, in which           role, leading to overall evolutionary compromises
horizontal gene transfer may be much less            in the organism. For example, genes for traits
important.                                           optimal in males make worse females.
Frontier questions                                         What stabilizes these interactions, what
• Are standard evolutionary models adequate          allows cooperation to evolve in the face of
     to explain and predict microbial evolution?     selfish genetic interests, and how the signature of
     To what extent do results from experimental     competition remains are questions that have only
     studies of microbes and viruses generalize?     recently been made accessible by advances in
• How do selection and co-evolution operate          genomics, phylogenetics, experimental
     in structured microbial communities such as     evolution, and molecular manipulation.
     biofilms?                                       Frontier questions
• What are the mechanisms and evolutionary           • What kinds of genes are important in social
     consequences of horizontal gene flow? How             interactions?
     does horizontal gene transfer influence         • How prevalent is the role of imprinting in
     cooperation and competition in microbial              genomic conflicts?
     populations?                                    • Is evolutionary conflict a major explanation
• What is the diversity of genome structure                for rapidly evolving genes? If so, what are
     among microbes and viruses, and what is the           the pleiotropic effects of rapid evolution?
     functional significance of this diversity?      • Are there general rules for the suppression
• How can we quantify microbial and viral                  of conflict during the evolution of
     diversity, define species, and classify               cooperation? How are cooperating systems
     unculturable organisms? How do microbial              stabilized against cheaters?

•   What determines the evolution of virulence?      on evolution of phenotypic attributes within
    What is the genetic architecture of              these groups.
    virulence?                                       Frontier questions
•   What is the role of evolution of conflict and    • Do different types of characters evolve at
    cooperation in major evolutionary                    different rates and at different phylogenetic
    transitions such as the origins of                   time scales within clades? Are there regular
    multicellularity, endosymbiosis, and                 patterns of divergence for different types of
    chromosomal organization?                            phenotypic characters when compared
•   What is the role of sexual conflict in               across clades?
    adaptation and speciation?                       • How does the environmental niche of
                                                         species evolve and to what extent is a
Large-Scale Patterns of Diversity in Time                species’ range determined by adaptation to
and Space                                                changing conditions? Does evolutionary
Scope: Large-scale patterns of biodiversity, like        change account for the success of invasive
the latitudinal species gradient and the diversity       species, and can such change be predicted?
of communities, have not received satisfactory       • How does the spatial structure of
evolutionary explanations. Understanding the             populations, species and communities affect
evolutionary basis for these patterns will require       evolutionary and coevolutionary change?
synthesis of within-population,                          How does the spatial structure of populations,
microevolutionary studies with across-taxa,              species, and communities evolve?
macroevolutionary investigations.                    • How can paleontological data be used to test
Rationale: The availability of well-corroborated         neontological hypotheses of selection and
phylogenies, data bases of species occurrences,          divergence? How can neontological data
and global environmental data now document the           test similar paleontological hypotheses?
ecological and evolutionary scale of diversity at    • How are processes of within-species
a large scale and in great detail, and the               divergence related to diversification of
development of new conceptual approaches and             clades?
computational methods permits analysis of these
data in manners not previously possible.             Applied Evolution
Phylogenetic studies have become the standard        Scope: Applied evolution marshals our
means of investigating historical, comparative       understanding of evolutionary principles to
questions, and a plethora of analytical methods      tackle significant environmental,
have been developed. At the same time,               epidemiological, and agricultural problems.
increasing understanding of past environments        Rationale: The scale on which humans are
and biotas permits the synthesis of neontological    changing the biosphere in the 21st century is
and paleontological data in novel and mutually       unprecedented. Global pressures by humans on
illuminating ways. Similarly, the recent             planetary resources not only cause extinctions
development of coalescent and comparative            and detectable shifts in species’ geographic
phylogeographic methods for inference of             ranges and phenologies, but also cause
within-species population histories now allows       measurable evolutionary change in natural and
similar questions to be investigated at the level    introduced populations. Emerging agricultural
of among-population differentiation. As a result,    pests and pathogens are moved almost
it is now possible to investigate the relationship   instantaneously around the globe. Applied
between processes leading to differentiation         evolution seeks ways in which evolutionary
among populations of the same species and those      principles can improve the human condition. Its
leading to diversification of entire clades.         applications range from improving ecosystem
      The challenge will be to develop methods       services to developing better vaccines. It also
that integrate across different disciplines and      encompasses a variety of approaches for
time-scales, spanning ecological,                    determining the impact of human activities on
microevolutionary and macroevolutionary time.        rates and patterns of evolutionary processes.
The assembly of suitable large scale data sets is    Finally, it includes efforts to trace the geographic
vital. For example, the Tree-of-Life program is      and taxonomic origins of rapidly spreading
developing large-scale, highly resolved              pathogens, to better understand their biological
phylogenies for many groups of taxa;                 effects and predict further spread, and to devise
comparable efforts are needed to collect the data    means of control.

     Examples of applied evolution span the           •   What is the impact of the agricultural
entire breadth of evolutionary biology. Using the         landscape on evolution of natural
tools of DNA sequencing and phylogenetics,                populations?
evolutionary biologists can determine the time        •   What factors influence the extent and
and geographic location of origin of invasive             consequences of gene flow between GM
species and emerging diseases. Evolutionary               crops and natural populations?
principles can be used to develop enzymes,
ribozymes, and even organisms with specific
functions and catalytic properties. Population        INSTITUTIONAL
genetics and ecological modeling can help             RESOURCES
predict if and how readily genes in genetically       Many of the resources necessary to advance the
modified organisms will spread into other             frontiers of evolutionary biology are already in
organisms.                                            place. Others are only now coming into
     One major challenge in this field is to better   existence. Some of the resources needed are
predict the course of evolution given detailed        institutional, but the scale of some questions will
information on the genetics and behavior of           require more collaboration among individual
organisms. This aspect of applied evolution will      investigators than has been typical of
have its greatest successes in understanding          evolutionary research in the past.
responses of very simple systems, such as those       • NESCent – The National Evolutionary
in microbes or viruses. In many cases, these               Synthesis Center will serve as a focal point
same systems will be the ones with the greatest            for a variety of activities including
impact on human populations and environmental              databasing and informatics development,
change.                                                    catalysis of cross-disciplinary interactions,
     Basic research has much to offer here.                and scientific synthesis. It will provide a
Experimental evolutionary approaches, in which             venue for the assembly, annotation, and
evolutionary changes in laboratory populations             integration of major evolutionary databases,
are measured in real time, will play an important          including genomic, phylogenetic, and
role in understanding the diversity of genetic and         phenotypic databases; for fostering the
phenotypic responses to intense selection. By              development of integrative, cross-
providing biologists with a catalog of genes and           disciplinary approaches to the solution of
physiological properties, whole genome                     evolutionary questions; and for encouraging
sequences of microbes and simple eukaryotes                the integration and synthetic interpretation
will also be a major bulwark of applied evolution          of evolutionary data and ideas.
in the future. Finally, large-scale monitoring of     • NEON – The National Ecological
environmental variables, such as those                     Observatory Network will provide an
envisioned in NEON, will allow biologists to               integrated, national platform at which a core
predict with increasing certainty the spread and           set of standardized ecological variables is
fate of organisms and pathogens and their impact           measured. It will provide a natural set of
on agriculture and the environment.                        locations for large-scale experiments
Frontier questions                                         designed both to measure the strength,
• Are there rules to predict changes in                    variability, and predictability of selection
     virulence or resistant of pathogens? Can we           and to assess the influence of evolutionary
     predict potential pest/pathogen status based          history on large-scale community and
     on ecological, genomic or phylogenetic                ecosystem processes.
     characteristics?                                 • RCN – Research Collaboration Networks,
• Can we use evolutionary theory to improve                which had just been established at the time
     the efficacy of directed evolution?                   of the 1998 Working Group report, allow
     Conversely, can directed/experimental                 groups of individual investigators
     evolution inform evolutionary theory?                 investigating similar questions to coordinate
• Can we predict changes in selection and                  their research. Investigators who take
     drift from changes in environmental                   advantage of the RCN program will be able
     conditions?                                           to address more comprehensive questions
• Can we predict the relative frequencies of               than they could working in isolation from
     range shift, adaptation or extinction in              one another.
     response to environment change?

•   FIBR – The Frontiers in Integrative                    populations should be a priority, including
    Biological Research program encourages                 non-model species that are close relatives of
    investigators to study “major, under-studied           genetic model systems. The resources
    or unanswered questions in biology and                 needed are not only whole-genome
    to use innovative approaches to address                sequences, but also the genomics tools that
    them by integrating the scientific concepts            make genetic manipulation possible. To
    and research tools from across disciplines             make these resources available, however,
    including biology, math and the physical               evolutionary biologists will need to coalesce
    sciences, engineering, social sciences and             around a selected set of evolutionary model
    the information sciences.” Many of the                 systems for genomic development.
    research frontiers identified in this report are   •   Phenomic resources: Evolutionary
    natural candidates for support from the                analyses of complex, integrated phenotypes
    FIBR program.                                          are limited by the capacity to measure and
•   IGERT – The Integrative Graduate                       analyze relevant phenotypes on large
    Education and Research Traineeship                     numbers of individuals in the context of
    program “is intended to catalyze a cultural            evolutionary studies in the lab and field.
    change in graduate education … by                      Engineering resources for development of
    establishing innovative new models for                 new technologies for automated, high-
    graduate education and training.” Many of              throughput phenotype measurement systems
    the research frontiers in this report require          will be important to accomplish this task.
    integration of traditional biological              •   Large-scale experimental evolution:
    disciplines with the development of new                Replicated, experimental studies of
    computational, statistical, and analytical             evolution at a regional to national scale
    tools. Graduate training programs that seek            would be invaluable for understanding
    to train such students are natural candidates          short-term (1-100 year) evolutionary
    for support from the IGERT program.                    responses to environmental change in
                                                           natural populations. The developing
                                                           National Ecological Observatory Network
INFRASTRUCTURAL NEEDS                                      (NEON) holds great potential for enabling
AND OPPORTUNITIES                                          such large-scale evolutionary experiments.
Much of the infrastructure required for                    Planning for instrumentation relevant to
advancing evolutionary research is already in              genetic and evolutionary analyses in the
place, as outlined above. There are, however,              context of NEON is needed to achieve this
several areas in which the infrastructure falls            potential.
short and which are vital areas for future             •   Analytic resources: Databases for
investment.                                                phylogenetic, environmental, DNA
• Genomic resources: The choice and                        sequence, and protein structure data are
    development of genomic data and tools to               widely used and accessible, but comparable
    date have naturally focused on genetic                 resources for phenotypic data are lacking.
    model systems and species of applied                   The conceptual tools needed to develop an
    biomedical or agricultural importance.                 appropriate standard for phenotypic
    However, species vary in their utility for             metadata have not been developed. Just as
    informing us about evolutionary patterns               importantly, the computational and
    and processes. Mus musculus, Drosophila                analytical tools necessary to integrate data
    melanogaster, Arabidopsis thaliana and                 derived from phylogenetic, environmental,
    other species for which extensive genomic              DNA sequence, protein, and phenotypic data
    resources are now available allow us to                have not been developed. Even tools for
    answer some evolutionary questions and                 visualization and analysis of variation in
    their full value is yet to be exploited, but           complex phenotypes are largely lacking.
    these species are too divergent from one               Advances in all of these areas are needed to
    another and represent too little evolutionary          address many of the issues identified in this
    diversity to allow us to answer many critical          report.
    questions in evolutionary biology. The
    development of genomic resources for
    evolutionary significant species and natural

Appendix: Workshop participants

Dr. Scott V. Edwards                           Dr. Therese Ann Markow
Museum of Comparative Zoology                  Center for Insect Science
Harvard University                             University of Arizona
Cambridge, MA 02138                            Tucson, AZ 85721             

Dr. Jack Hayes                                 Dr. Patrick C. Phillips
Biology Department                             Department of Biology
University of Nevada Reno                      University of Oregon
Reno, NV 89557                                 Eugene, OR 97403-5289 USA                       

Dr. Kent E. Holsinger                          Dr. Michael Purugganan
Department of Ecology & Evolutionary Biology   Department of Genetics
University of Connecticut, U-3043              North Carolina State University
Storrs, CT 06269-3043                          Raleigh NC 27695            

Dr. Scott Hodges                               Dr. Kerry L. Shaw
Department of Ecology, Evolution & Marine      Department of Biology
Biology                                        University of Maryland
University of California                       College Park MD 20742-4415
Santa Barbara, CA 93106              
                                               Dr. Joan E. Strassmann
Dr. Joel G. Kingsolver                         Dept. of Ecology and Evolutionary Biology, MS
Department of Biology, CB-3280                 170
University of North Carolina                   Rice University, 6100 Main St.,
Chapel Hill NC 27599-3280                      Houston TX 77005-1892 USA                   

Dr. Jonathan B. Losos                          Dr. Holly A.Wichman
Department of Biology                          Department of Biological Sciences
Campus Box 1137                                University of Idaho
Washington University                          Moscow ID 83844-3051
Saint Louis, MO 63130-4899