National Science Foundation Research Coordination Network:
Integrating Ecology and Endocrinology in Avian Reproduction
(E-BIRD-USA)
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National Science Foundation Research Coordination Network: |
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Birds are some of the most familiar organisms of global ecosystems. Extensive research on this group has focused on ecology, evolution, physiology and many other branches of biology. Changes in the visibility and abundance of birds are excellent indicators of population and physiological responses to habitat changes, and are a major focus for public concern about detrimental environmental changes.
Increasingly, avian populations are affected by both large-scale climate change and by altered land use by humans. In order to understand how birds respond to these challenges, it is essential to determine how the environment affects reproduction of wild birds. The continuum from environmental variables (cues) to reproductive life-history traits depends upon a cascade of neural and physiological processes including perception of the physical and social environments, and transduction of that information into neuroendocrine and endocrine secretions that then regulate reproductive function. These are the processes that determine the extent and rate at which birds adapt to changes in their environment.
The objective of this network is to develop a framework whereby ecologists and endocrinologists can collaborate directly using avian reproduction as a model system. This framework will ultimately apply to all taxa because the principles involved will be universal. Ecologists and endocrinologists focused on avian reproduction will work toward developing theoretical and practical ways by which the two disparate disciplines can interact, resulting in new techniques and data bases that will set the stage for future integrative research on other topics.
Workshops will help formulate ideas, technical meetings (smaller groups) will target specific informational needs and methods to integrate and analyze data, and individual laboratory exchange visits will implement these. The reports from workshops, technical meetings and exchange visits will be posted on this web-site and will be a focal point of the network. Extensive literature citations, formal presentations of new theoretical frameworks and techniques, will be posted as well as a forum where participants can air their comments, criticisms, and identify potential problems and future directions.
There will ultimately be an important educational component that will grow out of the integrative research. For example, the principles developed by this network will likely aid us to teach truly integrative biology in the future. There is also a very strong conservation component. The framework will allow a much greater understanding of ecology, physiology/endocrinology that in turn will provide greater insight into conservation issues such as the impact of global change on reproduction, human disturbance and pollution, and monitoring re-introductions of endangered species.
We have identified certain individuals who represent diversity and they will be actively encouraged to participate at all levels. All participants will be required to search for, and identify other potential contributors and students that represent diversity from 2 and 4 year colleges to high schools. In this way we will broaden participation, and increase recruitment of researchers who represent diversity.
The network is twinned with a European initiative on the same topic – “Adaptation and Constraints in Avian Reproduction: Integrating Ecology and Endocrinology (E-BIRD)”. Drs. Marcel Visser and Marcel Lambrechts are P.I.s (link). There is also a Canadian network, P.I. Tony Williams (link), that forms the third major group. The respective networks and websites (E-BIRD) will be closely coordinated through the respective P.I.s.
The twentieth century has seen several revolutions in the biological sciences. In one hundred years we have progressed from cataloguing and describing species to sequencing genomes. Along the way we have made astonishing advances in cell and molecular biology, theoretical ecology, ecology, genetics, behavioral neurobiology, etc. These and other areas of the biological sciences will continue to develop, but one enormous hurdle awaits: how to integrate our knowledge of biology so we can deal with potentially catastrophic environmental problems as well as pave the way for a deeper and broader understanding of how life on this planet works.
A major recurring problem with the spectacular success biology has experienced is that individual researchers have become so specialized and focused that in many cases they have difficulty communicating with colleagues in other branches of biology. Advances in science and understanding are commonly reaching limits imposed by lack of knowledge of mechanisms explained by other disciplines and, therefore, emphasizing the need for interdisciplinary research to continue major breakthroughs in both understanding and solutions. In other words, molecular biology or theoretical ecology in isolation will not solve problems that involve populations, their component individuals, as well as the complex interplay of physiology, behavior, cells and molecules by which individuals function and interact. For example, developmental biologists have advanced understanding of cell differentiation, rate and processes, but lack a full understanding of endocrine controls on cells and rates of differentiation and the interplay of complex systems such as the brain. These require an understanding of the mortality agents (selection) arising in the environment and how selection acts on the phenotype. There is a need for opportunities to conduct interdisciplinary research at these levels. Signs of integration are emerging but some branches of biology are so far apart that interdisciplinary work linking them appears impossible.
Additionally, progress toward interdisciplinary research and education is often thwarted by lack of a mechanism to foster it when the rare opportunity does arise. Citing a report from the National Academy of Sciences, Jasanoff et al. (1997) assert that young scientists will be impeded in their advancement in the future unless they are trained from an early age to diversify their expertise and career objectives. They have reached this conclusion at a time when most institutions with biological science programs still advocate specialization, and split their departments into highly focused units that do not, and often cannot, communicate with one another. We need new forums and methods of communication to allow biologists to interact with each other as well as with the public.
Despite the trend toward specialization and isolation over the past thirty years, many biologists in widely different fields believe we will need integration and interdisciplinary work in the future to break through into exciting new areas of research. Ecologists acknowledge that more proximate approaches may reveal deeper insights into ecosystems, evolutionary biology and social interactions. At the other extreme, although sequencing of various genomes from yeast to human is greatly expanding our understanding of both the diversity and conservation of genetic information, how does one proceed from a gene sequence to its biological role? Linking genes to specific actions is a considerable problem largely because genes work in complex biological pathways and not in isolation (Cohen, 1997; Pfaff, 1997). The particular functions of a differentiated cell involve a complex interaction of many proteins that can be modified by hormones. Coordination of gene activity among various cells and tissues of the organism culminating in responses to internal or external environmental signals also involves hormones. In other words, the study of environmental endocrinology in ecological contexts is concerned with how hormones orchestrate transitions in morphology, physiology and behavior in relation to a changing and sometimes capricious environment.
Imagine observing an ecosystem and focusing on certain populations of individuals within it that apparently have a problem dealing with a change in the environment triggered by, for example, human disturbance. Immediately one wonders why some populations, or individuals within them, deal with the environmental challenge better than others. It is reasonable to then ask what aspects of their physiology, behavior and morphology are the cause of this failure (or success), and what the cell, molecular and genetic bases of these differences might be. The investigation of inter-individual variation is also the foundation for predicting how populations will evolve in response to environmental change.
Although it is relatively simple to construct hypothetical scenarios whereby we traverse the spectrum of biological science from ecosystem to molecule in either direction, it is not so intuitively obvious how we do this in practical terms. If such an interdisciplinary and integrative approach can be achieved, the dividends will be spectacular. A new age of biology will provide not only new research directions, but also determine how we will teach biology to future generations to prepare them to deal with global changes already underway. The current acute problem is how to achieve such a level of integration.
Given the fragmentation of biological sciences and the rapid progress its sub-disciplines have made in the past thirty years, it is no longer possible to be a first rate molecular biologist as well as be conversant with physiology, evolutionary biology, ecology, etc. Success in each field requires so much training and experience that it precludes a similar level of proficiency in other areas. No single individual will be able to provide the interdisciplinary expertise to bridge these issues. A collaborative effort of biologists, internationally recognized within their respective fields but also with a shared vision of integrating biology for the future, is essential.
We propose to develop a network for integration of ecology and endocrinology focused on a single theme – avian reproduction. Given the central importance of environmental endocrinology to many global issues, and its connections to the full spectrum of biological sub-disciplines, we believe that this topic will draw together investigators with the collective expertise to achieve our goals. While ecologists and endocrinologists do not have a history of working together to solve problems in basic or applied science, they nevertheless share intellectual approaches that will allow rapid and effective communication. Whether ecological or physiological, members of both disciplines are trained to think in terms of multivariate, systems-level interactions as well as positive and negative feedback in regulatory control.
This overarching theme is pivotal because hormones provide a link that extends from gene regulation to the responses of populations to environmental challenges. All animals use chemical signals whether neural, neuroendocrine or endocrine, to survive, reproduce and communicate. Various environmental cues are used to elicit these internal signals so that the organism may adapt optimally to its habitat. They then coordinate changes in development, physiology, morphology and behavior using common molecular and cellular mechanisms.
Hormones also have a major role in regulating responses to environmental perturbations such as natural stresses (e.g. bad weather, El Niño Southern Oscillation events, fire, increased numbers of predators), or anthropogenic disturbances such as environmental degradation, global climate change, and pollution that can have profound effects on reproduction. Many pollutants are now known to act as endocrine disrupters – i.e. they can mimic or block natural hormones and alter physiology, reproduction or development etc. accordingly. Clearly, the study of how organisms use hormones to adjust to a changing and often unpredictable environment - is an ideal template for the integration of molecular and organismal endocrinology with ecology beyond anything we have been able to accomplish to date.
Each investigator will be able to contribute to the theme in one or several ways, thus building research programs far greater and further reaching than anything more specialized research teams could accomplish. For example, preliminary studies show that mathematical analyses of natural history data such as egg-laying dates in birds provide a framework from which to predict how different populations of animals in very diverse habitats may use suites of environmental signals to time reproductive development and regression (e.g. Wingfield et al., 1991, 1993). Subsequent experimental tests in the laboratory supported these predictions (e.g. Wingfield et al., 1994, 1996) setting the stage for cell and molecular approaches to explore neural and neuroendocrine pathways involved in transducing environmental signals into hormone responses. This research program began with a collaboration of mathematical biologists and physiologists, and has now progressed to interactions of physiologists with cell and molecular biologists. It is just one example of a project currently underway that is using environmental endocrinology as it’s focus and the principle can be applied to many other biological processes.
At the other end of the spectrum, ecologists have focused on intra-specific changes in numbers of eggs laid each year, when they are laid, size of the eggs etc. and why these vary from region to region, individual to individual and year to year. (Lambrechts and Perret, 2000; Lambrechts et al., 2000; Visser et al., 2003). Changes in numbers and sizes of eggs may covary with other phenotypic traits such as development of embryos and nestlings that can be influenced by hormonal controls on parental care and nestling behavior (Schwabl, 1996; Starck and Ricklefs 1998, Martin 2002). This variability undoubtedly has an endocrine basis, and understanding the mechanisms will provide new insight into evolutionary aspects of these traits (Ketterson et al., 1996, Williams, 2001; Williams and Vezina, 2001). Neuroendocrine and endocrine pathways by which environmental variables regulate reproductive function are currently under investigation (Dawson et al., 2001; Hau, 2001; Ball and Balthazart, 2002). Furthermore, we know very little about life history differences between temperate, polar and tropical birds even though the latter may contain two thirds of all species (Hau, 2001).
Ultimately, we must understand these interactions if we are to generate new research directions from genes to ecosystems, and to predict the consequences of global climate changes, human disturbance etc. Only a "network" mode of operation, that fosters collaborations of biologists from different fields, could support such endeavors on a broader scale.
There are perhaps few vertebrate taxa that have been studied more extensively than the class Aves in relation to ecological, morphological, physiological and behavioral aspects of reproduction. Evolutionary aspects have also been intensively investigated. This immense database, and the large number of excellent investigators in this field that can potentially interact in novel ways, makes the theme of avian reproduction ideal for the formation of a research coordination network. For example, why do different populations and individuals breed at different times and for varying periods? This is probably a result of environmental factors because meta-populations, genetically mixed by dispersal of young, can show enormous variation in response to environmental signals even though they may be located within a few hundred meters of each other (Lambrechts and Perret, 2000; Lambrechts et al., 2000; Visser et al., 2003). Mathematical techniques can be applied to reproductive data such as egg-laying dates (Wingfield et al., 1992, 1993), to identify populations that may have short, highly predictable and inflexible breeding seasons versus longer more flexible breeding seasons. Data thus far suggests that populations of birds with inflexible breeding seasons are insensitive to environmental cues that cause major acceleration or inhibition of breeding in populations with flexible seasons (Wingfield et al., 1996, 1997). Now it is possible to compare closely related populations with different responses to environmental signals (Gwinner, 1996; Berthold, 1999) by using cellular and molecular probes to determine the neural and neuroendocrine bases of plasticity in reproductive function, and sensitivity to environmental signals (Tobet et al., 1997; Wasser et al., 1997; Ball and Balthazart, 2001; Dawson et al., 2001; Adkins-Regan and Weber, 2002; Balthazart and Adkins-Regan, 2002).
At a meeting in Wageningen, The Netherlands, in September 2002, participants were unanimous in proposing a network to serve as a nexus for collaboration between ecologists and endocrinologists. This is an extremely cost-effective way to facilitate rapid progression of innovative and integrative research from genes to ecosystems. The plan is to coordinate three major networks, one in Europe, funded by the European Science Foundation, one in Canada funded by NSERC and one in the U.S.A. funded by the National Science Foundation. Thus three levels of management are necessary: first to promote activities of the network within the U.S.A. and second, to coordinate activities with international participants. The P.I. will be responsible to directing the Steering Committee within the U.S.A. as well as to communicate extensively with international P.I.s, particularly when joint workshops are held, and for providing links between web sites promoting network activities on a global scale.
It is essential that an integrated program such as this be constantly self critical and sensitive not only to peer review of research, but also to educational needs, public opinion, and information transfer. A two-tier review system is proposed that will ensure the highest quality performance of the network, and also guarantee that it’s product remains greater than just the sum of its parts.
A Steering Committee of participating faculty in the U.S.A. will comment and advise on participation in workshops, technical meetings and laboratory exchange visits. The P.I. will be responsible for coordinating the steering committee, bringing proposals for technical meetings and exchanges to their attention, and guiding the decision process in an equitable way. The committee is drawn from across the U.S.A. and has been selected to balance gender and include as many faculty who represent diversity as possible. This group will meet once a year (coordinated with workshops), although the P.I. will invite continual input by electronic means through the website so that perceived weaknesses and/or strengths can be addressed quickly. Inputs from members of the Steering Committee will advise the P.I. as to what future new directions may be explored as well as assess our past performance. The P.I. will also be responsible for coordinating efforts and assessment review with the European and Canadian network leaders. The forum on the web site will also invite comment, criticism and debate from all participants, national and international, as well as from the biology research community as a whole.
The structure of the Steering Committee must be fluid, and at the outset the first task of the committee will be to provide a mechanism whereby new members can be brought in as others rotate off. It is critical that gender representation remain balanced and inclusion of members who represent diversity will be a high priority. The committee, along with the P.I. will be responsible for recruiting proposals for workshops, technical meetings and exchange visits and nurturing their development.
In the event that more proposals for technical visits and exchanges are submitted than funds can support, the committee will be responsible for discussion and decisions on which will be supported. The P.I. will be responsible for directing this discussion and asking for votes, on line, on any decisions thus ensuring a fair and equitable process.
Leaders will be designated for all workshops, technical meetings and exchange visits, and they will be required to write a report summarizing results, concepts, emerging new areas etc. These will be reviewed by the Steering Committee (coordinated by the P.I.) and the final product posted on the web site. The network will promote publication of new ideas, reviews, techniques, methods of analysis etc. – i.e. a true deliverable that can be disseminated widely. It is expected that new collaborative grant proposals will result thus advancing the field further (such proposals will be a another measure of success of the network).
Evaluations by participant students will be very useful to assess training aspects of the network. These would also be posted at the web site for general comment. Each workshop and technical meeting will be evaluated by all participants - another deliverable by which efficacy of the network will be monitored closely throughout the project period. A similar approach will be followed to assess our success in attracting participants who represent diversity.
The P.I. and the Steering Committee will be responsible for ensuring that all contributors to the web site understand that by so doing they place all materials (databases, literature information, reports etc.) in the public domain and everyone has access to this information for research, education and outreach.
The P.I. will not be involved in the practical organization of all the workshops, technical meetings and exchange visits envisaged. This will be achieved by local organizers, and details of exchange visits will be finalized by the participants themselves. The P.I. and the Steering Committee will evaluate the scientific quality of the activity and will oversee the organization and financial details. The Steering Committee will decide the topics, organizers and budgets for each of the workshops. However, in each case an endocrinologist and an ecologist, and a European and a North American will be involved in the organization of the workshops:
After four years, it is expected that the network will have established a well-connected group of avian ecologists and endocrinologists. It is also predicted that many other fields of biology will be connected to the network including investigators focusing on other organisms and other levels of analysis (molecule to ecosystem). Collaborative research projects will be underway or submitted for funding from regular NSF channels or from other sources. The web site will continue to develop after the period of funding requested here ends. The P.I., and those in Europe and Canada, are dedicated to updating it as necessary, and linking it to other organizations and networks in biological sciences.
We are developing this network in a combined effort with a group of Europeans, Co-P.I.s Marcel Visser, Ecological Institute, Heteren, The Netherlands, and Marcel Lambrechts, CNRS, Montpelier, France, Canadians P.I. Tony Williams (Simon Fraser University, British Columbia) and USA participants, P.I. John C. Wingfield, University of Washington, Seattle, Wa, USA. Coordination of web-sites will greatly enhance the effectiveness of the proposed activities.
Four workshops are proposed that are closely allied to those in the European proposal. Indeed the Europeans and North Americans plan on jointly attending these workshops, two in Europe and two in North America. This includes the final general workshop when all participants will be brought together for an extensive evaluation and to summarize integration. These common workshops are essential to keep international participants in contact and working actively to develop the network. At these times the Steering Committees of each group will meet to discuss past performance and future activities. Web-site coordination will also be assessed. The P.I.s of each network will be in continual contact on line throughout the duration of funding and beyond. The network web sites will develop as an important resource for international collaboration.
Because the network will bring together avian ecologists and endocrinologists, in order to facilitate exchange of knowledge between these fields, and to stimulate collaborative research, information and material sharing is essential. The primary tool for information sharing will be the creation of a web site. It will serve as a focal point for collaboration between ecologists and endocrinologists as well as a launching point for collaborations beyond the immediate scope of this proposal. An electronic newsletter (available to anyone who asks for inclusion on the web site roster) will be used to alert people when new information is made available. A list of laboratories with an emphasis on research on avian reproductive endocrinology and/or ecology will be available, including descriptions of the main research interests, species used and techniques available. Links to other associated sites will be useful here. The site will be set up so that interested parties will be able to e-mail all or selected groups of involved scientists for further information. Moreover, we will build a literature database on studies integrating ecological and endocrinological avian research and beyond. The web site will also function as the primary source of information on the network in the U.S.A., international links, educational opportunities, etc.
It is proposed, and expected, that the collaborative research directions resulting from the workshops, technical meetings and exchange visits will be published in peer-reviewed journals. These published data (and older literature already available) will be collected together in a citation resource available on line. It is planned that reports and developments from workshops and technical meetings will be posted on the web site with commentary from peers in the field and ongoing debate on how new technology, theory etc. can be used in a more broad context (biology as a whole).
It is also envisioned that as the network develops, databases will develop, grow and be coordinated internationally. For example, there is now an extensive literature on the hormonal responses to stress, especially modulation of the stress response in varying environmental conditions. What is much less understood are the ecological bases of these responses and their evolution. It is here that unpublished data (perhaps not sufficient for publication alone) could also be posted to add to the database so that others could re-analyze the data in ecological contexts according to expertise that users with access to the site will bring. Again, it will be the responsibility of the P.I. and Steering Committee to ensure that everyone that contributes to the database on line understands the public nature of the site, AND that others will have access to those databases.
Links: Society for Integrative and Comparative Biology (SICB) and American Association for the Advancement of Science (AAAS) web-sites to provide access to the broader scientific community. After the four year period of this proposal to develop the network, we will organize symposia at national meetings (e.g. SICB, Society for Behavioral Neuroendocrinology, Neuroscience, Animal Behavior Society, Behavioral Ecology meetings, Ecological Society, Society for Conservation Biology and others) and international meetings (e.g. International Ornithological Congress, International Symposium on Comparative Endocrinology, International Union of Physiological Sciences and others) to emphasize new approaches more broadly.
It is planned to specifically invite faculty and postdoctoral fellows that represent diverse ethnicities to workshops, and technical meetings. Indeed at all these meetings there will be a mandatory session on recruiting and inviting participants that represent diversity. Targeted individuals will also be of high priority when planning exchange visits to promote specific collaborations. We will begin outreach to Latin American countries and elsewhere when opportunities exist and advertise the web site in other society newsletters, journals, etc. through announcements. The web site will also be advertised to biology departments in 2 and 4 year colleges and high school programs to target minorities. Thus the plan is to identify and attract researchers representing diversity and with expertise/interest in the featured topics to workshops, technical meetings and exchange visits and nurture their participation and development in the field. Students will be targeted so that those representing diversity will also be recruited into the field. It is planned to make special effort to invite faculty from institutions with strong MARC programs (Minority Access to Research Careers) and encourage them to attend workshops and technical meetings with their talented MARC students.
At the exploratory workshop held in Wageningen, Netherlands, September, 2002, the following future workshops were identified as being highly relevant for the European, Canadian and U.S.A. proposals.
These will develop as the network grows and participants interact. Possible topics currently under discussion are: