Grand Opportunities: Strategies for Addressing Grand Challenges in ...

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NOT FOR PUBLIC RELEASE Integrative and Comparative Biology, pp. 1–7 doi:10.1093/icb/icr052

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Grand Opportunities: Strategies for Addressing Grand Challenges in Organismal Animal Biology Jonathon H. Stillman,1,*,† Mark Denny,‡ Dianna K. Padilla,§ Marvalee Wake,† Sheila Patekô and Brian Tsukimura*,*

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*Romberg Tiburon Center and Department of Biology, San Francisco State University, 3150 Paradise Drive, Tiburon, CA 94920, USA; †Department of Integrative Biology, University of California, Berkeley, Valley Life Sciences Bldg Berkeley, CA 94720-3140, USA; ‡Hopkins Marine Station, Stanford University, 120 Oceanview Blvd. Pacific Grove CA 93950, USA; § Department of Ecology and Evolution, Stony Brook University, Stony Brook, NY 11794-5245, USA; ôDepartment of Biology, 221 Morrill Science Center, 611 North Pleasant Street, University of Massachusetts, Amherst, MA 01003, USA; **Department of Biology, California State University, Fresno, 2555 E. San Ramon Avenue, MS#SB73, Fresno, CA 93740, USA 1

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E-mail: [email protected]

The Biology Directorate at the National Science Foundation (NSF) has requested that organismal biologists develop a vision and articulate the grand research challenges that will drive the future of organismal biology, and the large-scale community-wide efforts that would be needed to address those challenges. Over the past decade, organismal animal biologists have been slow to develop community-wide initiatives relative to other bioscience communities (e.g. molecular biologists, ecologists, evolutionary biologists, and plant biologists). In response to NSF’s request, the Society for Integrative and Comparative Biology (SICB) organized an effort to begin to articulate grand visions of the research questions that will form

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the foundation of future research in organismal animal biology (hereafter referred to as ‘‘organismal biology’’ for brevity). White papers, now known as contributions in the ‘‘Grand Challenges in Organismal Biology’’ (GCOB) series, have been published in Integrative and Comparative Biology over the past 2 years (Denny and Helmuth, 2009; Denver et al., 2009; Satterlie et al., 2009; Schwenk et al., 2009; Mykles et al., 2010; Sih et al., 2010). These papers define a number of large-scale forwardthinking research efforts that cross the broad array of disciplines encapsulated by SICB and move organismal biology in new directions (1) genotype–phenotype relationships, (2) integrating living and physical systems, (3)

utilizing functional diversity, (4) organism-environment linkages, (5) evolutionary stability versus change, (6) how non-model organisms work, (7) garnering public support for organismal biology, (8) transforming organismal biology into 21st century science, (9) fostering interdisciplinary and cross-disciplinary research to yield emergent principles about organisms, (10) community research efforts in addressing GCOB, and (11) the predictive power of organismal biology in the context of ecological and evolutionary change.

Implementing GCOBs At the 2010 SICB annual meeting a workshop was held to initiate a dialog across organismal biology

ß The Author 2011. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. [br]For permissions please email: [email protected]

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that focused on how to address 55 the GCOBs articulated by SICB (Tsukimura et al., 2010). A number of presentations were made by Executive Committee members of SICB and other pro- 60 fessional societies to stimulate discussion. Major requirements for implementation, including bridging research fields and new interdisciplinary approaches to 65 education, were discussed at length. Recommendations resulting from that workshop included establishment of interdisciplinary integrative research cooperatives 70 as a means of increasing activity between large and small research laboratories and expanding coordinated research efforts beyond NIH-listed model organisms, fa- 75 cilitated by sequencing the genomes of a wider range of organisms. Much discussion centered on overcoming the vast educational challenges to prepare 80 our students to become the scientists able and ready to take on the challenges of interdisciplinary integrative research spanning organismal biology and genomics. 85 Participants recognized that to overcome that challenge, significant shifts in the mechanics of our educational efforts may be required. Scientific communication 90 at all levels from colleagues to the general public needs improvement. Sharing of information and cooperation (not competition) must be encouraged. Training 95 (and re-training) scientists to enable them to access changing technology and approaches should be facilitated. We may need to make difficult decisions 100 about whether ‘‘context’’ or ‘‘content’’ is more important for educational objectives that prepare students for future research environments. Participants agreed that 105 a mechanism for developing an umbrella coalition is needed to maintain discussion throughout

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the year. Outcomes from the 2010 workshop that stood out as important elements that will allow us to address the grand challenges were increased awareness of the grand challenges and identified foci, integration and education. At the 2011 SICB meeting, a second GCOB workshop was organized with the primary objective of engaging SICB members in productive breakout discussions to focus our effort to develop a plan or plans for implementation of grand challenges, and to move this process forward at a more rapid pace. SICB is not the only society with members that are organismal biologists, but SICB as a whole possesses the breadth of research approaches required to address many of the GCOBs. However, the complexity of GCOB questions requires novel collaborations and attitudes about organismal biology’s contributions to science and society. SICB is well-poised to play a leadership role among organismal biologists in addressing GCOBs because of the broad expertise in our society and commitment reflected by our membership. Organismal biologists, such as those in SICB, have the opportunity to shape their own destiny with respect to NSF’s long-term plans for funding in organismal biology. To develop our future, we must join in a broadly accepted vision of our research arenas at least 5–10 years into the future. We must do more than define GCOB questions: we must organize a vision for how to marshal the expertise, financial support, research facilities, and communication channels needed to address the GCOB questions in ways that will be productive and that will continue to keep our efforts in organismal biology fresh and forward-thinking. At the 2011 GCOB workshop,

participants were challenged to become involved in thinking hard about the future of organismal biology, and developing a community-based approach to meet the grand challenges.

Grand-challenge strategies in other scientific communities The 2011 SICB GCOB workshop opened with a review of how previous efforts had unfolded. Other scientific communities have moved forward in addressing their own grand-challenge research objectives. In many cases, major research programs have resulted from coordinated efforts that involve building community interest, articulating that interest in a series of workshops and white papers, and consolidation of focus by the community to address specific scientific goals and identify (and obtain) required resources to reach those goals. For example, the systematics community initiated the ‘‘A Tree of Life (AToL)’’ program with the initial goal to identify evolutionary relationships among as many organisms as possible, especially at higher levels of organization, and in doing so address fundamental and important problems in ecology, agriculture, human health and society, and development of bioinformatic resources. The current focus among systematic biologists is a mission to assess and map as much of the Earth’s biodiversity as possible, thereby informing conservation efforts to preserve that biodiversity. The molecular biology community involved in plant sciences worked together beginning in the 1990s to launch an initiative to sequence the genomes of Arabidopsis (the primary model species for plant biology) and all of the major crop plants. While not every plant biologist

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participated, there was over- 55 whelming support from the community in this initiative. In response, NSF launched a series of requests for proposal initiatives beginning in 1998 and including 60 the Plant Genome Research Program, the National Plant Genome Initiative, GenomeEnabled Plant Research, Transferring Research from 65 Model Systems, Tools and Resources for Plant Genome Research, and for fiscal year 2010, Comparative Plant Genome Sequencing. In 2000, the 70 Arabidopsis research community proposed the ‘‘Arabidopsis 2010’’ project involving the determination of the function of every gene in the Arabidopsis genome 75 by 2010. The plant community is now working on their next large vision, the 2020 project, as articulated in white papers (Raikhel, 2008). More recently, the plant 80 biology community has launched the ‘‘iPlant collaborative,’’ a cybernetwork designed to help plant biologists develop interdisciplinary integrative research to ad- 85 dress grand challenges in plant biology (http://www.iplantcolla borative.org). Software engineers at iPlant work to develop cyberinfrastructure including ‘‘Discovery 90 Environments’’ to help biologists work on grand challenges. iPlant cyber-resources are allocated by a community-representative iPlant board of directors. Members of 95 the ecology and environmental biology community have launched a series of initiatives aimed at solving large-scale grand challenges. In the early 1990s, the 100 Sustainable Biosphere Initiative was launched by ESA and resulted in a series of workshops and white papers that presented a 10-year outlook for ecological sciences. 105 Centers and institutes including the National Center for Ecological Analysis and Synthesis

(NCEAS), the National Evolutionary Synthesis Center (NESCent), and the National Institute for Mathematical and Biological Synthesis (NIMBios) have all shaped the way in which ecologists frame and address grand-challenge-scale questions. In recent years, the ecology and evolutionary biology community has published a new set of white papers to define the future of these centers. Presently there is a new competition for the nextgeneration of a national environmental synthesis center that will stimulate research, education and outreach at the interface of the biological, geological and social sciences. Organismal biologists are now in the early stages in developing community-wide initiatives such as those undertaken by the systematics community, plant biologists, and ecological and evolutionary biology communities. We have articulated ideas about grand challenges in organismal biology through SICB workshops and synthetic white papers (Denny and Helmuth, 2009; Denver et al., 2009; Satterlie et al., 2009; Schwenk et al., 2009; Evans et al., 2010; Mykles et al., 2010; Robinson et al., 2010; Sih et al., 2010). A group of organismal animal biologists with primary affiliation in the American Physiological Society (APS) held a workshop in 2007 to discuss developing a National Center Network for Physiological Research, Integration, Synthesis and Modeling (PRISM). The stated goals of PRISM (Carey, 2007) were broad and forward-looking, but PRISM’s initial efforts were directed toward development of a center for research on the physiology of large mammals so as to preserve and maintain present expertise, not to develop a dynamic future for

organismal biology. PRISM’s initial efforts have not gained traction, but discussion of PRISM at the April, 2011 APS may substantially shift the present goals of PRISM. We hope to see increased discussion among organismal biologists allied with SICB and APS so that we can work together on scientist-based, not scientificsociety-based approaches to developing the resources necessary to address GCOBs.

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How to start addressing GCOBs? To encourage discussion of how a research community could meet GCOBs, a strawman framework was presented for how to progress from a GCOB idea to garnering the research support needed to address the GCOB (Fig. 1). In this plan, SICB Executive Officers would initiate the process by formation of a grand challenge steering committee (GCSC), which would work to identify one focal interdisciplinary GCOB question. The process of moving from that question to a forwardreaching 5–10 year research agenda then involves three design/discussion loops. Loop 1 is a process that involves a small group of selected field-leading scientists, loop 2 involves a broader group of scientists and students, and loop 3 involves a smaller group of scientists working to engage the community of organismal biologists at large and the public, including funding agencies, in the GCOB research agenda. In loop 1 (Fig. 1), the GCSC would identify relevant fields (e.g., biology, physics, mathematics) pertinent to the GCOB question and recruit leadership participants from each of those fields. Those participants would work together to refine the GCOB focal question, produce

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Fig. 1. One proposed approach for initiating the development of SICB-based GCOB-implementation plan.

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a white paper on novel interdisciplinary approaches to addressing the refined GCOB question, and hold a workshop with additional participants. At the workshop (Fig. 1, loop 2), participants would interact in small subgroups organized to encourage novel interdisciplinary and emergent ideas about how to address the refined GCOB question, identify required resources, and generate a research plan. Subgroups would then be shuffled to generate a new set of interactions among participant, and the process repeated until the GCOB question and approach to addressing the question had been further refined (Fig. 1, loop 3). This workshop would result in a white paper explaining both the process and the outcome. This paper could be used to identify public support for the GCOB question, including networking with representatives from funding agencies and/or foundations. Another white paper would then be issued to communicate how the research

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community would coordinate their efforts in addressing the GCOB question, and this white paper, along with the others could then be used as motivation for funding agencies to launch initiatives to support the sort of work outlined in these workshops. While abstract, members of the audience did find the plan to resonate with their expectation of a process that will ultimately address GCOB questions. As an exemplar of how a community could meet GCOBs, current efforts in ecomechanics, the interface between the fields of ecology and biomechanics, were presented. Researchers in ecology and biomechanics have recently become aware of the potential utility of collaborative interaction, but the scope and direction of these interactions has not been defined. To craft a definition, a workshop [funded by the Partnership for Interdisciplinary Studies of the Coastal Ocean (PISCO)] was held in September 2009 at the Friday Harbor

Laboratories. The outcome of this workshop was a ‘‘manifesto’’ detailing the potential highlights and roadblocks to fully developing the field of ecomechanics. Segments of this manifesto have been published as review articles, and there is the possibility that the entire document (and its ongoing revisions) will be made available online. A second workshop (funded by the Society for Experimental Biology) was held in Cambridge, England, in March of 2011. The output of this workshop will be a special dedicated edition of the Journal of Experimental Biology. The next step for ecomechanics will be to gather feedback, from both biomechanics and ecologists, on the vision spelled out in products of these workshops. The manner in which feedback will be obtained has yet to be determined, but could potentially take advantage of the capabilities of web-based ‘‘social’’ networks. We anticipate that feedback will allow finetuning of the vision for

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ecomechanics, from which research agendas and the necessary funding for such a research focus can be established. 55 5

Participants’ discussion Groups of workshop participants were then tasked with discussing the following two questions: 60

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(1) How should a broad, cohesive and long-term vision for organismal biology research be developed? (2) How can investment in this long-term vision be sustained and stimulated by organismal biologists across all career stages?

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To facilitate small and productive discussion groups, participants were asked to distribute themselves among round tables. In all, there were five discussion groups with 8–10 people in each group. Student scribes recorded the content of discussion. Discussion was observed by SICB executive committee members as well as the director and program officers from the NSF Division of Integrative Organismal Systems. Following discussion, each discussion group was called on to articulate their main thoughts on the two discussion questions.

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Developing a long-term vision

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Ideas that emerged from the discussion of Question 1 involved developing a SICB committee (e.g., akin to the student and postdoctoral affairs committee 95 via the SICB secretariat) that would provide a leadership role in developing GCOB activities. Activities proposed included workshops involving scientists at 100 a range of career stages, broadening interactions with other disciplines in animal biology as well as in fields beyond biology, and

defining/refining a common vision of the future of organismal biology. The plant biology community has effectively organized their Arabidopsis 2010 and Arabidopsis 2020 (Raikhel, 2008) projects around a 10-year research activity plan, and so integrative biologists may be well served by adopting a similar long-range vision to their activities. Workshops should address broad questions (e.g., how do organisms respond to a changing environment) that have the potential to engage organismal biologists from across SICB directorates (as well as other societies such as APS, Society for Developmental Biology, Animal Behavior Society). The format of workshops should encourage cross-fertilization among faculty, post-doctoral fellows and graduate students in brain-storming ideas. At these workshops, participants should feel free to express ideas without fear of intimidation or reproach should their ideas be deemed outrageous. The workshops should be summarized as white papers intended to communicate broadly to interested members of the research community, and could serve as starting documents for cyberspace dialogs on the subject through online forums and wikis. In addition to dialogs, this cyberinfrastructure could also be developed with applications to encourage sharing of data and meta-analyses and the development of networks to coordinate research Broadening interaction with other disciplines was viewed as a component essential for addressing many GCOB research areas. Overcoming communication barriers will allow better crossunderstanding of our fields, especially in terms of mutual understanding of the research challenges and specific questions.

Interdisciplinary approaches aid in merging intellectual approaches and material resources needed to address large challenging questions. Sharing facilities and equipment may improve crossfertilization of ideas by bringing disparate groups together. Interdisciplinary collaborations require improving effectiveness in communicating research topics and rationale for why a given research area is important. There was considerable discussion of what position SICB ought to take regarding the focused study of model versus non-model organisms. The plant biology community was successful in their ultimate goals of crop-plant research by starting with the Arabidopsis genome sequencing project as an initial foray into sequencing a plant genome. Is it possible for SICB scientists to come together in the way that plant biologists have in the development of models that will allow us to address GCOBs from the vantage of integrative and comparative biology? Doing so will allow greater vertical integration among levels of biological complexity, and enhance our understanding, for example, of how relationships between genes and organisms vary in the context of environmental change.

Sustaining a long-term vision by organismal biologists across all career stages Ideas that emerged from discussion of Question 2 principally centered on developing ways to integrate research and educational activities in a focused interdisciplinary setting. An exemplar for how we have successfully done this is the NSF-Polar Programs sponsored Antarctic biology course. This international course

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attracts biologists from across a 55 wide array of disciplines, and has also attracted participants from other scientific disciplines (e.g., engineering), all of whom have an interest in understanding life 60 in the cold (and high and dry). The Antarctic course successfully merges across training stages (from graduate students to senior faculty), and provides an 65 ideal environment for establishment of novel interdisciplinary collaborations. The focal point of this course away from a particular biological problem (e.g., develop- 70 mental biology) to a broader question (e.g., life in the cold) is a key to the engagement of participants and aids in addressing the challenge that scientists from 75 disparate disciplines have difficulty communicating with each other when immersed in their own field. This course helps biologists understand engineers and 80 vice-versa because both groups are put in an environment (literally, Antarctica) where they must think more broadly about what they are doing and why they are 85 doing it. Such opportunities for training may presently be unique to Antarctica, but they could be developed elsewhere and for ad- 90 dressing different grand-challenge questions. Summer courses at biological field stations (e.g., The Marine Biological Laboratory, Woods Hole Oceanographic 95 Institute, Friday Harbor Laboratories, Hopkins Marine Station) have traditionally been wonderful immersion learning environments where students engage 100 in subjects that cannot be effectively taught during a normal academic term. New summer field courses focusing on GCOB questions, and that bring expertise 105 from a wide array of approaches, such as the Antarctic biology course exemplar, could be very

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successful. Course instructors, like those in the Antarctic biology course, would bring their own research expertise to bear and also have the needed perspective to help bridge the disparate fields represented. Potentially, the development of national and/or regional centers for GCOB research could occur at these field stations and part of the center’s mission could be the summer GCOB courses. Such national and regional centers have been quite successful in the European systems where research is focused on a particular set of questions and/or areas (e.g., The Alfred Wegener Institute in Germany is focused on polar marine biology). These centers not only could provide both a place for intellectual exchange and data mining, but also could provide appropriate research facilities for engaging in actual work as required to address the GCOB. The Crary laboratory at McMurdo base in Antarctica provides discussion rooms and wet laboratories for the Antarctic Biology course; that blend is an integral aspect of the development of new collaborative efforts. The centers should provide shared tools and resources and help engage the community in science through effective communication and outreach. To overcome the challenge of educating future generations of scientists such that they can work seamlessly among different scientific disciplines, both within biology and between biology and other fields, we need to develop some novel educational approaches that involve all career stages, especially undergraduate, graduate, and postdoctoral students. Educational efforts in training students to be integrative, interdisciplinary, and to have a broad perspective must start early. Novel undergraduate

majors, and perhaps new types of undergraduate degrees, could be a great way to start. A suggestion was made to establish a new integrative organismal biology graduate student and/or postdoctoral funding opportunity specifically in topics related to addressing grand challenges in organismal biology through interdisciplinary approaches. Participants would be expected to engage in collaborative research between at least two laboratories representing different scientific fields. For example, to understand organism-environment linkages, one of the grand challenges posed by Schwenk et al. (2009), participants could work among laboratories that specialize in biology, geosciences, engineering, mathematics, and/or computer sciences relevant to a specific research question related to the grand challenge. Those laboratories need not be located at the same university, but must have research areas that in combination provide a new and effective way of addressing the GCOB. Graduate fellowships would involve rotations among each of the participant laboratories. Postdoctoral fellowships would also include REU funding so that the postdoctoral scholar would gain experience in mentoring students, and undergraduate students would gain perspective on interdisciplinary approaches during the travel amongst participant laboratories. Cyberinfrastructure will likely play an important role in the successful maintenance of GCOB efforts, especially in facilitating interdisciplinary communication. SICB members and other integrative organismal biologists could launch a site modeled after iPlant in which datasets could be standardized and used in integrative meta-analyses, and through

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which researchers from disparate fields and physical locations 55 could work together to integrate their approaches toward addressing GCOB questions. In addition to iPlant, effective grandchallenges cyberinfrastructure has 60 been developed by research communities in engineering (http:// www.engineeringchallenges.org/) and global health (http://www .grandchallenges.org/), for exam65 ple. The engineering grandchallenges site has interactive polling and discussion forums, as well as dynamic content. Webinars could be organized to engage par70 ticipants in GCOB discussions, and online forums for further discussion organized to enable frequent open communication among organismal biologists 75 specifically centered on GCOB issues. To keep a channel for discussion open, we have established a new website, (http://www.grand challengesinbio.org/). At this site, 80 we have established a forum to continue discussion on questions 1 and 2 from our workshop, as well as other questions involving which of the GCOB questions we 85 ought to be addressing first. Our future directions may well flow from a continued discussion about what process we ought to be following. Finally, when moving forward 90 in a coordinated group effort in seeking public support to transform the ways in which we approach our science, we must be mindful of GCOB questions of social relevance, best approaches in public communication, and 95 strategies for garnering public support. Training in clear communication with policy makers, the media, and the general public is needed for the majority of our lead scientists, and getting 100 that training should be a priority.

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Conclusions We urge the SICB Executive Committee to take interim action and establish the infrastructure needed to proceed with the organization to develop and meet the Grand Challenges in Organismal Biology. As evidenced in this document, a number of useful suggestions about both the challenges and the strategies for meeting them have been presented. Now, leadership must emerge that will organize, prioritize, and activate the efforts. We cannot make progress by concentrating on the Grand Challenges only once a year at our meetings. We recommend that a Grand Challenges Steering Committee of members committed to the effort be appointed immediately with the mandate to determine SICB’s initial foci, establish an action plan, and designate the leaders of each focus group, with the expectation that each group will develop a research or communication activity and seek funding for it. These groups should then report substantive progress at next year’s annual meeting. Only by taking action and developing focus can we begin to determine our future.

Acknowledgments We wish to thank all of the participants of the workshop for their intellectual input into this project.

Funding This project was funded by the National Science Foundation (IOS- 1007750 to B.T.) and the Society for Integrative and Comparative Biology.

References Carey H. 2007. One physiology. The Physiol 50:49–54.

Denny M, Helmuth B. 2009. Confronting the physiological bottleneck: a challenge from ecomechanics. Int Comp Biol 49:197–201. Denver RJ, Hopkins PM, McCormick SD, Propper CR, Riddiford L, Sower SA, Wingfield JC. 2009. Comparative endocrinology in the 21st century. Int Comp Biol 49:339–48. Evans DH, Axelsson M, Beltz B, Burggren W, Castellini M, Clements KD, Crockett L, Gilmour KM, Henry RP, Hirose S, Ip AYK, Londraville R, Lucu C, Poertner H-O, Summers A, Wright P. 2010. Frontiers in aquatic physiology - grand challenge. Front Physiol 1:6. Mykles DL, Ghalambor CK, Stillman JH, Tomanek L. 2010. Grand challenges in comparative physiology: Integration across disciplines and across levels of biological organization. Int Comp Biol 50:6–16. Raikhel N. 2008. 2020 vision for biology: The role of plants in addressing grand challenges in biology. Mol Plant 1:561–3. Robinson GE, Banks JA, Padilla DK, Burggren WW, Cohen CS, Delwiche CF, Funk V, Hoekstra HE, Jarvis ED, Johnson L, Martindale MQ, del Rio CM, Medina M, Salt DE, Sinha S, Specht C, Strange K, Strassmann JE, Swalla BJ, Tomanek L. 2010. Empowering 21st century biology. Bioscience 60:923–30. Satterlie RA, Pearse JS, Sebens KP. 2009. The black box, the creature from the black lagoon, august krogh, and the dominant animal. Int Comp Biol 49:89–92.

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