FUNDING AGENCY: National Science Foundation

PROGRAM: Foundations in Integrative Biological Research (FIBR)

TITLE: From Genes to Ecosystems: How do Ecological and Evolutionary Processes Interact in Nature?

INVESTIGATORS: David Reznick (UC Riverside), Joseph Travis (Florida State), Cathy Pringle (University of Georgia), Douglas Fraser (Siena College), Regis Ferriere (University of Arizona), Michael Kinnison (University of Maine), Alex Flecker (Cornell University), Cameron Ghalambor (Colorado State), Jim Gilliam (North Carolina State), Andrew Hendry (McGill University), Paul Bentzen (Dalhousie University), Steve Thomas (University of Nebraska), Don deAngelis (U.S. Geological Survey)

INTELLECTUAL MERIT: While ecological processes are known to drive adaptive evolution, the feedback from adaptive evolution to ecological processes has been explored only in theory and simple model systems. These explorations suggest a potentially profound importance for the feedback from evolution to ecological processes. Yet the importance of adaptive dynamics in natural systems remains to be elucidated; to do so requires a target organism that can display significant evolution in a manageable interval of time in a context where the ecological consequences can be measured. We will, for the first time, experimentally evaluate reciprocal feedbacks between evolution and ecosystem processes and hence evaluate such theory in a natural setting. We do so using a focal species, the guppy (Poecilia reticulata), in which rapid evolution of body size, life histories and other traits have already been documented. Prior results suggest that feedbacks between evolution and ecology are important in this system because some evolutionary changes we have observed are inconsistent with theory that does not include ecological interactions. We propose to transplant guppies from sites where they co-occur with a diversity of predators to streams from which they have been previously excluded by waterfalls and that contain a single predator, Rivulus hartii, then to evaluate ecological and co-evolutionary interactions that result. Rivulus preys on guppies, but guppies also prey on Rivulus and the two species compete. Our experimental setting benefits from additional barrier waterfalls that limit upstream dispersal of guppies, but do not exclude Rivulus, thus providing a built-in control. We also will manipulate light environments of a subset of experimental sites in order to alter basal resources and assess how ecological context influences evolutionary trajectories. Our specific aims are to: 1) evaluate population dynamics, changes in demography, resource utilization, and evolution, both by mean phenotype and genetic lineage, of the introduced guppies 2) similarly characterize Rivulus response to guppy introduction 3) quantify impacts of guppies and Rivulus on lower trophic levels, 4) quantify associated changes in availability and demand for potentially limiting nutrients 5) manipulate primary productivity to evaluate effects of ecosystem context on life history evolution and 6) use our results to further develop eco-evolutionary theory. Research in focal streams will be complemented by experiments conducted in existing artificial channels designed to identify underlying interactions and examine cause-and-effect relationships implied by the introduction experiments. Comparative studies across a wide variety of streams and fish communities will be used to refine experimental results. Methods will include the use of: 1) molecular genetic markers and mark-recapture to assess individual reproductive success and demographic variables, 2) mark-recapture methodologies to characterize population biology of guppies and Rivulus, 3) natural occurring isotopes to assess patterns of resource utilization, 3) electric exclosures to assess effects of fish on lower trophic levels, 4) ecological stoichiometry to examine nutrient imbalance in trophic interactions and 5) isotope tracer experiments to quantify nitrogen flux through ecosystem compartments.

BROADER IMPACTS: Our research program represents the first comprehensive effort to experimentally study ecology and evolution in a natural ecosystem. Because the proposed research explicitly links theory and experimentation in an iterative manner, this work will produce a general conceptual framework that can be applied to other ecosystems. For example, our results will be applicable in conservation biology and the management of exploited populations. Human activity frequently introduces exotic species, reduces abundance of native species, and alters ecosystem processes. Consequences of these changes are often studied in an evolutionarily static framework. We argue that incorporating evolutionary change can improve our understanding of the consequences of human induced changes to the environment. For example, introduced species often are initially restricted in their distribution, then abruptly proliferate to become invasive pests. This change may well be caused by evolution of the invader after it becomes established. As a second example, guppies have served as an evolutionary model for the likely consequences of fishing on commercially exploited fish populations. Commercially exploited fish show phenotypic changes in life histories that parallel the way guppies evolve under predation; they often do not recover or recover very slowly when fishing stops. Two possible reasons for delayed recovery are that exploited populations have evolved and the structure of the ecosystem has changed. The proposed research will substantially improve our ability to incorporate eco-evolutionary interactions into these other disciplines. This research will build a theoretical and operational framework for collaboration across a breadth of biological disciplines.

KEY PERSONNEL

David Reznick (DR - University of California, Riverside): David Reznick is the leading PI on this project and is an evolutionary biologist who has specialized in the empirical study of adaptation. His prior work includes a combination of comparative studies with laboratory and field experiments. He has over 25 years of experience working with guppies on the island of Trinidad. He has developed mark-recapture methods for evaluating the population dynamics of natural populations, quantifying the life history patterns of natural populations, quantifying the genetic components of variation within and among populations in life histories in the laboratory and executing field experiments that have allowed the estimate of the rate of evolution and intensity of selection on life history traits in nature. His contributions will include the execution of the introduction experiments, participation in the evaluation of the population dynamics of the introduced populations of guppies, the comparative and experimental study of life history evolution in Rivulus and laboratory evaluations of the evolution of life history traits. He will host the major outreach programs for undergraduates from minority institutions and will coordinate the complete research effort.
http://www.biology.ucr.edu/people/faculty/Reznick.html

Joseph Travis (JT - Florida State University): Joseph Travis brings nearly 30 years of experience in population biology to the group, with over 20 years focusing on poeciliid fish. His empirical work has included studies of numerical dynamics, predator-prey interactions, community ecology, physiological ecology, population and quantitative genetics, and sexual selection and mating systems. He contributes a broad view of how evolutionary and ecological processes interact, especially with respect to how those processes unfold under different regimes of numerical dynamics. His strength is the design of experimental work for testing assumptions and predictions of theory and in the statistical analysis of observation and experimental data. He brings a broad overview to the group, along with experience across many of the subdisciplines represented by the expertise of the others.
http://bio.fsu.edu/~jtravis/

Catherine Pringle (CP - University of Georgia): Cathy Pringle is a stream ecologist/limnologist who is widely known for her work on species-community-ecosystem linkages that combines field studies and experimental approaches. CP's interdisciplinary collaborations with biogeochemists, hydrologists, and behavioral ecologists have successfully advanced integration across disciplines and she serves as an invited member of the National Center for Ecological Synthesis' Scientific Advisory Board. She has developed innovative experimental techniques to work in running water systems - most notably an electric exclosure technique, by which macrobiota presence and absence is manipulated via an electric field. CP has extensive experience studying stream ecosystems in the US, Costa Rica, and Puerto Rico, and she has worked more recently in Panama, Micronesia and Madagascar. She has served as President of the North American Benthological Society and is an elected US Representative of the International Society of Limnology and Oceanography. CP's contributions will include investigation of the impact of guppy introductions on stream ecosystem properties using an electric exclosure technique to manipulate the presence and absence of fishes in situ. CP will also estimate invertebrate secondary production and use stable isotope and gut analysis techniques to characterize food web configuration in experimental streams.
http://cpringle.myweb.uga.edu/home.html

Douglas Fraser (DF - Siena College) and James Gilliam (JG - North Carolina State University): In combination that two investigators have over 40 years of experience with Trinidad stream ecology, focusing especially on Rivulus hartii. They have published on models and data concerning habitat selection, non-lethal responses to predation, threat-influenced movement, and community ecology, among other topics. They also bring expertise on ontogenetic dietary shifts, various modeling skills, and estimation of demographic parameters via mark-recapture techniques. Finally, they bring expertise in the design and execution of replicated experiments in a field setting, including their replicated, artificial streams built alongside a natural stream located close to our research base.
http://www.siena.edu/biology/faculty/Fraser-FP.asp
http://www4.ncsu.edu/unity/users/j/jfgzo/www/jfgzo.html

Regis Ferriere (RF - University of Arizona) and Donald DeAngelis (DDA - U.S. Geological Survey): Regis Ferriere has fifteen years of experience modeling the interplay of ecological and evolutionary processes. He was one of the pioneers of the mathematical modeling of invasion fitness in structured, density-dependent populations. He also contributed seminal studies of eco-evolutionary feedbacks in communities of coevolving mutualistic species, and in ecosystems including multiple trophic levels and nutrient cycles. He has a strong record of collaborative research with pure and applied mathematicians, which has led him to discover a unifying mathematical framework for modeling the evolutionary dynamics of adaptive traits. His work extends to applications to conservation biology and natural resource management in an evolutionary perspective, and to the empirical evaluation of selection gradients in experimental populations of vertebrates. Don De Angelis is one of the early developers of the individual-based modeling (IBM) approach to populations and communities, and has applied the approach in many models of fish populations. He has also published widely on ecosystem modeling and theory. Most recently, he has used the IBM approach to model possible evolutionarily stable strategies regarding the use of induced defenses by aquatic organisms. (DeAngelis et al., in press). This approach incorporates the feedbacks between the species’s evolutionary traits, its population size, and the abundance of resource and predators of the species and hence is very similar to the theory that will be requied for the current project. RF will collaborate with JT and DDA to develop the ecological model of the study system, derive the selection gradients of the life history traits under consideration, and obtain predictions that will be used to inform the statistical analyses of eco-evolutionary responses to the introduction experiment and canopy manipulation. RF, JT and DDA will coordinate their modeling efforts with the collection of ecosystem data led by CP, AF and ST. The theory will be based on mathematical analysis and numerical simulations that will benefit greatly from DDA’s expertise with IBM. The IBM approach will make it possible to incorporate details on the genetic system provided by the work of CG, MK, AH and PB, that would otherwise be intractable. A model specifically tailored to the study system will be used as a stepping stone toward generalization, with the aim of extending current life history theory to multiple species that interact in their ecosystem network. RF and DDA will broaden the temporal scale of their models to derive predictions on patterns of long-term coevolutionary changes of adaptive traits and ecosystem processes. They will, in collaboration with DR, AH and MK, investigate the consequences of their theory for our general understanding of the pace of adaptive evolution in complex ecosystems. Because RF is also an experienced field biologist, he will participate in components of the field work to the extent that is required for him to gain insights into the dynamics of the natural system. Furthermore, he will play an active role in the design and execution of experiments that evaluate predictions of theory, thereby fostering an active exchange between the empirical and theoretical components of the research.
http://eebweb.arizona.edu/faculty/bios/ferriere.html
http://sofia.usgs.gov/people/deangelis.html

Alex Flecker (AF - Cornell University) and Steven Thomas (ST - Cornell University): Alex Flecker has more than 25 years of experience investigating tropical streams. His prior research includes large-scale experimental manipulations of fish in natural streams coupled with mesocosm studies to characterize multiple trophic level interactions among fish, invertebrates, and primary producers. Steve Thomas has 14 years of experience studying stream ecosystems and is an expert in the use of isotope tracers to quantify nutrient cycling and oxygen mass balance approaches for measuring ecosystem scale metabolic activity. AF and ST are currently working together to examine the importance of fish in modulating ecosystem processes such as nitrogen cycling and primary productivity, and to evaluate the relationship between nutrient supply, organism stoichiometry and ecosystem measures of nutrient demand. Together, AF and ST will coordinate: 1) the evaluation and interpretation of ecological interactions associated with guppy introductions, 2) the use of isotope approaches to understand the importance of resource availability and bottom-up controls over the coarse of early life history evolution, 3) the design and execution of light manipulation experiments that assess the role of ecological context in guppy evolutionary patterns, and 4) oxygen mass balance measurements to quantify variation in stream energy flow over the course of the project.
http://www.eeb.cornell.edu/flecker/flecker.html
http://www.eeb.cornell.edu/Thomas/Thomas%20webpage.htm

Cameron Ghalambor (CG - Colorado State University): Cameron Ghalambor did his post-doctoral work on Trinidadian guppies and was Co-PI with DR on a NSF proposal examining the evolutionary trade-offs between life histories, morphology, swimming performance, and behavior. He is thus intimately familiar with the study system and has extensive experience rearing and maintaining lab populations of guppies. CG’s role in the proposed research will be twofold. First, because of his familiarity with the study sites he will take part in the field component of the research. The field work will primarily involve the capture, marking, and re-sampling of introduced fish. CG and one graduate will travel to Trinidad three times each year to contribute to this part of the proposed work. Second, he will conduct many of the lab assays that will assess the rate of genetic change in the introduced populations. CG has extensive experience carrying out these assays and the appropriate laboratory facilities. These lab assays will be carried out every 9 months and will involve rearing the second generation guppies of wild caught introduced individuals. CG will use two rearing environments to evaluate genetic vs. environmental differences of second generation individuals. The first rearing environment will be isolated 2 gal tanks and focus on the size and age of maturity in males. The second rearing environment will consist of replicated 600gal tanks (see budget justification) that contain either just guppies (control treatment) or guppies and their native predator in an enclosure (predator treatment). CG has successfully used this experimental design to more explicitly evaluate differences between populations in predator induced plasticity.
http://rydberg.biology.colostate.edu/faculty/profile.php?name=Ghalambor

Michael Kinnison (MK - University of Maine): Michael Kinnison is a population/evolutionary biologist with expertise in studying contemporary adaptation in both natural and introduced populations of fishes. MK obtained his PhD in 1999 but already has over 30 publications, including some major works (with AH and others) on measuring and interpreting rates of contemporary evolution in the wild and the role of contemporary evolution in ecology and conservation. He also co-edited (with AH) a volume on contemporary evolution containing collected works by other highly regarded authors. Among other projects, MK has performed research on clinal variation in guppy diversity in North Slope river systems of Trinidad and currently has an active research program to experimentally evaluate the interaction between gene flow and adaptation in natural populations of guppies. This program led MK to developed methods for marking and genotyping individual guppies so that he can evaluate the reproductive contributions of individuals to subsequent generations. MK’s experience with these techniques and with quantifying patterns of contemporary evolution and selection in the wild will be important to several evolutionary elements of our program. In particular, MK will coordinate DNA sampling throughout the guppy introduction experiments, and assist in the mark-recapture and phenotype measurement efforts in the field. He has already successfully executed these same steps as part of his current NSF research program. Following genotyping of guppy samples, MK will assist with pedigree reconstruction (with PB, AH and JT) and will perform animal model estimation of trait inheritance, selection and evolutionary responses in the wild. MK’s pedigree approaches will also allow us to discern aspects of sexual and natural selection influencing early evolution and to look at the process of adaptation both as changes in the mean phenotype of the populations and as the differential contribution of individuals to subsequent generations. Finally, MK will also contribute to the implementation of our stream channel experiments on the ecosystem effects of guppy and Rivulus interactions and help coordinate the development of guppy website modules summarizing our findings (building off a site he already has in construction).
http://kinnison.umaine-biology.net/

12. Andrew Hendry (AH - McGill University): Andrew Hendry shares a similar background to MK in research and in contemporary evolution, as represented by their joint publications. He has field experience with salmon, three-spined sticklbacks, Galapagos finches, and guppies. He has also edited a volume on salmonid fishes that includes chapters on contemporary evolution. Finally, he senior authored a study (2000, Science 290: 516-518) that demonstrates the early evolution of reproductive isolation in an introduced salmon population that had subdivided into local populations with differences in breeding habitat. This diversity of study systems gives him an equally diverse background in ecology and population biology and special insights into the interactions between ecological and evolutionary processes. AH has developed methods for characterizing the stream environments of guppies and quantifying color patterns and shape in photographed field samples of guppies; these same methods will be applied in the current proposal. He also developed theory on the interaction between gene flow and adaptation. He will apply these skills and experience to our characterization of Rivulus and guppies in the introduction experiments, including mark-recapture analyses and will play a major role in the design and execution of complimentary studies of guppies and Rivulus.
http://www.biology.mcgill.ca/faculty/hendry/

Paul Bentzen (PB - Dalhousie University): Paul Bentzen is a leader in applying genetic techniques to the analysis of fitness in natural populations of fish and other aquatic organisms. For example, he has applied genetic markers and parentage analysis to evaluate: 1) the relative fitness of hatchery versus wild salmon, 2) the influence of mating system on reproductive success in salmon and other fishes, and 3) the patterns of survival through the vulnerable larval phases of the life cycle in rainbow smelt. These and other projects share the property of his use of highly variable molecular markers to evaluate reproductive success or survival through different life stages. He has developed microsatellite markers for 15 species of fish and four species of aquatic invertebrates. He has already developed eleven tetranucleotide loci for guppies; others are available from the literature. Tetranucleotide loci have more discrete differences among alleles and can be more readily scored without error. He has also developed the methods to process the fish efficiently and on a large enough scale to yield data on the short time-frame required for our project. He will supervise the processing of all tissue samples, and participate in the parentage analysis. He has already successfully completed a study of this scale on guppies in collaboration with AH and MK.
http://biology.dal.ca/us/f/bentzen/bentzen.html