Grantee: University of Connecticut, Storrs, CT, USA
Researcher: Mark C. Urban, Ph.D.
Grant Title: Does evolution affect the assembly dynamics of biological communities?
https://doi.org/10.37717/220020277
Program Area: Studying Complex Systems
Grant Type: Research Award
Amount: $449,851
Year Awarded: 2011
Duration: 5 years
Explaining context dependency in natural communities
The biological diversity of life on Earth occupies a mosaic network of environments. Ecologists seek to predict why one species lives in this patch and not another. A century of research in community ecology has revealed few generalities. In many cases, one species dominates one patch but not another one even though the patches share the same environmental conditions. This failure of prediction has led some to speculate that ecology alone cannot explain natural species distributions (1). Where does community ecology go from here? I suggest that a community ecology informed by evolutionary biology will explain the high levels of context dependency observed in diversity patterns. Here I propose manipulative experiments to parameterize and inform emerging theory that lies at the interface of complex adaptive systems research in evolution and ecology.
Historically, ecologists have assumed that evolution occurred too slowly to influence ecological dynamics. This assumption has produced a longstanding gap between evolutionary and ecological thought (2). Yet, evidence increasingly suggests that populations often evolve rapidly in response to strong selection and in concert with ecological dynamics (3-6). Moreover, evolutionary dynamics can interact with ecological dynamics to produce outcomes that cannot be predicted based on each dynamic alone (6,7). Future research that links emerging theory with experiments is necessary to test rapidly developing theoretical predictions and to usher in new community ecology theories originating from the first principles of evolutionary biology (8).
Evolving metacommunity as a doubly complex adaptive system
My colleagues and I recently developed a theoretical framework to understand how evolution influences multiple communities that occur together in a regional landscape -- the so-called evolving metacommunity framework (7,9,10). A metacommunity is a set of biological communities for which migration integrates local dynamics across the larger region to produce emergent effects (11). This ecological concept, however, neglects the potential for evolutionary dynamics. In the same metacommunity, populations can adapt to local conditions as mediated by regional migration (10). The evolving metacommunity combines these two dynamics: populations adapt to local interactions, and migration shapes both ecological and evolutionary dynamics. Metacommunity ecology and metapopulation genetics each individually fulfill the four properties of a complex adaptive system delineated by Holland (12) and clarified for biological systems by Levin (13). Hence, the evolving metacommunity is a doubly complex adaptive system that determines global and regional distributions of genetic and species diversity.
The monopolization effect -- evolutionary context dependence
The monopolization effect has emerged as one of the most important and novel predictions from the evolving metacommunity framework (14,15). A monopolization effect occurs when community assembly depends on a race between local adaptation in the initial colonizing species and the arrival of another species. To illustrate this dynamic, first imagine a new patch generated by a disturbance. The first species to arrive is poorly adapted to local conditions. Other better adapted competing species exist in the metacommunity, but have not yet arrived. If these competitors arrive quickly, then they will outcompete and replace this initial colonist. In this case, the initial traits of the colonizing species will predict the community dynamics as is commonly assumed in traditional community ecology. But now consider what happens if the initial colonist adapts for several generations before the competitor arrives. This local adaptation allows the initial colonist to monopolize available resources and prevent other competing species from colonizing or reaching high abundances. Early colonization and local adaptation now determine community dynamics rather than each species' initial traits because evolution alters these traits. Community assembly thus depends on the outcome of a race between local adaptation and the immigration of pre-adapted species.
The monopolization effect is a new concept in community ecology. Underlying theory has developed in the last three years (7,15,16). We recently showed that monopolization effects can occur under a wide parameter range even if the original colonist only has a few generations to adapt before another colonist arrives (16). We have since expanded this theory to include multiple patches and multiple pre-adapted species in a metacommunity. Even in this conservative case, we observe monopolization effects as long as migration rate is moderate and genetic variation exists to fuel an adaptive response.
Monopolization effects thus offer a potentially general mechanism underlying community assembly dynamics that could explain the high levels of context-dependency observed in natural communities. Monopolization effects also could inform other universal questions such as why sexual reproduction repeatedly evolves despite the demographic cost of producing non-fertile males. Theory on monopolization effects suggests that sexual organisms should originate in regions with high patch disturbance rates because they can re-combine genes to adapt quickly to newly colonized patches. Hence, understanding monopolization effects will reveal if evolution introduces context-dependency into patterns of biological diversity and will contribute to our understanding of the value of sex.
Testing the monopolization effect
Despite its broad potential relevance to understanding community dynamics and species distributions, the monopolization effect has not been tested empirically in realistically complex systems. Therefore, further theoretical developments await insights from tests of existing theory. Here I propose to test multiple predictions in a tractable community of small crustaceans, which play key roles in mediating dynamics between aquatic plants and top predators in lake communities. These species are also conducive to experimental evolution because they have rapid generation lengths. I will focus on the water flea Daphnia pulex, which has become a model organism for both ecological and evolutionary studies (17) and which can be studied under laboratory, semi-natural, and natural field conditions.
I propose experiments to test for monopolization effects in carefully controlled laboratory conditions and in more realistic and complex communities formed in arrays of large outdoor mesocosms. The goal of these experiments is to test existing theoretical predictions and then use insights derived in real systems to inform the further development of this emerging body of theory. In each experiment, I will manipulate the important variables determined from theoretical models thus far: migration rate, pre-adaptation to the novel environment, genetic variance, and sexual or asexual reproduction. I will first establish colonies of D. pulex clones as well as their natural competitor, the water flea Ceriodaphnia reticulata (18), collected from natural ponds. I will then raise clones of both species in each of three temperatures to select for thermal adaptations to each environment. Therefore, I can directly control the genetic variance in the D. pulex colonizing population by altering the number of clones and their laboratory population of origin. I can also manipulate incidence of sex because some D. pulex clones are obligately parthenogenetic (19), allowing contrasts between evolution limited to new mutations versus evolution aided by new genetic variance through sexual recombination.
In the laboratory experiment, I will first introduce D. pulex to a novel hot environment. Then I will introduce C. reticulata at varying time points to simulate different colonization intervals between D. pulex and C. reticulata. I will also vary D. pulex genetic variation and C. reticulata pre-adaptation factorially. Lastly I will use asexual and sexual D. pulex clones to test the value of sex in facilitating rapid adaptation to novel habitats.
I will then expand upon laboratory experiments and conduct experiments in outdoor arrays of 1000-L mesocosms that simulate more realistic aquatic communities. I will create spatial arrays of paired ambient and heated "ponds" at varying distances from source populations of the two species, each adapted to either of the environments. Ponds will be colonized both by source populations of laboratory cultures and natural colonists. By varying distances between target and source ponds, I can test for an effect of inter-patch migration on monopolization effects. If monopolization effects occur, then some ponds will be dominated by the species initially maladapted to that environment.
Monopolization effects in broader context
Species and genetic diversities depend on analogous processes -- the locally homogenizing effect of environmental selection and the disruptive effect of inter-patch migration. Yet these two complex adaptive systems have seldom been united owing to artificial disciplinary boundaries kept in place by independent funding opportunities, journal foci, and departmental distinctions (2,20). Whenever we explore regions of overlap, we discover novel emergent dynamics not predicted by ecology and evolution alone (6). One of these novel dynamics occurs through the monopolization effect. I propose to test if monopolization effects can explain the context-dependency often observed in community ecology. Results will provide the necessary feedback between model and reality to inform the next generation of community ecology theories. If monopolization effects are common as suggested by new theory (16), then results will lead us to a more integrated and accurate community ecology. Monopolization effects have profound implications not only for basic science, but also for applied science, such as predicting how evolution will affect community responses to climate change, counteracting the spread of diverse agricultural pests, and understanding the dynamics between multiple disease agents and the human body.
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