Department Fish Ecology and Evolution

Explaining the ecological causes of evolutionary diversification is a major focus of biology, but surprisingly little has been said about the effects of evolutionary diversification on ecosystems^1-3. The number of species in an ecosystem and their traits are key predictors of many ecosystem-level processes, such as rates of productivity, biomass sequestration and decomposition^4,5. Here we demonstrate short-term ecosystem-level effects of adaptive radiation in the threespine stickleback (Gasterosteus aculeatus) over the past 10,000 years. These fish have undergone recent parallel diversification in several lakes in coastal British Columbia, resulting in the formation of two specialized species (benthic and limnetic) from a generalist ancestor⁶. Using a mesocosm experiment, we demonstrate that this diversification has strong effects on ecosystems, affecting prey community structure, total primary production, and the nature of dissolved organic materials that regulate the spectral properties of light transmission in the system. However, these ecosystem effects do not simply increase in their relative strength with increasing specialization and species richness; instead, they reflect the complex and indirect consequences of ecosystem engineering by sticklebacks. It is well known that ecological factors influence adaptive radiation^7,8. We demonstrate that adaptive radiation, even over short timescales, can have profound effects on ecosystems.

At present, the disciplines of evolutionary biology and ecosystem science are weakly integrated. As a result, we have a poor understanding of how the ecological and evolutionary processes that create, maintain, and change biological diversity affect the flux of energy and materials in global biogeochemical cycles. The goal of this article was to review several research fields at the interfaces between ecosystem science, community ecology and evolutionary biology, and suggest new ways to integrate evolutionary biology and ecosystem science. In particular, we focus on how phenotypic evolution by natural selection can influence ecosystem functions by affecting processes at the environmental, population and community scale of ecosystem organization. We develop an eco-evolutionary model to illustrate linkages between evolutionary change (e.g. phenotypic evolution of producer), ecological interactions (e.g. consumer grazing) and ecosystem processes (e.g. nutrient cycling). We conclude by proposing experiments to test the ecosystem consequences of evolutionary changes.

Organisms alter the biotic and abiotic conditions of ecosystems. They can modulate the availability of resources to other species (ecosystem engineering) and shape selection pressures on other organisms (niche construction). Very little is known about how the engineering effects of organisms vary among and within species, and, as a result, the ecosystem consequences of species diversification and phenotypic evolution are poorly understood. Here, using a common gardening experiment, we test whether morphologically similar species and populations of Diaptomidae copepods (Leptodiaptomus ashlandi, Hesperodiaptomus franciscanus, Skistodiaptomus oregonensis) have similar or different effects on the structure and function of freshwater ecosystems. We found that copepod species had contrasting effects on algal biomass, ammonium concentrations, and sedimentation rates, and that copepod populations had contrasting effects on prokaryote abundance, sedimentation rates, and gross primary productivity. The average size of ecosystem-effect contrasts between species was similar to those between populations, and was comparable to those between fish species and populations measured in previous common gardening experiments. Our results suggest that subtle morphological variation among and within species can cause multifarious and divergent ecosystem-effects. We conclude that using morphological trait variation to assess the functional similarity of organisms may underestimate the importance of species and population diversity for ecosystem functioning.

All living organisms modify their biotic and abiotic environment. Niche construction theory posits that organism-mediated modifications to the environment can change selection pressures and influence the evolutionary trajectories of natural populations. While there is broad support for this proposition in general, there is considerable uncertainty about how niche construction is related to other similar concepts in ecology and evolution. Comparative studies dealing with certain aspects of niche construction are increasingly common, but there is a troubling lack of experimental tests of the core concepts of niche construction theory. Here, we propose an operational framework to evaluate comparative and experimental evidence of the evolutionary consequences of niche construction, and suggest how such research can improve our understanding of ecological and evolutionary dynamics in ecosystems. We advocate for a shift toward explicit experimental tests of how organism-mediated environmental change can influence the selection pressures underlying evolutionary responses, as well as targeted field-based comparative research to identify the mode of evolution by niche construction and assess its importance in natural populations.

There is increasing evidence that rapid phenotypic evolution can strongly influence population dynamics, but how are such eco-evolutionary dynamics influenced by the source of trait variation (i.e., genetic variation or phenotypic plasticity)? To investigate this, we used rotifer–algae microcosm experiments to test how the phenotypic and genetic composition of prey populations affect predator–prey population dynamics. We chose four genetically distinct strains of the green alga Chlamydomonas reinhardtii that varied in their growth rate, standing levels of defense, and inducible defense. To additionally test for strain specificity of plasticity responses, we quantified protein expression of each strain in the presence and absence of rotifer predators (Brachionus calyciflorus). We then tested how different strain combinations influenced the outcome of pairwise competition trials with and without rotifer predation. We tracked individual strain frequencies using quantitative polymerase chain reaction (qPCR), and compared the observed dynamics to a suite of eco-evolutionary models of varying complexity. We found that variation in trade-offs between growth and defense between algal strains strongly influenced the outcome of competition and the overall predator–prey dynamics. Our purely ecological model of the observed dynamics, which allowed for the presence of phenotypic plasticity but no trait variation between strains, never outperformed any of our eco-evolutionary models in which strains could have different trait values. Our best fitting eco-evolutionary model allowed strains to differ in an inducible defense trait. Overall, our results provide some of the first experimental evidence that variation in phenotypically plastic responses among prey genotypes can be an important component of eco-evolutionary dynamics in a predator–prey system.

Phenotypic differences among closely related populations and species can cause contrasting effects on ecosystems; however, it is unknown whether such effects result from genetic divergence, phenotypic plasticity, or both. To test this, we reared sympatric limnetic and benthic species of whitefish from a young adaptive radiation in a common garden, where the benthic species was raised on two distinct food types. We then used these fish in a mesocosm experiment to test for contrasting ecosystem effects of closely related species and of plastically induced differences within a species. We found that strong contrasting ecosystem effects resulted more frequently from genetic divergence, although they were not stronger overall than those resulting from phenotypic plasticity. Overall, our results provide evidence that genetically based differences among closely related species that evolved during a young adaptive radiation can affect ecosystems, and that phenotypic plasticity can modify the ecosystem effects of such species.

Evolution by niche construction occurs when organism-mediated modification of the environment causes an evolutionary response. Physicists have postulated that evolution in general, and evolution mediated via feedbacks between organisms and their environment in particular (i.e. evolution by niche construction), could increase the capacity of biological systems to dissipate free energy in an open thermodynamic system, and help them maintain a state far from thermodynamic equilibrium. Here, we propose using the bacterium Pseudomonas fluorescens (strain SBW25) as a model system to experimentally test theories in both evolutionary biology (e.g. niche construction) and physics (e.g. dissipative systems theory). P. fluorescens rapidly and predictably evolves multiple strategies for exploiting oxygen in unmixed culture flasks. This evolutionary dynamic is mediated by feedbacks between the modification of the oxygen gradient by P. fluorescens and the ecological and evolutionary responses of Pseudomonas to modified environmental conditions. To confirm this, we experimentally manipulated two aspects of the system that influence the strength of the feedback between P. fluorescens and oxygen gradients in the system. First, we inhibited the metabolism of the strain used to inoculate the cultures, and, second, we disturbed the formation of mats at the air–liquid interface. Overall, we found convincing experimental evidence of evolution by niche construction, and conclude that this study system is amenable to experimental investigations of both niche construction and dissipative systems theory.

Summary Differences in how organisms modify their environment can evolve rapidly and might influence adaptive population divergence [1, 2]. In a common garden experiment in aquatic mesocosms, we found that adult stickleback from a recently diverged pair of lake and stream populations had contrasting effects on ecosystem metrics. These modifications were caused by both genetic and plastic differences between populations and were sometimes comparable in magnitude to those caused by the presence/absence of stickleback. Lake and stream fish differentially affected the biomass of zooplankton and phytoplankton, the concentration of phosphorus, and the abundance of several prey (e.g., copepods) and non-prey (e.g., cyanobacteria) species. The adult-mediated effects on mesocosm ecosystems influenced the survival and growth of a subsequent generation of juvenile stickleback reared in the same mesocosms. The prior presence of adults decreased the overall growth rate of juveniles, and the prior presence of stream adults lowered overall juvenile survival. Among the survivors, lake juveniles grew faster than co-occurring stream juveniles, except in mesocosm ecosystems previously modified by adult lake fish that were reared on plankton. Overall, our results provide evidence for reciprocal interactions between ecosystem dynamics and evolutionary change (i.e., eco-evolutionary feedbacks) in the early stages of adaptive population divergence.

Despite a conceptual understanding that evolution and species interactions are inextricably linked, it remains challenging to study ecological and evolutionary dynamics together over long temporal scales. In this review, we argue that, despite inherent challenges associated with reconstructing historical processes, the interplay of ecology and evolution is central to our understanding of macroevolution and community coexistence, and cannot be safely ignored in community and comparative phylogenetic studies. We highlight new research avenues that foster greater consideration of both ecological and evolutionary dynamics as processes that occur along branches of phylogenetic trees. By promoting new ways forward using this perspective, we hope to inspire further integration that creatively co-utilizes phylogenies and ecological data to study eco-evolutionary dynamics over time and space.

Host resistance to parasites is a rapidly evolving trait that can influence how hosts modify ecosystems. Eco-evolutionary feedbacks may develop if the ecosystem effects of host resistance influence selection on subsequent host generations. In a mesocosm experiment, using a recently diverged (<100 generations) pair of lake and stream three-spined sticklebacks, we tested how experimental exposure to a common fish parasite (Gyrodactylus spp.) affects interactions between hosts and their ecosystems in two environmental conditions (low and high nutrients). In both environments, we found that stream sticklebacks were more resistant to Gyrodactylus and had different gene expression profiles than lake sticklebacks. This differential infection led to contrasting effects of sticklebacks on a broad range of ecosystem properties, including zooplankton community structure and nutrient cycling. These ecosystem modifications affected the survival, body condition, and gene expression profiles of a subsequent fish generation. In particular, lake juvenile fish suffered increased mortality in ecosystems previously modified by lake adults, whereas stream fish showed decreased body condition in stream fish-modified ecosystems. Parasites reinforced selection against lake juveniles in lake fish-modified ecosystems, but only under oligotrophic conditions. Overall, our results highlight the overlapping timescales and the interplay of host-parasite and host-ecosystem interactions. We provide experimental evidence that parasites influence host-mediated effects on ecosystems and, thereby, change the likelihood and strength of eco-evolutionary feedbacks.

Dynamic interactions between ecological conditions and the phenotypic composition of populations likely play an important role in evolution, but the direction and strength of these feedbacks remain difficult to characterize. We investigated these dynamics across two generations of threespine sticklebacks from two evolutionary lineages undergoing secondary contact and hybridization. Independently manipulating the density and lineage of adults in experimental mesocosms led to contrasting ecosystem conditions with strong effects on total survival in a subsequent generation of juveniles. Ecosystem modifications by adults also varied the strength of selection on competing hybrid and non-hybrid juveniles. This variation in selection indicated (1) a negative eco-evolutionary feedback driven by lineage-specific resource depletion and dependence and (2) a large performance advantage of hybrid juveniles in depleted environments. This work illustrates the importance of interactions between phenotype, population density and the environment in shaping selection and evolutionary trajectories, especially in the context of range expansion with secondary contact and hybridization.

There is increasing evidence that closely related species have contrasting ecosystem effects, but very little is known about the temporal scale of these effects. When organisms' ecosystem-effects persist beyond or emerge after their presence in the ecosystem, this might increase the potential for eco-evolutionary feedbacks to accompany evolutionary diversification. Here we studied lab-raised whitefish of a benthic-limnetic species pair from a postglacial adaptive radiation to test whether closely related species have contrasting effects on mesocosm ecosystems (hereafter ecosystem effects). We found that the presence of whitefish (ecological effect) had strong effects on some ecosystem components, for example by reducing snail and mussel abundance and increasing phytoplankton abundance. Whitefish species had contrasting effects (evolutionary effect) on benthic algal cover, dissolved organic carbon, and zooplankton community composition, but these effects only emerged several months after whitefish were removed from the ecosystem. The effects of plasticity and the interactive effects of species and plasticity were relatively weak and, with one exception, not significant. Ecological and evolutionary effect sizes were uncorrelated over both phases of the experiment, as were effect sizes between phases for both ecological and evolutionary contrasts. Overall, our results suggest that adaptive radiation can have effects on the structure and functioning of ecosystems, but that the temporal dynamics and mechanistic basis of these effects are insufficiently understood.

Evolution is a fundamental ecosystem process. The study of genomic variation of organisms can not only improve our understanding of evolutionary processes, but also of contemporary and future ecosystem dynamics. We argue that integrative research between the fields of genomics and ecosystem ecology could generate new insights. Specifically, studies of biodiversity and ecosystem functioning, evolutionary rescue, and eco-evolutionary dynamics could all benefit from information about variation in genome structure and the genetic architecture of traits, whereas genomic studies could benefit from information about the ecological context of evolutionary dynamics. We propose new ways to help link research on functional genomic diversity with (reciprocal) interactions between phenotypic evolution and ecosystem change. Despite numerous challenges, we anticipate that the wealth of genomic data being collected on natural populations will improve our understanding of ecosystems.

Biological systems consist of elements that interact within and across hierarchical levels. For example, interactions among genes determine traits of individuals, competitive and cooperative interactions among individuals influence population dynamics, and interactions among species affect the dynamics of communities and ecosystem processes. Such systems can be represented as hierarchical networks, but can have complex dynamics when interdependencies among levels of the hierarchy occur. We propose integrating ecological and evolutionary processes in hierarchical networks to explore interdependencies in biological systems. We connect gene networks underlying predator–prey trait distributions to food webs. Our approach addresses longstanding questions about how complex traits and intraspecific trait variation affect the interdependencies among biological levels and the stability of meta-ecosystems.

1. Theoretical models pertaining to feedbacks between ecological and evolutionary processes are prevalent in multiple biological fields. An integrative overview is currently lacking, due to little crosstalk between the fields and the use of different methodological approaches.
2. Here, we review a wide range of models of eco‐evolutionary feedbacks and highlight their underlying assumptions. We discuss models where feedbacks occur both within and between hierarchical levels of ecosystems, including populations, communities and abiotic environments, and consider feedbacks across spatial scales.
3. Identifying the commonalities among feedback models, and the underlying assumptions, helps us better understand the mechanistic basis of eco‐evolutionary feedbacks. Eco‐evolutionary feedbacks can be readily modelled by coupling demographic and evolutionary formalisms. We provide an overview of these approaches and suggest future integrative modelling avenues.
4. Our overview highlights that eco‐evolutionary feedbacks have been incorporated in theoretical work for nearly a century. Yet, this work does not always include the notion of rapid evolution or concurrent ecological and evolutionary time scales. We show the importance of density‐ and frequency‐dependent selection for feedbacks, as well as the importance of dispersal as a central linking trait between ecology and evolution in a spatial context.

There is growing concern over tipping points arising in ecosystems because of the crossing of environmental thresholds. Tipping points lead to abrupt and possibly irreversible shifts between alternative ecosystem states, potentially incurring high societal costs. Trait variation in populations is central to the biotic feedbacks that maintain alternative ecosystem states, as they govern the responses of populations to environmental change that could stabilize or destabilize ecosystem states. However, we know little about how evolutionary changes in trait distributions over time affect the occurrence of tipping points and even less about how big-scale ecological shifts reciprocally interact with trait dynamics. We argue that interactions between ecological and evolutionary processes should be taken into account in order to understand the balance of feedbacks governing tipping points in nature.

Species interactions lie at the heart of many theories of macroevolution, from adaptive radiation to the Red Queen. Although some theories describe the imprint that interactions will have over long time scales, we are still missing a comprehensive understanding of the effects of interactions on macroevolution. Current research shows strong evidence for the impact of interactions on macroevolutionary patterns of trait evolution and diversification, yet many macroevolutionary studies have only a tenuous relationship to ecological studies of interactions over shorter time scales. We review current research in this area, highlighting approaches that explicitly model species interactions and connect them to broad‐scale macroevolutionary patterns. We also suggest that progress has been made by taking an integrative interdisciplinary look at individual clades. We focus on African cichlids as a case study of how this approach can be fruitful. Overall, while the evidence for species interactions shaping macroevolution is strong, further work using integrative and model‐based approaches is needed to spur progress towards understanding the complex dynamics that structure communities over time and space.