Gregor F. Fussmann

Rapid evolution drives ecological dynamics in a predator-prey system

Ecological and evolutionary dynamics can occur on similar timescales. However, theoretical predictions of how rapid evolution can affect ecological dynamics are inconclusive and often depend on untested model assumptions. Here we report that rapid prey evolution in response to oscillating predator density affects predator–prey (rotifer–algal) cycles in laboratory microcosms. Our experiments tested explicit predictions from a model for our system that allows prey evolution. We verified the predicted existence of an evolutionary tradeoff between algal competitive ability and defence against consumption, and examined its effects on cycle dynamics by manipulating the evolutionary potential of the prey population. Single-clone algal cultures (lacking genetic variability) produced short cycle periods and typical quarter-period phase lags between prey and predator densities, whereas multi-clonal (genetically variable) algal cultures produced long cycles with prey and predator densities nearly out of phase, exactly as predicted. These results confirm that prey evolution can substantially alter predator–prey dynamics, and therefore that attempts to understand population oscillations in nature cannot neglect potential effects from ongoing rapid evolution.

Evolution as a critical component of plankton dynamics

Microevolution is typically ignored as a factor directly affecting ongoing population dynamics. We show here that density–dependent natural selection has a direct and measurable effect on a planktonic predator–prey interaction. We kept populations of Brachionus calyciflorus, a monogonont rotifer that exhibits cyclical parthenogenesis, in continuous flow–through cultures (chemostats) for more than 900 days. Initially, females frequently produced male offspring, especially at high population densities. We observed rapid evolution, however, towards low propensity to reproduce sexually, and by 750 days, reproduction had become entirely asexual. There was strong selection favouring asexual reproduction because, under the turbulent chemostat regime, males were unable to mate with females, produced no offspring, and so had zero fitness. In replicated chemostat experiments we found that this evolutionary process directly influenced the population dynamics. We observed very specific but reproducible plankton dynamics which are explained well by a mathematical model that explicitly includes evolution. This model accounts for both asexual and sexual reproduction and treats the propensity to reproduce sexually as a quantitative trait under selection. We suggest that a similar amalgam of ecological and evolutionary mechanisms may drive the dynamics of rapidly reproducing organisms in the wild.

Rapid contemporary evolution and clonal food web dynamics

Character evolution that affects ecological community interactions often occurs contemporaneously with temporal changes in population size, potentially altering the very nature of those dynamics. Such eco-evolutionary processes may be most readily explored in systems with short generations and simple genetics. Asexual and cyclically parthenogenetic organisms such as microalgae, cladocerans and rotifers, which frequently dominate freshwater plankton communities, meet these requirements. Multiple clonal lines can coexist within each species over extended periods, until either fixation occurs or a sexual phase reshuffles the genetic material. When clones differ in traits affecting interspecific interactions, within-species clonal dynamics can have major effects on the population dynamics. We first consider a simple predator–prey system with two prey genotypes, parametrized with data from a well-studied experimental system, and explore how the extent of differences in defence against predation within the prey population determine dynamic stability versus instability of the system. We then explore how increased potential for evolution affects the community dynamics in a more general community model with multiple predator and multiple prey genotypes. These examples illustrate how microevolutionary ‘details’ that enhance or limit the potential for heritable phenotypic change can have significant effects on contemporaneous community-level dynamics and the persistence and coexistence of species.

Community response to enrichment is highly sensitive to model structure.

Biologists use mathematical functions to model, understand and predict nature. For most biological processes, however, the exact analytical form is not known. This is also true for one of the most basic life processes: the uptake of food or resources. We show that the use of several nearly indistinguishable functions, which can serve as phenomenological descriptors of resource uptake, may lead to alarmingly different dynamical behaviour in a simple community model. More specifically, we demonstrate that the degree of resource enrichment needed to destabilize the community dynamics depends critically on the mathematical nature of the uptake function.

EFFECTS OF SUCCESSIONAL DYNAMICS ON METAPOPULATION PERSISTENCE

The classical (Levins) metapopulation scenario envisions a species persisting in a network of habitat patches through a balance between frequent local (within-patch) extinctions and recolonizations. Although this is the dominant paradigm for species in fragmented habitats, empirical support is limited, and it has been argued that very restrictive conditions on migration rates are required: high enough for recolonization to balance extinctions, but low enough that local populations do not fluctuate in synchrony. Through simulation and analysis of a stochastic spatial model, we argue that the likelihood of persistence via the classical scenario is strongly affected by some basic properties of within-patch successional dynamics whose importance has not been emphasized in metapopulation theory: the distribution of successional stage durations, and whether patches are “refractory” vs. immediately available for recolonization after an extinction has occurred. These properties are tied to the biological causes o...

Evolutionary and plastic rescue in multitrophic model communities

Under changing environmental conditions, intraspecific variation can potentially rescue populations from extinction. There are two principal sources of variation that may ultimately lead to population rescue: genetic diversity and phenotypic plasticity. We compared the potential for evolutionary rescue (through genetic diversity) and plastic rescue (through phenotypic plasticity) by analysing their differential ability to produce dynamical stability and persistence in model food webs. We also evaluated how rescue is affected by the trophic location of variation. We tested the following hypotheses: (i) plastic communities are more likely to exhibit stability and persistence than communities in which genetic diversity provides the same range of traits. (ii) Variation at the lowest trophic level promotes stability and persistence more than variation at higher levels. (iii) Communities with variation at two levels have greater probabilities of stability and persistence than communities with variation at only one level. We found that (i) plasticity promotes stability and persistence more than genetic diversity; (ii) variation at the second highest trophic level promotes stability and persistence more than variation at the autotroph level; and (iii) more than variation at two trophic levels. Our study shows that proper evaluation of the rescue potential of intraspecific variation critically depends on its origin and trophic location.

Aquatic primary production in a high-CO2 world

Here, we provide a review of the direct effect of increasing CO2 on aquatic primary producers through its function as a source of carbon, focusing our analysis on the interpretation of this increase as an increase in the availability of a resource. This provides an interesting context to evaluate ecological and evolutionary theories relating to nutrient availability and leads us to: the assessment of theories about limitation of productivity and the integration of CO2 into the co-limitation paradigm; the prediction of community composition and of change in communities from known changes in the environment; and evaluation of the potential for evolutionary adaptation in conditions that increase growth.

Cycles, phase synchronization, and entrainment in single-species phytoplankton populations

Complex dynamics, such as population cycles, can arise when the individual members of a population become synchronized. However, it is an open question how readily and through which mechanisms synchronization-driven cycles can occur in unstructured microbial populations. In experimental chemostats we studied large populations (>109 cells) of unicellular phytoplankton that displayed regular, inducible and reproducible population oscillations. Measurements of cell size distributions revealed that progression through the mitotic cycle was synchronized with the population cycles. A mathematical model that accounts for both the cell cycle and population-level processes suggests that cycles occur because individual cells become synchronized by interacting with one another through their common nutrient pool. An external perturbation by direct manipulation of the nutrient availability resulted in phase resetting, unmasking intrinsic oscillations and producing a transient collective cycle as the individuals gradually drift apart. Our study indicates a strong connection between complex within-cell processes and population dynamics, where synchronized cell cycles of unicellular phytoplankton provide sufficient population structure to cause small-amplitude oscillations at the population level.

Long-term culture at elevated atmospheric CO2 fails to evoke specific adaptation in seven freshwater phytoplankton species

The concentration of CO2 in the atmosphere is expected to double by the end of the century. Experiments have shown that this will have important effects on the physiology and ecology of photosynthetic organisms, but it is still unclear if elevated CO2 will elicit an evolutionary response in primary producers that causes changes in physiological and ecological attributes. In this study, we cultured lines of seven species of freshwater phytoplankton from three major groups at current (approx. 380 ppm CO2) and predicted future conditions (1000 ppm CO2) for over 750 generations. We grew the phytoplankton under three culture regimes: nutrient-replete liquid medium, nutrient-poor liquid medium and solid agar medium. We then performed reciprocal transplant assays to test for specific adaptation to elevated CO2 in these lines. We found no evidence for evolutionary change. We conclude that the physiology of carbon utilization may be conserved in natural freshwater phytoplankton communities experiencing rising atmospheric CO2 levels, without substantial evolutionary change.

Experimental elimination of parasites in nature leads to the evolution of increased resistance in hosts

A reduction in the strength of selection is expected to cause the evolution of reduced trait expression. Elimination of a parasite should thus cause the evolution of reduced resistance to that parasite. To test this prediction in nature, we studied the fourth- and eighth-generation descendants of guppies (Poecilia reticulata) introduced into four natural streams following experimental elimination of a common and deleterious parasite (Gyrodactylus spp.). After two generations of laboratory rearing to control for plasticity and maternal effects, we infected individual fish to assess their resistance to the parasite. Contrary to theoretical expectations, the introduced guppy populations had rapidly and repeatably evolved increased resistance to the now-absent parasite. This evolution was not owing to a resistance-tolerance trade-off, nor to differences in productivity among the sites. Instead, a leading candidate hypothesis is that the rapid life-history evolution typical in such introductions pleiotropically increases parasite resistance. Our study adds a new dimension to the growing evidence for contemporary evolution in the wild, and also points to the need for a re-consideration of simple expectations from host–parasite theory. In particular, our results highlight the need for increased consideration of multiple sources of selection and pleiotropy when studying evolution in natural contexts.