Casey P. terHorst

THE RISK OF POLYSPERMY IN THREE CONGENERIC SEA URCHINS AND ITS IMPLICATIONS FOR GAMETIC INCOMPATIBILITY AND REPRODUCTIVE ISOLATION

Abstract Developmental failure caused by excess sperm (polyspermy) is thought to be an important mechanism driving the evolution of gamete-recognition proteins, reproductive isolation, and speciation in marine organisms. However, these theories assume that there is heritable variation in the susceptibility to polyspermy and that this variation is related to the overall affinity between sperm and eggs. These assumptions have not been critically examined. We investigated the relationship between ease of fertilization and susceptibility to polyspermy within and among three congeneric sea urchins. The results from laboratory studies indicate that, both within and among species, individuals and species that produce eggs capable of fertilization at relatively low sperm concentrations are more susceptible to polyspermy, whereas individuals and species producing eggs that require higher concentrations of sperm to be fertilized are more resistant to polyspermy. This relationship sets the stage for selection on gamete traits that depend on sperm availability and for sexual conflict that can influence the evolution of gamete-recognition proteins and eventually lead to reproductive isolation.

Evolution of prey in ecological time reduces the effect size of predators in experimental microcosms

Ecologists have long studied the effect of predators on prey population abundance while evolutionary biologists have measured prey trait evolution in response to predation. Ecological and evolutionary processes were generally thought to occur on different time scales, but recent evidence suggests that evolution may alter the ecological effects of predation over the course of ecological experiments. We used a protozoan and its mosquito-larvae predator, naturally found in the water-filled leaves of pitcher plants, to examine the effect of prey evolution on predator-prey interactions. In experiments conducted over 12 days (approximately 50 prey generations, but less than one predator generation), we measured a decrease in the effect of mosquito larvae predators on protozoa prey populations. In a separate set of experiments, we found that the presence of predators corresponded with evolution of smaller cell size and increased population growth rate. In ecological experiments, two situations commonly occur: strong selection pressure applied by the treatment itself and discrepancies in generation times of associate species. Our results suggest that in either situation, the resulting evolutionary patterns may lead to dramatic and important changes in ecological effect size.

FERTILIZATION SUCCESS CAN DRIVE PATTERNS OF PHASE DOMINANCE IN COMPLEX LIFE HISTORIES1

Many algal life cycles alternate between two free‐living generations. Life histories in which the two generations look identical (isomorphic) are common, particularly in the Rhodophyta. Reports of natural populations dominated by one generation of the life history have sought explanation in terms of phase‐specific differences in mortality and reproductive output, yet in many cases identification of these adaptations has been elusive or inconsistent with predictions. We hypothesized that the gametophyte‐to‐sporophyte ratio of ecologically equivalent isomorphs could result from variation in fertilization rate. We developed two models to test this hypothesis: one representing a generalized isomorphic life history and the other specific to red algae with a Polysiphonia‐type life history. Fertilization rate affected the gametophyte‐to‐sporophyte ratio, especially at low fertilization rates. In the general model, gametophytes dominated the population regardless of fertilization rate unless egg production greatly exceeded meiospore production. In the red algal model, phase dominance depended on the combination of fertilization rate and the number of carpospores produced per fertilization. The generational composition of model multiphasic algal populations results from their inherent reproductive characteristics and the dynamic environment to which fertilization and mortality rates are tied.

Evolution in Response to Direct and Indirect Ecological Effects in Pitcher Plant Inquiline Communities

Ecologists have long recognized the importance of indirect ecological effects on species abundances, coexistence, and diversity. However, the evolutionary consequences of indirect interactions are rarely considered. Here I conduct selection experiments and examine the evolutionary response of Colpoda sp., a ciliated protozoan, to other members of the inquiline community of purple pitcher plants (Sarracenia purpurea). I measured the evolution of six traits in response to (1) predation by mosquito larvae, (2) competition from other ciliated protozoans, and (3) simultaneous predation and competition. The latter treatment incorporated both direct effects and indirect effects due to interactions between predators and competitors. Population growth rate and cell size evolved in response to direct effects of predators and competitors. However, trait values in the multispecies treatment were similar to those in the monoculture treatment, indicating that direct effects were offset by strong indirect effects on the evolution of traits. For most of the traits measured, indirect effects were opposed to, and often stronger than, direct effects. These indirect effects occurred as a result of behavioral changes of the predator in the presence of competitors and as a result of reduced densities of competitors in the presence of predators. Incorporating indirect effects provides a more realistic description of how species evolve in complex natural communities.

The relative importance of rapid evolution for plant-microbe interactions depends on ecological context

Evolution can occur on ecological time-scales, affecting community and ecosystem processes. However, the importance of evolutionary change relative to ecological processes remains largely unknown. Here, we analyse data from a long-term experiment in which we allowed plant populations to evolve for three generations in dry or wet soils and used a reciprocal transplant to compare the ecological effect of drought and the effect of plant evolutionary responses to drought on soil microbial communities and nutrient availability. Plants that evolved under drought tended to support higher bacterial and fungal richness, and increased fungal : bacterial ratios in the soil. Overall, the magnitudes of ecological and evolutionary effects on microbial communities were similar; however, the strength and direction of these effects depended on the context in which they were measured. For example, plants that evolved in dry environments increased bacterial abundance in dry contemporary environments, but decreased bacterial abundance in wet contemporary environments. Our results suggest that interactions between recent evolutionary history and ecological context affect both the direction and magnitude of plant effects on soil microbes. Consequently, an eco-evolutionary perspective is required to fully understand plant–microbe interactions.

Quantifying nonadditive selection caused by indirect ecological effects.

In natural biological communities, species interact with many other species. Multiple species interactions can lead to indirect ecological effects that have important fitness consequences and can cause nonadditive patterns of natural selection. Given that indirect ecological effects are common in nature, nonadditive selection may also be quite common. As a result, quantifying nonadditive selection resulting from indirect ecological effects may be critical for understanding adaptation in natural communities composed of many interacting species. We describe how to quantify the relative strength of nonadditive selection resulting from indirect ecological effects compared to the strength of pairwise selection. We develop a clear method for testing for nonadditive selection caused by indirect ecological effects and consider how it might affect adaptation in multispecies communities. We use two case studies to illustrate how our method can be applied to empirical data sets. Our results suggest that nonadditive selection caused by indirect ecological effects may be common in nature. Our hope is that trait-based approaches, combined with multifactorial experiments, will result in more estimates of nonadditive selection that reveal the relative importance of indirect ecological effects for evolution in a community context.

Testing successional hypotheses of stability, heterogeneity, and diversity in pitcher-plant inquiline communities

Succession is a foundation concept in ecology that describes changes in species composition through time, yet many successional patterns have not been thoroughly investigated. We highlight three hypotheses about succession that are often not clearly stated or tested: (1) individual communities become more stable over time, (2) replicate communities become more similar over time, and (3) diversity peaks at mid-succession. Testing general patterns of succession requires estimates of variation in trajectories within and among replicate communities. We followed replicate aquatic communities found within leaves of purple pitcher plants (Sarracenia purpurea) to test these three hypotheses. We found that stability of individual communities initially decreased, but then increased in older communities. Predation was highest in younger leaves but then declined, while competition was likely strongest in older leaves, as resources declined through time. Higher levels of predation and competition corresponded with periods of higher stability. As predicted, heterogeneity among communities decreased with age, suggesting that communities became more similar over time. Changes in diversity depended on trophic level. The diversity of bacteria slightly declined over time, but the diversity of consumers of bacteria increased linearly and strongly throughout succession. We suggest that studies need to focus on the variety of environmental drivers of succession, which are likely to vary through time and across habitats.

Eco‐evolutionary dynamics in plant‐soil feedbacks

Summary In the past decade, ecologists have begun to more fully appreciate the role of evolution in explaining contemporary ecological processes. Evolution is most likely to affect ecological patterns when selection pressure is particularly strong, or when the generation time of at least one interacting species is relatively short. Interactions between plants and soil microbes are an excellent candidate for examining eco–evo interactions because interactions between organisms are tightly knit with the potential for species with relatively short generation times to impose strong selection on one another. Here, we examine the potential for eco–evolutionary dynamics in plant–soil feedbacks (PSFs). Genetic variation in plant traits and subsequent evolution of those traits can affect traits and species composition of soil microbial communities. Soil microbial communities can, in turn, alter the evolutionary trajectory of plant traits. Further, the direction and magnitude of PSFs can affect the plant community, which may alter the selection on plant traits via intra- and interspecific interactions. Finally, we consider how eco-evolutionary feedbacks might enhance or mitigate the effects of PSFs in driving the structure of natural plant communities.

Direct and indirect transgenerational effects alter plant-herbivore interactions

Theory suggests that environmental effects with transgenerational consequences, including rapid evolution and maternal effects, may affect the outcome of ecological interactions. However, indirect effects occur when interactions between two species are altered by the presence of a third species, and can make the consequences of transgenerational effects difficult to predict. We manipulated the presence of insect herbivores and the competitor Medicago polymorpha in replicated Lotus wrangelianus populations. After one generation, we used seeds from the surviving Lotus to initiate a reciprocal transplant experiment to measure how transgenerational effects altered ecological interactions between Lotus, Medicago, and insect herbivores. Herbivore leaf damage and Lotus fecundity were dependent on both parental and offspring environmental conditions. The presence of insect herbivores and Medicago in the parental environment resulted in transgenerational changes in herbivore resistance, but these effects were non-additive, likely as a result of indirect effects in the parental environment. Indirect transgenerational effects interacted with more immediate ecological indirect effects to affect Lotus fecundity. These results suggest that explanations of ecological patterns require an understanding of transgenerational effects and that these effects may be difficult to predict in species-rich, natural communities where indirect effects are prevalent.

The ghost of competition present.

Communities have been viewed as the end product of an assembly process that results in increasing stability through time as progressively better competitors eventually dominate the other species that can emigrate from a regional pool. Previous work has explained species assemblages based on the traits of the successful species. We suggest that the traits of unsuccessful species in the regional pool may also be important for understanding which species are successful in communities. We constructed a simulation model to study what distinguishes stable, uninvasible assemblages from other possible assemblages from a regional pool of species. Our model demonstrates that both the interactions among the successful species and the interactions between these species and unsuccessful species attempting to invade the community contribute significantly to determining success in the final stable community. Understanding the structure of natural communities may require some knowledge of the unobserved “ghost” species that fail to establish in that same community yet still have significant effects on structure.