Modelling inducible defences in predator-prey interactions: assumptions and dynamical consequences of three distinct approaches.

Inducible defences against predation are widespread in the natural world, allowing prey to economise on the costs of defence when predation risk varies over time or is spatially structured. Through interspecific interactions, inducible defences have major impacts on ecological dynamics, particularly predator-prey stability and phase lag. Researchers have developed multiple distinct approaches, each reflecting assumptions appropriate for particular ecological communities. Yet, the impact of inducible defences on ecological dynamics can be highly sensitive to the modelling approach used, making the choice of model a critical decision that affects interpretation of the dynamical consequences of inducible defences. Here, we review three existing approaches to modelling inducible defences: Switching Function, Fitness Gradient and Optimal Trait. We assess when and how the dynamical outcomes of these approaches differ from each other, from classic predator-prey dynamics and from commonly observed eco-evolutionary dynamics with evolving, but non-inducible, prey defences. We point out that the Switching Function models tend to stabilise population dynamics, and the Fitness Gradient models should be carefully used, as the difference with evolutionary dynamics is important. We discuss advantages of each approach for applications to ecological systems with particular features, with the goal of providing guidelines for future researchers to build on.

Melanism protects alpine zooplankton from DNA damage caused by ultraviolet radiation.

Melanism is widely observed among animals, and is adaptive in various contexts for its thermoregulatory, camouflaging, mate-attraction or photoprotective properties. Many organisms exposed to ultraviolet radiation show increased fitness resulting from melanin pigmentation; this has been assumed to result in part from reduced UV-induced damage to DNA. However, to effectively test the hypothesis that melanin pigmentation reduces UV-induced DNA damage requires quantification of UV-specific DNA damage lesions following UV exposure under controlled conditions using individuals that vary in pigmentation intensity. We accomplished this using alpine genotypes of the freshwater microcrustacean Daphnia melanica, for which we quantified cyclobutane pyrimide dimers in DNA, a damage structure that can only be generated by UV exposure. For genotypes with carapace melanin pigmentation, we found that individuals with greater melanin content sustained lower levels of UV-induced DNA damage. Individuals with more melanin were also more likely to survive exposure to ecologically relevant levels of UV-B radiation. Parallel experiments with conspecific genotypes that lack carapace melanin pigmentation provide additional support for our conclusion that melanism protects individuals from UV-induced DNA damage. Finally, within-genotype comparisons with asexually produced clonal siblings demonstrate that melanin content influences DNA damage even among genetically identical individuals raised in the same environment.

Divergence in DNA photorepair efficiency among genotypes from contrasting UV radiation environments in nature.

Populations of organisms routinely face abiotic selection pressures, and a central goal of evolutionary biology is to understand the mechanistic underpinnings of adaptive phenotypes. Ultraviolet radiation (UVR) is one of earth's most pervasive environmental stressors, potentially damaging DNA in any organism exposed to solar radiation. We explored mechanisms underlying differential survival following UVR exposure in genotypes of the water flea Daphnia melanica derived from natural ponds of differing UVR intensity. The UVR tolerance of a D. melanica genotype from a high-UVR habitat depended on the presence of visible and UV-A light wavelengths necessary for photoenzymatic repair of DNA damage, a repair pathway widely shared across the tree of life. We then measured the acquisition and repair of cyclobutane pyrimidine dimers, the primary form of UVR-caused DNA damage, in D. melanica DNA following experimental UVR exposure. We demonstrate that genotypes from high-UVR habitats repair DNA damage faster than genotypes from low-UVR habitats in the presence of visible and UV-A radiation necessary for photoenzymatic repair, but not in dark treatments. Because differences in repair rate only occurred in the presence of visible and UV-A radiation, we conclude that differing rates of DNA repair, and therefore differential UVR tolerance, are a consequence of variation in photoenzymatic repair efficiency. We then rule out a simple gene expression hypothesis for the molecular basis of differing repair efficiency, as expression of the CPD photolyase gene photorepair did not differ among D. melanica lineages, in both the presence and absence of UVR.

Linking genes to communities and ecosystems: Daphnia as an ecogenomic model.

How do genetic variation and evolutionary change in critical species affect the composition and functioning of populations, communities and ecosystems? Illuminating the links in the causal chain from genes up to ecosystems is a particularly exciting prospect now that the feedbacks between ecological and evolutionary changes are known to be bidirectional. Yet to fully explore phenomena that span multiple levels of the biological hierarchy requires model organisms and systems that feature a comprehensive triad of strong ecological interactions in nature, experimental tractability in diverse contexts and accessibility to modern genomic tools. The water flea Daphnia satisfies these criteria, and genomic approaches capitalizing on the pivotal role Daphnia plays in the functioning of pelagic freshwater food webs will enable investigations of eco-evolutionary dynamics in unprecedented detail. Because its ecology is profoundly influenced by both genetic polymorphism and phenotypic plasticity, Daphnia represents a model system with tremendous potential for developing a mechanistic understanding of the relationship between traits at the genetic, organismal and population levels, and consequences for community and ecosystem dynamics. Here, we highlight the combination of traits and ecological interactions that make Daphnia a definitive model system, focusing on the additional power and capabilities enabled by recent molecular and genomic advances.

Adaptation to local ultraviolet radiation conditions among neighbouring Daphnia populations.

Understanding the historical processes that generated current patterns of phenotypic diversity in nature is particularly challenging in subdivided populations. Populations often exhibit heritable genetic differences that correlate with environmental variables, but the non-independence among neighbouring populations complicates statistical inference of adaptation. To understand the relative influence of adaptive and non-adaptive processes in generating phenotypes requires joint evaluation of genetic and phenotypic divergence in an integrated and statistically appropriate analysis. We investigated phenotypic divergence, population-genetic structure and potential fitness trade-offs in populations of Daphnia melanica inhabiting neighbouring subalpine ponds of widely differing transparency to ultraviolet radiation (UVR). Using a combination of experimental, population-genetic and statistical techniques, we separated the effects of shared population ancestry and environmental variables in predicting phenotypic divergence among populations. We found that native water transparency significantly predicted divergence in phenotypes among populations even after accounting for significant population structure. This result demonstrates that environmental factors such as UVR can at least partially account for phenotypic divergence. However, a lack of evidence for a hypothesized trade-off between UVR tolerance and growth rates in the absence of UVR prevents us from ruling out the possibility that non-adaptive processes are partially responsible for phenotypic differentiation in this system.

Variation in circulating corticosterone levels is associated with altitudinal range expansion in a passerine bird.

Organisms frequently need to adjust physiological mechanisms to successfully breed in novel habitats. To explore how some populations physiologically acclimate to novel environmental conditions while others do not, we examine three subspecies of the white-crowned sparrow, Zonotrichia leucophrys. Of these subspecies, Z. l. pugetensis has expanded its breeding range to high altitude over the last 60 years. We investigate physiological acclimation to high altitude conditions by comparing circulating levels of glucocorticoids among Z. l. gambelii, which only breeds at high altitude, Z. l. nuttalli, which only breeds at low altitude, a population of Z. l. pugetensis that breeds at low altitude, and a Z. l. pugetensis population that now breeds at high altitude. Glucocorticoids mediate physiological and behavioral responses to environmental conditions and are constitutively secreted, but can also be released facultatively. We hypothesized that elevation of the glucocorticoid corticosterone (CORT) may facilitate breeding in high altitude environments. We tested this hypothesis by comparing baseline and stress-induced CORT levels of subspecies breeding at low altitude, Z. l. pugetensis and Z. l. nuttalli, to subspecies breeding at high altitude, Z. l. pugetensis and Z. l. gambelii. We found that populations breeding at high altitude exhibit higher baseline and stress-induced levels of CORT. Additionally, we found that Z. l. pugetensis exhibit greater variation in the stress-induced CORT response. These results suggest an importance of modulation of hormonal mechanisms in facilitating breeding in high altitude environments, and that variation in these mechanisms may be associated with facilitating altitudinal range expansion.

Consumer-resource dynamics is an eco-evolutionary process in a natural plankton community.

When traits affecting species interactions evolve rapidly, ecological dynamics can be altered while they occur. These eco-evolutionary dynamics have been documented repeatedly in laboratory and mesocosm experiments. We show here that they are also important for understanding community functioning in a natural ecosystem. Daphnia is a major planktonic consumer influencing seasonal plankton dynamics in many lakes. It is also sensitive to succession in its phytoplankton food, from edible algae in spring to relatively inedible cyanobacteria in summer. We show for Daphnia mendotae in Oneida Lake, New York, United States, that within-year ecological change in phytoplankton (from spring diatoms, cryptophytes and greens to summer cyanobacteria) resulted in consumers evolving increasing tolerance to cyanobacteria over time. This evolution fed back on ecological seasonal changes in population abundance of this major phytoplankton consumer. Oneida Lake is typical of mesotrophic lakes broadly, suggesting that eco-evolutionary consumer-resource dynamics is probably common.

Molecular barcodes detect redundancy and contamination in hairpin-bisulfite PCR.

PCR amplification of limited amounts of DNA template carries an increased risk of product redundancy and contamination. We use molecular barcoding to label each genomic DNA template with an individual sequence tag prior to PCR amplification. In addition, we include molecular 'batch-stamps' that effectively label each genomic template with a sample ID and analysis date. This highly sensitive method identifies redundant and contaminant sequences and serves as a reliable method for positive identification of desired sequences; we can therefore capture accurately the genomic template diversity in the sample analyzed. Although our application described here involves the use of hairpin-bisulfite PCR for amplification of double-stranded DNA, the method can readily be adapted to single-strand PCR. Useful applications will include analyses of limited template DNA for biomedical, ancient DNA and forensic purposes.

Indirect evolutionary rescue: prey adapts, predator avoids extinction.

Recent studies have increasingly recognized evolutionary rescue (adaptive evolution that prevents extinction following environmental change) as an important process in evolutionary biology and conservation science. Researchers have concentrated on single species living in isolation, but populations in nature exist within communities of interacting species, so evolutionary rescue should also be investigated in a multispecies context. We argue that the persistence or extinction of a focal species can be determined solely by evolutionary change in an interacting species. We demonstrate that prey adaptive evolution can prevent predator extinction in two-species predator-prey models, and we derive the conditions under which this indirect evolutionary interaction is essential to prevent extinction following environmental change. A nonevolving predator can be rescued from extinction by adaptive evolution of its prey due to a trade-off for the prey between defense against predation and population growth rate. As prey typically have larger populations and shorter generations than their predators, prey evolution can be rapid and have profound effects on predator population dynamics. We suggest that this process, which we term 'indirect evolutionary rescue', has the potential to be critically important to the ecological and evolutionary responses of populations and communities to dramatic environmental change.

A population-epigenetic model to infer site-specific methylation rates from double-stranded DNA methylation patterns.

Cytosine methylation is an epigenetic mechanism in eukaryotes that is often associated with stable transcriptional silencing, such as in X-chromosome inactivation and genomic imprinting. Aberrant methylation patterns occur in several inherited human diseases and in many cancers. To understand how methylated and unmethylated states of cytosine residues are transmitted during DNA replication, we develop a population-epigenetic model of DNA methylation dynamics. The model is informed by our observation that de novo methylation can occur on the daughter strand while leaving the opposing cytosine unmethylated, as revealed by the patterns of methylation on the two complementary strands of individual DNA molecules. Under our model, we can infer site-specific rates of both maintenance and de novo methylation, values that determine the fidelity of methylation inheritance, from double-stranded methylation data. This approach can be used for populations of cells obtained from individuals without the need for cell culture. We use our method to infer cytosine methylation rates at several sites within the promoter of the human gene FMR1.