Evolutionary plant-pollinator responses to anthropogenic land-use change: impacts on ecosystem services.

Agricultural intensification at field and landscape scales, including increased use of agrochemicals and loss of semi-natural habitats, is a major driver of insect declines and other community changes. Efforts to understand and mitigate these effects have traditionally focused on ecological responses. At the same time, adaptations to pesticide use and habitat fragmentation in both insects and flowering plants show the potential for rapid evolution. Yet we lack an understanding of how such evolutionary responses may propagate within and between trophic levels with ensuing consequences for conservation of species and ecological functions in agroecosystems. Here, we review the literature on the consequences of agricultural intensification on plant and animal evolutionary responses and interactions. We present a novel conceptualization of evolutionary change induced by agricultural intensification at field and landscape scales and emphasize direct and indirect effects of rapid evolution on ecosystem services. We exemplify by focusing on economically and ecologically important interactions between plants and pollinators. We showcase available eco-evolutionary theory and plant-pollinator modelling that can improve predictions of how agricultural intensification affects interaction networks, and highlight available genetic and trait-focused methodological approaches. Specifically, we focus on how spatial genetic structure affects the probability of propagated responses, and how the structure of interaction networks modulates effects of evolutionary change in individual species. Thereby, we highlight how combined trait-based eco-evolutionary modelling, functionally explicit quantitative genetics, and genomic analyses may shed light on conditions where evolutionary responses impact important ecosystem services.

Coevolution of group-living and aposematism in caterpillars: warning colouration may facilitate the evolution from group-living to solitary habits.

BACKGROUND: Animals use diverse antipredator mechanisms, including visual signalling of aversive chemical defence (aposematism). However, the initial evolution of aposematism poses the problem that the first aposematic individuals are conspicuous to predators who have not learned the significance of the warning colouration. In one scenario, aposematism evolves in group-living species and originally persisted due to kin selection or positive frequency-dependent selection in groups. Alternatively, group-living might evolve after aposematism because grouping can amplify the warning signal. However, our current understanding of the evolutionary dynamics of these traits is limited, leaving the relative merit of these scenarios unresolved. RESULTS: We used a phylogenetic comparative approach to estimate phenotypic evolutionary models to enable inferences regarding ancestral states and trait dynamics of grouping and aposematic colouration in a classic model system (caterpillars). We find strong support for aposematism at the root of the clade, and some (but weaker) support for ancestral solitary habits. Transition rates between aposematism and crypsis are generally higher than those between group-living and solitary-living, suggesting that colouration is more evolutionarily labile than aggregation. We also find that the transition from group-living to solitary-living states can only happen in aposematic lineage, suggesting that aposematism facilitates the evolution of solitary caterpillars, perhaps due to the additional protection offered when the benefits of grouping are lost. We also find that the high frequency of solitary, cryptic caterpillars is because this state is particularly stable, in that the transition rates moving towards this state are substantially higher than those moving away from it, favouring its accumulation in the clade over evolutionary time. CONCLUSIONS: Our results provide new insights into the coevolution of colour and aggregation in caterpillars. We find support for an aposematic caterpillar at the root of this major clade, and for the signal augmentation hypothesis as an explanation of the evolution of aposematic, group-living caterpillars. We find that colouration is more labile than aggregation behaviour, but that the combination of solitary and cryptic habits is particularly stable. Finally, our results reveal that the transitions from group-living to solitary-living could be facilitated by aposematism, providing a new link between these well-studied traits.

A theory for investment across defences triggered at different stages of a predator-prey encounter.

We introduce a general theoretical description of a combination of defences acting sequentially at different stages in the predatory sequence in order to make predictions about how animal prey should best allocate investment across different defensive stages. We predict that defensive investment will often be concentrated at stages early in the interaction between a predator individual and the prey (especially if investment is concentrated in only one defence, then it will be in the first defence). Key to making this prediction is the assumption that there is a cost to a prey when it has a defence tested by an enemy, for example because this incurs costs of deployment or tested costs as a defence is exposed to the enemies; and the assumption that the investment functions are the same among defences. But if investment functions are different across defences (e.g. the investment efficiency in making resources into defences is higher in later defences than in earlier defences), then the contrary could happen. The framework we propose can be applied to other victim-exploiter systems, such as insect herbivores feeding on plant tissues. This leads us to propose a novel explanation for the observation that herbivory damage is often not well explained by variation in concentrations of toxic plant secondary metabolites. We compare our general theoretical structure with related examples in the literature, and conclude that coevolutionary approaches will be profitable in future work.

The evolution of variance in sequential defences.

The defences used by organisms against predators display a great degree of variability. Defence phenotypes can differ substantially among individuals of the same species, and a single individual can itself deploy a variety of defences. Here, we use a mathematical model that includes mutation and selection to understand the evolutionary origin of this variability in a population of a species that deploys defences sequentially ("first" and "second" defences). Typically, the first defence evolves to have lower variance, i.e. appears more closely accumulated around the ideal phenotype, than the second defence (even when the breaching the first defence incurs more fitness loss than breaching the second defence with the other parameters the same for both defences). However, if the first defence is much less effective in repelling predators, or is much less tolerant of deviation from the ideal phenotype, then the first defence can evolve to have higher variance than the second. Other factors like mutation strength and the losses in the fitness when each defence fails also influence the defence variance. Larger mutation rate incurs larger equilibrium variances, and when the comparative importance in fitness of one defence increases, then the ratio between the variances of this defence and the other defence decreases. Sequentially acting defences are found in many organisms, so we encourage empirical research to test our theoretical predictions.