Coevolution in mutualistic communities Plants Animals Network structure for a plant-frugivore community in southeastern Spain. Bascompte and Jordano, 2007 Scott L. Nuismer

What is coevolution? "Thus I can understand how a flower and a bee might slowly become, either simultaneously or one after the other, modified and adapted to each other in the most perfect manner, by the continued preservation of all the individuals which presented slight deviations of structure mutually favourable to each other." — Charles Darwin, The Origin of Species Coevolution: Reciprocal evolutionary change in interacting species (Janzen, 1980) Species 1 Species 2

For interacting pairs of species, coevolution: Generates diversity both within and among species – Levels of genetic polymorphism – Phenotypic diversification among populations Drives major evolutionary transitions – Sexual vs. Asexual reproduction – Ploidy level Modulates epidemiological dynamics – Incidence and severity of disease  Coevolution matters for pairs of interacting species

Plants Animals Network structure for a plant-frugivore community in southeastern Spain. But most species interact with many others Bascompte and Jordano, 2007 What role does coevolution play in these complex communities?

Quantifying the impact of coevolution We can answer these questions by developing a simple model… Does coevolution alter trait distributions? Does coevolution alter community function? Does coevolution alter network structure? Question 1: Question 2: Question 3:

A simple model of mutualistic communities Animals Plants Each species is defined by a phenotype distribution and abundance

Traits determine interaction probability Phenotypic matching e.g., Phenology P[Interact] x - y P[Interact] Phenotypic differences (threshold) e.g., Corolla depth – proboscis length, Fruit size – beak size x - y Consider two different functional forms of interaction

Animals Plants Assumes mutualistic communities are organized by single “key” traits Abundance + Traits + P[Interact] = Network structure We want to predict how this network structure evolves

Predicting trait (co)evolution Let’s start by defining individual fitness: Abiotic environment: WAWA Species interactions: Phenotype, z Optimal phenotype,  Assume all interactions are benefical Assume random encounters Focus on only inter-guild interactions Consider interactions mediated by either “matching” or “differences”

Predicting coevolution and community structure: Two complementary approaches Analytical approximation Strong selection Evolving G Fitness Individual based simulation

Does coevolution alter network structure? Does coevolution alter community function? Answering the questions using the model Does coevolution alter trait distributions? Question 1: Question 2: Question 3:

Coevolution causes trait distributions to converge among guilds Coevolution causes trait values to converge within guilds Weak coevolutionModerate coevolution Species mean trait value Frequency within community Species mean trait value Frequency within community Plants Animals Plants Animals Does coevolution alter trait distributions? Case I: Phenotype matching

Coevolution causes animal trait values to increase and plant trait values to decrease (or vice versa) Weak coevolutionModerate coevolution Species mean trait value Frequency within community Species mean trait value Frequency within community Plants Animals Plants Animals Does coevolution alter trait distributions? Case II: Phenotype differences

Does coevolution alter trait distributions? Yes! But the details depend on the functional relationship between plant and animal traits Phenotypic matching e.g., Phenology P[Interact] x - y P[Interact] Phenotypic differences (threshold) e.g., Corolla depth – proboscis length, Fruit size – beak size x - y

Does coevolution alter network structure? Does coevolution alter trait distributions? Does coevolution alter community function? Question 1: Question 2: Question 3: Answering the questions using the model

Study how coevolution influences interaction rate and connectance Low interaction rate and connectance High interaction rate and connectance Does coevolution alter community function?

Phenotype matching Phenotype differences  Coevolution increases the rate of interaction within communities. Why? Average fitness consequences to plants Average fitness consequences to animals Does coevolution alter community function? Interaction rate

Why does coevolution increase interaction rates? Species mean trait value Frequency within community Species mean trait value Frequency within community Proportion Successful interactions Proportion Unsuccessful interactions Plants Animals Plants Animals Trait Evolution: MatchingInteraction rate: Matching Trait Evolution: DifferencesInteraction rate: Differences

Yes. In all cases, mutualistic coevolution increases the rate of interaction and network connectance Low interaction rate and connectance High interaction rate and connectance Coevolution Does coevolution alter community function?

Does coevolution alter trait distributions? Does coevolution alter network structure? Question 1: Question 2: Question 3: Answering the questions using the model

Study how coevolution influences the nestedness of mutualistic communities Low nestednessHigh nestedness Does coevolution alter network structure?

MatchingDifferences Strength of Coevolution What explains these patterns? Strength of Coevolution Nestedness (Plant) Nestedness (Animal) Does coevolution alter network structure?

Case I: Phenotype matching A. Trait distributionsNetwork structure Number of species B. Plants Animals Plants Animals Mean phenotype Number of species IE = N A = N P = IE = N A = N P = Before coevolution After coevolution

Does coevolution alter network structure? Case II: Phenotype differences A. B. Trait distributionsNetwork structure Plants Animals Plants Animals Mean phenotype Number of species IE = 0.90 N A = N P = IE = 0.52 N A = N P = Before coevolution After coevolution

Does coevolution alter network structure? YES! Anti-nestedness & Reciprocal specialization Random community Coevolution (phenotype matching) Coevolution (phenotype differences) Low nestedness & Generalization Random community

Conclusions I Mutualistic coevolution drives rapid shifts in trait distributions Species mean trait value Frequency within community Plants Animals

Conclusions II Mutualistic coevolution increases rates of interaction and the connectance of networks Low interaction rateHigh interaction rate Coevolution

Conclusions III Coevolution drives rapid changes in network structure Before coevolution After coevolution 500 Generations

Acknowledgements Collaborators Funding National Science Foundation Jordi Bascompte Pedro Jordano