Coevolution in mutualistic communities

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

2. What is coevolution? Species 1 Coevolution: Reciprocal evolutionary change in interacting species (Janzen, 1980) Species 2 "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

3. 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

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

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

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

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

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

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

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

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

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

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

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

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

16. Does coevolution alter community function? • Study how coevolution influences interaction rate andconnectance Low interaction rate and connectance High interaction rate and connectance

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

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

19. Does coevolution alter community function? 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

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

21. Does coevolution alter network structure? • Study how coevolution influences the nestednessof mutualistic communities Low nestedness High nestedness

22. Does coevolution alter network structure? Matching Differences Nestedness (Animal) Nestedness (Plant) Strength of Coevolution Strength of Coevolution What explains these patterns?

23. Does coevolution alter network structure? Case I: Phenotype matching Plants Plants Trait distributions Animals Animals Network structure A. IE = 0.061 NA = -8.16 NP = -6.59 Before coevolution Number of species B. IE = 0.134 NA = -28.00 NP = -25.41 After coevolution Number of species Mean phenotype

24. Does coevolution alter network structure? Case II: Phenotype differences Plants Plants Trait distributions Animals Animals Network structure A. IE = 0.52 NA = 31.42 NP = 32.20 Before coevolution Number of species B. IE = 0.90 NA = -9.08 NP = -16.44 After coevolution Number of species Mean phenotype

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

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

27. Conclusions II • Mutualistic coevolution increases rates of interaction and the • connectance of networks Low interaction rate High interaction rate Coevolution

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

29. Acknowledgements Collaborators Jordi Bascompte Pedro Jordano Funding National Science Foundation