Selection on fruit traits is mediated by the interplay between frugivorous birds, fruit flies, parasitoid wasps and seed‐dispersing ants

• Published in: Journal of evolutionary biology 2020-07, Vol.33 (7), p.874-886
• Main Authors: Palacio, Facundo X., Siepielski, Adam M., Lacoretz, Mariela V., Ordano, Mariano
• Format: Article
• Language: English
• Subjects: Acromyrmex lundii; Animals; Antagonists; Ants; Biological Evolution; Birds; Cannabaceae - genetics; Celtis ehrenbergiana; Correlation; Crops; Dispersal; Dispersion; Fitness; Food Chain; frugivory; Fruit - genetics; Fruit flies; Fruits; Host-Parasite Interactions; Infestation; Insecta; Life cycles; Multivariate statistical analysis; Mutualism; Parasitoids; plant–animal interactions; Reproductive fitness; Rhagoletotrypeta pastranai; Seed Dispersal; Seeds; Seeds - genetics; selection gradients; Selection, Genetic; Species; Species diffusion; structural equation model; Structural equation modeling; Trophic levels; Ulmaceae - genetics; Utetes anastrephae; Weight
• ISSN: 1010-061X; 1420-9101
• DOI: 10.1111/jeb.13656

Every organism on Earth must cope with a multitude of species interactions both directly and indirectly throughout its life cycle. However, how selection from multiple species occupying different trophic levels affects diffuse mutualisms has received little attention. As a result, how a given species amalgamates the combined effects of selection from multiple mutualists and antagonists to enhance its own fitness remains little understood. We investigated how multispecies interactions (frugivorous birds, ants, fruit flies and parasitoid wasps) generate selection on fruit traits in a seed dispersal mutualism. We used structural equation models to assess whether seed dispersers (frugivorous birds and ants) exerted phenotypic selection on fruit and seed traits in the spiny hackberry (Celtis ehrenbergiana), a fleshy‐fruited tree, and how these selection regimes were influenced by fruit fly infestation and wasp parasitoidism levels. Birds exerted negative correlational selection on the combination of fruit crop size and mean seed weight, favouring either large crops with small seeds or small crops with large seeds. Parasitoids selected plants with higher fruit fly infestation levels, and fruit flies exerted positive directional selection on fruit size, which was positively correlated with seed weight. Therefore, higher parasitoidism indirectly correlated with higher plant fitness through increased bird fruit removal. In addition, ants exerted negative directional selection on mean seed weight. Our results show that strong selection on phenotypic traits may still arise in perceived diffuse species interactions. Overall, we emphasize the need to consider diverse direct and indirect partners to achieve a better understanding of the mechanisms driving phenotypic trait evolution in multispecies interactions. Birds and ants exerted selection pressures on fruit and seed traits, and their selection regimes were influenced by fruit fly infestation and parasitoidism levels. Strong selection may occur in perceived diffuse mutualisms, casting doubt on the long‐held notion that multispecies interactions can only relax selection on phenotypic traits.