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An article by researchers from Brazil and other countries, published in Nature, combines evolutionary and network theories to calculate how species can co-evolve in large mutualist networks

Since Darwin's theory of natural selection, in the 19th century, it is known that interactions between species can generate responses capable of shaping the planet's biodiversity.

The classic example of coevolution by mutualism involves a parasite and its host. When the first one evolves a new form of attack, the second one develops another type of defense and adapts. However, when it comes to a broad network of interactions with hundreds of species – such as plants pollinated by many insects – it is more difficult to determine what effects drove co-evolution across this network.

In these networks, species that do not interact with each other can still influence species evolution through indirect effects. An example of an indirect effect would be an evolutionary change in a plant caused by one pollinator that ends up leading to evolutionary changes in another pollinator.

New research managed to quantify, for the first time, the weight of indirect interactions in coevolution. The conclusion is that the impact can be much greater than expected.

In the study, published in this October 18 in the journal nature, a group of ecologists and biologists from five institutions – University of São Paulo (USP), State University of Campinas, University of California, Doñana Ecological Station and University of Zurich – combined evolutionary theory and network theory to calculate how species can co-evolve in large mutualism networks.

The researchers, supported by the Foundation for Research Support of the State of São Paulo (Fapesp) , developed a mathematical model to analyze interaction networks and separate the effects of direct and indirect interactions. The studied networks describe the mutualistic interactions that occur in a location, such as the interactions between bees that pollinate flowers by collecting nectar or birds that consume fruits of various plant species and disperse seeds.

The study also brings important results for the adaptation and vulnerability of species in situations of abrupt environmental change.

“The results we obtained with this approach suggest that the relationships between species that do not interact directly with each other may have a greater weight than expected in the co-evolution of species . Surprisingly, the indirect impact is greater for specialist species, those that interact with only one or a few species directly. As an example, we can imagine this process as being analogous to behavioral changes in people mediated by social networks. These changes are often caused by people they do not live with directly, but know through mutual friends,” said Paulo Roberto Guimarães Jr., a professor at USP's Biosciences Institute and the study's main author.

75 ecological networks were analyzed, ranging from very small networks, with about ten species, to structures with more than 300 species interacting with each other. Each network takes place in different places on the planet, in terrestrial and marine environments. To collect the data, the team, formed, in addition to Guimarães, by Mathias Pires (Unicamp), Pedro Jordano (IEG), Jordi Bascompte (University of Zurich) and John Thompson (UC-Santa Cruz) had the collaboration of researchers who previously described the interactions in each network.

With the data in hand, the team divided six types of mutualism categorized into two major classes: intimate mutualisms, the case of interactions between anemones and clownfish that spend practically their entire lives in a single anemone, and mutualisms of multiple partners, such as pollination performed by bees and seed dispersal by vertebrates, which normally establish many interactions with different species in the same place.

The results showed that non-directly interacting species can be just as important as directly interacting species in shaping the evolution of a species. However, the weight of direct and indirect interactions depends on the type of mutualism.

“When the relationship is very close between partners in the same network – as is the case with clownfish and anemones or certain species of ants that live inside trees – what matters most are the direct interactions. This is because these interaction networks are more compartmentalized. So, there aren't that many paths for direct effects to propagate. When the interaction is not so close, indirect effects can have an even greater effect than direct ones on the evolution of a species,” said Mathias Pires, from the Biology Institute at Unicamp, another author of the study.

In a simulation performed with a species-rich seed dispersal network, less than 30% of the selective effects on the specialist species were driven by its direct partners, while the effects of indirect species accounted for around 40%.

A matter of time

One of the clear consequences for the impact of indirect relationships is the greater vulnerability of species in situations of abrupt environmental change. This is because the more important the indirect effects, the slower the process of adapting to changes can be.

“An environmental change that affects one species can generate a ripple effect that spreads to other species that also evolve in response, causing new selective pressures. Indirect effects can create conflicting selection pressures and species can take a long time to adapt to new situations, which can make these species more vulnerable to extinction. In the end, environmental changes can cause changes that are faster than the ability of species immersed in a network to adapt”, said Guimarães.

The quantification of indirect effects in complex networks is a challenge not only for Ecology. Indirect effects are a fundamental component of processes that affect the genetic structure of populations, the financial market, international relations and cultural practices.

“The interesting thing about using this method that we developed is that it can be applied in several areas. The interaction networks approach is transdisciplinary and the tools developed to answer questions about a specific topic in ecology, for example, can be used to study questions about social networks or economics, just be creative”, said Pires.

The article Indirect effects drive coevolution in mutualistic networks (doi:10.1038/nature24273), by Paulo R. Guimarães Jr, Mathias M. Pires, Pedro Jordano, Jordi Bascompte and John N. Thompson, can be read in nature (Click here).