Indirect interactions may be more significant for species evolution

An article by researchers in Brazil and elsewhere that was published in Nature combines evolutionary and network theory to calculate how species coevolve in large-scale mutualistic networks.

By Maria Fernanda Ziegler  |  Agência FAPESP – Ever since Darwin expounded his theory of natural selection in the nineteenth century, interactions among species have been known to be capable of creating responses that help shape the planet’s biodiversity. 

The classical example of mutualistic coevolution involves a parasite and its host. When the parasite develops a new form of attack, the host adapts to develop a new form of defense. However, in a wider network of interactions involving hundreds of species, such as plants pollinated by many insects, it is harder to know which effects will determine coevolution throughout the network.

In networks such as these, species that do not interact may nevertheless indirectly influence the evolutions of other species. An example of an indirect effect is an evolutionary change in a plant caused by a pollinator that leads to an evolutionary change in another pollinator.

New research has quantified the significance of indirect interactions in coevolution for the first time. The conclusion is that their effects can be much greater than expected.

In the study, published in October in the journal Nature, a group of ecologists and biologists affiliated with five institutions – the University of São Paulo (USP) and the University of Campinas in Brazil, the University of California (UC) in the US, the Doñana Biological Station (EBD) in Spain, and the University of Zurich in Switzerland – combined evolutionary theory and network theory to calculate how species can coevolve in large mutualistic networks.

The researchers, supported by FAPESP, developed a mathematical model to analyze interaction networks and separate the effects of direct interactions from those of indirect interactions. The networks studied describe the mutualisms that occur in an area, such as bees that pollinate flowers by collecting nectar or birds that consume the fruits of various plant species and disperse the seeds.

The study also produced important findings on species adaptations and vulnerabilities in situations of abrupt environmental change.

“The results we obtained with this approach suggest relations among species that don’t interact directly may be more significant than expected for species coevolution,” said Paulo Roberto Guimarães Jr., lead author of the study and professor at the University of São Paulo’s Bioscience Institute (IB-USP) in Brazil. “Surprisingly, the indirect impact is greatest on specialist species, which interact directly with only one or a few other species. We can think of this process as analogous to behavioral changes in human beings mediated by social networks. Such changes are often caused by individuals with whom they don’t interact with directly but know about through friends they have in common.”

The researchers analyzed 75 ecological networks ranging from very small networks with some tens of species to networks with more than 300 interacting species. Each network was located at a different part of the planet, both on land and in the oceans. Data collection was performed by Guimarães, Mathias Pires (UNICAMP), Pedro Jordano (EBD), Jordi Bascompte (University of Zurich) and John Thompson (UC Santa Cruz) as well as other researchers who had previously described the interactions in certain networks.

They found six types of mutualism in the data, which they grouped into two broad classes: intimate mutualisms in which an organism completes at least one life stage on a single host, such as anemones hosting clownfish (Amphiprioninae), and multiple-partner mutualisms in which an individual interacts with multiple partners throughout its life, such as pollination by bees or seed dispersal by vertebrates.

According to the authors, species that do not interact directly can be as important in evolutionary terms as species that do, but the significance of direct and indirect interactions depends on the type of mutualism.

“When the relationship between partners in the same network is very intimate, as in the case of the anemone and clownfish or certain ant species that live inside trees, direct interactions are more relevant because these networks are more compartmentalized and there aren’t so many paths for direct effects to propagate,” said Pires, a scientist at UNICAMP’s Biology Institute and an author of the study. “When the interaction is not intimate, indirect effects may influence the evolution of a species more than direct effects.”

In a simulation involving a species-rich seed dispersal network, less than 30% of the selective effects on specialist species were driven by their direct partners, whereas the combined effects of non-interacting species accounted for approximately 40% of the selective effects on the traits of specialists. 

A matter of time

The significance of indirect relationships clearly includes greater vulnerability of the species concerned to rapid environmental change. The stronger the indirect effects, the slower the process of adapting to change.

“An environmental change that affects a species may have effects that cascade through other species, which also evolve in response, creating new selective pressures. Indirect effects may create conflicting selective pressures, and species may take longer to adapt to new situations, making them more vulnerable to extinction. Ultimately, environmental change may drive alterations that occur at a faster pace than the adaptive capacity of the species in the network,” Guimarães said.

Quantifying indirect effects of interactions in complex networks is not just a challenge for ecology. Indirect effects are a key component of processes that help shape the genetic structures of populations, financial markets, international relations, and cultural practices.

“An interesting facet of the method we developed is that it can be used in many different areas,” Pires said. “The interaction network approach is transdisciplinary, and tools developed to answer questions about a specific point in ecology, for example, can be used to study aspects of social or economic networks. Creativity is all you need.”

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, published in Nature, can be retrieved at the following address: nature.com/articles/doi:10.1038/nature24273.