How different species indirectly interact in nature – 08/10/2023 – Fundamental Science

Who hasn’t been influenced by what a friend of a friend told them? Or at the suggestion of a cousin’s neighbor? In our social circles, we are constantly influenced—and are constantly influencing—in an indirect way.

In social networks, for example, indirect effects guide the diffusion of different behaviors, be it the consumption of alcoholic beverages and drugs, cooperation between individuals, altruism and the perception of happiness in a given population. Indirect effects can also control the spread of contagious diseases, the emergence of innovations in different areas and the interconnection of global markets. In general, every process that propagates through interactions between the elements of a system ultimately depends on indirect effects.

The same thing happens in nature: in an ecological community, thousands of individuals of different species interact. During a simple walk on the campus of the University of São Paulo, when observing butterflies, bees and flies pollinating the flowers, one notices how numerous are the opportunities for indirect influences. For example, a butterfly can deplete or reduce the amount of nectar in a flower and thus harm a bee that will later visit that same flower. In this case, it is an indirect ecological effect mediated by the influence of a species on the density of a resource (nectar) shared with other species.

But species can also be indirectly influenced by evolutionary effects. The butterfly’s ability—to take the example—to consume nectar and pollinate a plant depends on the fit of its proboscis—its sucking mouthparts—to the flower’s pollen tube. Therefore, in a given population, both individuals of that butterfly species and of the plant species whose attributes are adjusted and generate a more efficient interaction, with a greater acquisition of resources by insects, and a greater efficiency of plant pollination, would benefit.

As a consequence, the ecological interaction between the plant and the butterfly can result in selective pressures that favor traits with a higher fit, causing evolutionary changes in both species. If such changes are reciprocal, the phenomenon is defined as coevolution.

But what happens when a third species also co-evolves with the plant, such as certain bees or flies? What if we consider a community with hundreds of plant and pollinator species? It is in these scenarios that indirect evolutionary effects manifest themselves. The challenge, then, is to quantify the magnitude of such effects and identify the consequences for the ecology and evolution of species in the wild. And it is on this challenge that my doctoral research in ecology at USP focuses, under the guidance of biologist Paulo Guimarães Jr.

The work combines mathematical modeling, numerical simulations and empirical data to understand how these indirect evolutionary effects shape the average fitness of a species, which consists of its ability to survive and reproduce. The results showed that, in communities of mutualistic species — those that benefit each other —, indirect evolutionary effects hinder the adaptability of species to the point that many suffer a reduction in their average fitness after co-evolving in a network of interactions. And this came as a surprise, since the direct effects of mutualisms increase the fitness of interacting individuals.

An important implication of this result was the observation of an eventual reduction in the average fitness of the species when some external factor disturbs the community and increases the indirect evolutionary effects. honey bee, Apis mellifera, for example, when introduced into a community, interacts with many plant species, potentiates indirect effects, and may reduce the fitness of other plant species and pollinators. Therefore, the results indicate that invasive species can be disruptive not only in ecological time (decades and centuries), but also over evolutionary time (thousands of years).

I recently published these findings as first author in an article in the journal Nature, which undoubtedly means quite an achievement for us, Brazilian scientists at the beginning of our careers. But to arrive at these results, the time and help of researchers from different areas were crucial.

Our research was carried out over five years, had three different versions, accumulated a folder with more than 12,000 files and brought together a team of nine researchers from four different countries (Brazil, Spain, United States and Switzerland). A true journey. Time was essential to mature the idea, carry out analyzes and refine the manuscript, while the collaborators were fundamental in different stages.

With the geneticist Ana Paula Assis (USP) we learned a lot about evolution and quantitative genetics; physicist Marcus Aguiar (Unicamp) instructed us and solved quantitative problems that at first seemed impossible; ecologist Mathias Pires (Unicamp) guided us in many of the analyzes that deal with the practical implications of the work.

But, once the pieces of the puzzle have been put together and shared with colleagues several “eureka” moments, I see that the real achievement lies in what motivates me and many of the scientists I know: asking, learning and discovering. To paraphrase the physicist Richard Feynman, the prize is in the pleasure of discovering, in the emotion of discovery and in sharing with peers.

Interestingly, I met Richard Feynman in a course I took in my master’s degree, taught by ecologist Sérgio Reis (Unicamp). It was because of this discipline that I spoke to my then co-advisor for the master’s degree, Rodrigo Cogni (USP), about my interest in researching theory in ecology and evolution. Rodrigo Cogni told me about Paulo Guimarães Jr., my current advisor, who told me about our collaborators… As you can see, even my doctoral thesis resulted from a cascade of indirect effects.

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Leandro Giacobelli Cosmo is a doctoral candidate in ecology at the University of São Paulo.

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