How Evolution Works - Variation Matters in Predator-Prey and Parasite-Host Interactions

Melissa blue butterfly, Lycaeides melissa
Recently colonized alfalfa as a food plant for its caterpillars

Variation Matters: Genetic Effects in Interacting Species Jointly Determine Ecological Outcomes

The greatest diversity of life is not counted in the number of species, but in the diversity of interactions among them, according to the finding of a research group led by evolutionary geneticist, Professor Zachariah Gompert, of the Department of Biology, Utah State University, Logan, UT, USA, a 2019 NSF CAREER Award recipient.

The question the research group sought to answer was to what extent is the interaction between, for example, a microbe and a host is the same for all members of the microbe and host species, or does it vary according to the genetic make-up of the two species?

Not surprisingly, the outcome was that genetic variations in both species affect the interaction. This is, in fact, what so-called Darwinian evolution depends on, as small variations give more or less advantage to both species in an interaction, i.e. as the environment 'selects' for greater or lesser fitness.

For example, a caterpillar that can consume a plant despite any measures the plant might have evolved to deter it, will depend not just on the caterpillar's genetic make-up but also on the genetic make-up of the plant. This is the very stuff of evolutionary arms races in which the competing interests of each species in such a relationship are environmental selectors for the other. A caterpillar better able to consume a plant is a selector for variations in the plant that are better at deterring the caterpillar, and those variations in the plant are selectors for variations in the caterpillar that make it better able to consume the plant.

So the biodiversity between caterpillars and plants is not just between two species, but between the multiple genes that determine the outcome of that interaction.

The group's findings are published in PNAS, sadly behind a paywall, although the abstract is available under a Creative Commons license.

Quoting Professor Gompert, the news release by By Mary-Ann Muffoletto of Utah State University explains the research:

The greatest diversity of life is not counted in the number of species, says Utah State University evolutionary geneticist Zachariah Gompert, but in the diversity of interactions among them.

It’s often unclear if the outcome of an interaction, such as whether a microbe can infect a host, is the same for all members of a species or depends on the genetic makeup of the specific individuals involved

For example, he says, one might ponder why a particular butterfly either can or can’t feed on a particular plant.

Is that affected by the specific genetic makeup of the butterfly or is it the specific genetic makeup of the individual plant? Or is it affected by genetic interactions between the butterfly and plant species?

Gompert and colleagues from University of Nevada, Rice University, University of Wyoming, University of Tennessee, Texas State University and Michigan State University address this knowledge gap through a series of experiments using a recent host-range expansion of alfalfa by the Melissa blue butterfly (Lycaeides melissa). The team reports its findings in the Aug. 29, 2022 issue of Proceedings of the National Academy of Sciences. The research was supported by the National Science Foundation.

We show that genetic differences among Melissa blue caterpillars and alfalfa plants account for nearly half of the variability in caterpillar growth and survival. Our results suggest individual variation matters, and the outcome of this plant-insect interaction is affected by many genes with mostly independent — or additive — effects. Moreover, genetic differences among alfalfa plants have consistent effects on caterpillar growth in multiple butterfly populations and species, making such effects predictable.

Collecting extensive data over several years at field plots in Utah and Nevada, the team’s results support the hypothesis that both plant and insect genotypes matter, and about equally so for caterpillar growth and survival. Beyond issues specific to insects and their host plants, genetic variation within species could also be important for other host-parasite interactions, Gompert says.

Including, for example, susceptibility to parasitic diseases in humans and other animals being a function of both genetic variation in hosts and among pathogen strains. But the generality of this hypothesis remains to be tested.

More detail is given in the abstract to the team's paper in PNAS:

Significance

Studies of ecological interactions often ignore genetic variation, and studies of coevolution have rarely assayed the genetics of hosts and parasites at the same time. We show that genetic differences among Melissa blue caterpillars and alfalfa plants account for 17 to 49% of the variability in caterpillar growth and survival. The genetic contribution includes heritable variation in defensive compounds, including saponins. Our results suggest that the outcome of this plant–insect interaction is affected by many genes with mostly independent (additive) effects. Moreover, genetic differences among alfalfa plants have consistent effects on caterpillar growth in multiple butterfly populations and species. Our results thus advance understanding of the evolution of ecological interactions, including host–parasite interactions beyond herbivorous insects and plants.

Abstract

Plant–insect interactions are common and important in basic and applied biology. Trait and genetic variation can affect the outcome and evolution of these interactions, but the relative contributions of plant and insect genetic variation and how these interact remain unclear and are rarely subject to assessment in the same experimental context. Here, we address this knowledge gap using a recent host-range expansion onto alfalfa by the Melissa blue butterfly. Common garden rearing experiments and genomic data show that caterpillar performance depends on plant and insect genetic variation, with insect genetics contributing to performance earlier in development and plant genetics later. Our models of performance based on caterpillar genetics retained predictive power when applied to a second common garden. Much of the plant genetic effect could be explained by heritable variation in plant phytochemicals, especially saponins, peptides, and phosphatidyl cholines, providing a possible mechanistic understanding of variation in the species interaction. We find evidence of polygenic, mostly additive effects within and between species, with consistent effects of plant genotype on growth and development across multiple butterfly species. Our results inform theories of plant–insect coevolution and the evolution of diet breadth in herbivorous insects and other host-specific parasites.

Gompert, Zachariah; Saley, Tara; Philbin, Casey; Yoon, Su’ad A.; Perry, Eva; Sneck, Michelle E.; Harrison, Joshua G.; Buerkle, C. Alex; Fordyce, James A.; Nice, Chris C.; Dodson, Craig D.; Lebeis, Sarah L.; Lucas, Lauren K.; Forister, Matthew L.
Additive genetic effects in interacting species jointly determine the outcome of caterpillar herbivory
Proceedings of the National Academy of Sciences (PNAS) 202, 119(36), e2206052119; DOI: 10.1073/pnas.2206052119

Copyright: © 2022 The authors.
Published by PNAS. Open access
Reprinted under a Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

So, a detailed study into the mechanism of evolution has confirmed that it is small variations in the genes of different, interacting species which determines their mutual evolution, exactly as the modern synthesis of the Theory of Evolution says. Darwin and Wallace, of course, knew nothing of genes when they proposed this mechanism as the cause of biodiversity on Earth.

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