Attention:The NSF Public Access Repository (PAR) system and access will be unavailable from 11:00 PM ET on Thursday, October 15th until 12:00 AM ET on Friday, October 16th due to maintenance. We apologize for the inconvenience.


Title: Grand Challenges in Coevolution
Coevolution—reciprocal evolutionary change between interacting lineages (Thompson, 1994; see Glossary)—is thought to have played a profound role in the evolution of Life on Earth. From similar patterns across the wings of unrelated lineages of butterflies (Hoyal Cuthill and Charleston, 2015), egg mimicry of “cheating” brood parasites (Davies, 2010), to the role of animal pollinators in driving the diversification of flowering plants (Kay and Sargent, 2009), to the ubiquity of sexual reproduction and sexual conflicts (Hamilton, 2002; Arnqvist and Rowe, 2005; King et al., 2009), the formation of the eukaryotic cell (Martin et al., 2015; Imachi et al., 2020), and even the origin of living organisms themselves (Mizuuchi and Ichihashi, 2018), evolutionary changes among interacting lineages have played profound and important roles in the history of Life. This Grand Challenges inaugural contribution encompasses eclectic opinions of the editorial board as to what are the next frontiers of coevolution research in the 21st century. Coevolutionary biology is a field that has garnered a lot of attention in recent years, in part as a result of technical advances in nucleotide sequencing and bioinformatics in the burgeoning field of host–microbial interactions. Many seminal studies of coevolution examined reciprocal evolutionary change between two or a few interacting macroscopic species that imposed selective pressures on one another (e.g., insect or bird pollinators and their flowering host plants). Understanding the contexts under which coevolution occurs, as opposed to scenarios in which each partner adapts independently to a particular environment (Darwin, 1862; Stiles, 1978) is important to elucidate coevolutionary processes. A whole spectrum of organismal interactions has been examined under the lens of coevolution, providing additional context, and nuance to ecological strategies traditionally categorized as ranging from beneficial to detrimental for participating species (Figure 1). In particular, a coevolutionary perspective has revealed that even “mutualisms” are not always fully beneficial or cooperative for the partners involved. Instead, the tendency to “cheat” permeates across symbiotic partnerships (Perez-Lamarque et al., 2020). Conversely, recent evidence suggests that non-lethal predation by co-evolved predators, which has traditionally been assumed to be entirely antagonistic, may provide sessile prey with some indirect benefit through enhanced opportunities to acquire beneficial symbiotic microorganisms (Grupstra et al., 2021). Herein, we discuss some of the recent areas of active research in coevolution, restricting our focus to coevolution between interacting species.  more » « less
Award ID(s):
1942647 2032919
PAR ID:
10318434
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ;
Editor(s):
Elgar, Mark A.
Date Published:
Journal Name:
Frontiers in ecology and evolution
Volume:
9
ISSN:
2296-701X
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. In 2009, Jones and Deitz published a tribe-level taxonomic revision and reclassification of the cryptic, arboreal leafhopper subfamily Ledrinae Kirschbaum, 1868 (Hemiptera: Cicadellidae), based on cladistic analyses of 235 morphological features for 75 cicadellid species. Their evolutionary reconstructions found strong node support for a monophyletic ingroup comprising five lineages—each morphologically and geographically cohesive—and also identified numerous traditionally placed taxa (sensu Oman et al 1990) that did not belong. In light of the robustness of their results, the authors recognized the five independent ingroup clades as tribes of Ledrinae, and described three of these as new. 
    more » « less
  2. Abstract Antagonist interactions, such as predator-prey interactions, are widespread in nature and drive both ecological and evolutionary outcomes. Coevolutionary outcomes of antagonistic interactions have been shown to be influenced by environmental conditions, yet the role of abiotic stress in modifying these outcomes remains insufficiently understood. Here we explored how the addition of temperature stress altered evolutionary trajectories of traits of both species in the Pseudomonas fluorescens – Tetrahymena pyriformis (bacteria- ciliate) predator prey system. We found that temperature stress impeded the evolution of traits important for antagonistic interactions in both species. Prey defense levels as well as predators’ ability to eat prey were limited under temperature stress. We also found that the addition of temperature stress altered growth rate evolution in evolving populations of both species. Taken together, our results show that temperature stress not only alters the evolutionary trajectories of both predator and prey traits but also hinders their coevolution. These findings suggest that environmental stressors may weaken reciprocal coevolution which could have important consequences for the stability and persistence of ecological communities. 
    more » « less
  3. Abstract Coevolution has come to be widely understood as specific, simultaneous, reciprocal adaptation by pairs of interacting species. This strict-sense definition arose from a desire for conceptual clarity, but it has never reflected the much wider diversity of ways in which interacting species may shape each other’s evolution. As a result, much of the literature on the evolutionary consequences of species interactions pays homage to the strict-sense definition while addressing some other form of coevolution. This tension suggests we should re-frame the key question in coevolution research, from “when is it coevolution?” to, rather, “how is it coevolution?”. The result is not so much a definition of coevolution as a mission statement: We can describe how species coevolve by documenting the ways that each species shaped the other’s genetic diversity over a shared history of interaction. Making this change shifts our focus from identifying case studies for a single, narrowly defined process to describing the many ways — specific and diffuse, simultaneous and stepwise, adaptive and non-adaptive — in which species evolve together. 
    more » « less
  4. Vertebrates host complex microbiomes that impact their physiology. In many taxa, including colourful wood-warblers, gut microbiome similarity decreases with evolutionary distance. This may suggest that as host populations diverge, so do their microbiomes, because of either tight coevolutionary dynamics, or differential environmental influences, or both. Hybridization is common in wood-warblers, but the effects of evolutionary divergence on the microbiome during secondary contact are unclear. Here, we analyse gut microbiomes in two geographically disjunct hybrid zones between blue-winged warblers (Vermivora cyanoptera) and golden-winged warblers (Vermivora chrysoptera). We performed 16S faecal metabarcoding to identify species-specific bacteria and test the hypothesis that host admixture is associated with gut microbiome disruption. Species identity explained a small amount of variation between microbiomes in only one hybrid zone. Co-occurrence of species-specific bacteria was rare for admixed individuals, yet microbiome richness was similar among admixed and parental individuals. Unexpectedly, we found several bacteria that were more abundant among admixed individuals with a broader deposition of carotenoid-based plumage pigments. These bacteria are predicted to encode carotenoid biosynthesis genes, suggesting birds may take advantage of pigments produced by their gut microbiomes. Thus, host admixture may facilitate beneficial symbiotic interactions which contribute to plumage ornaments that function in sexual selection. 
    more » « less
  5. Gonzalez-Voyer, Alejandro; Rohner, Patrick (Ed.)
    Abstract Phylogenetic comparative methods are a major tool for evaluating macroevolutionary hypotheses. Methods based on the mean-reverting stochastic Ornstein–Uhlenbeck process allow for modelling adaptation on a phenotypic adaptive landscape that itself evolves and where fitness peaks depend on measured characteristics of the external environment and/or other organismal traits. Here, we give an overview of the conceptual framework for the many implementations of these methods and discuss how we might interpret estimated parameters. We emphasize that the ability to model a changing adaptive landscape sets these methods apart from other approaches and discuss why this aspect captures long-term trait evolution more realistically. Recent multivariate extensions of these methods provide a powerful framework for testing evolutionary hypotheses but are also more complicated to use and interpret. We provide some guidance on their usage and put recent literature on the topic in biological rather than mathematical terms. We further show how these methods provide a starting point for modelling reciprocal selection (i.e., coevolution) between interacting lineages. We then briefly review some critiques of the methodologies. Finally, we provide some ideas for future developments that we think will be useful to evolutionary biologists. 
    more » « less