Antagonistic Coevolution Research Articles

Beyond genes‐for‐behaviour: The potential for genomics to resolve long‐standing questions in avian brood parasitism

AbstractBehavioural ecology by definition of its founding ‘Tinbergian framework’ is an integrative field, however, it lags behind in incorporating genomic methods. ‘Finding the gene/s for a behaviour’ is still rarely feasible or cost‐effective in the wild but as we show here, genomic data can be used to address broader questions. Here we use avian brood parasitism, a model system in behavioural ecology as a case study to highlight how behavioural ecologists could use the full potential of state‐of‐the‐art genomic tools. Brood parasite–host interactions are one of the most easily observable and amenable natural laboratories of antagonistic coevolution, and as such have intrigued evolutionary biologists for decades. Using worked examples, we demonstrate how genomic data can be used to study the causes and mechanisms of (co)evolutionary adaptation and answer three key questions for the field: (i) Where and when should brood parasitism evolve?, (ii) When and how should hosts defend?, and (iii) Will coevolution persist with ecological change? In doing so, we discuss how behavioural and molecular ecologists can collaborate to integrate Tinbergen's questions and achieve the coherent science that he promoted to solve the mysteries of nature.

Evolution of mate harm resistance in females from Drosophila melanogaster populations selected for faster development and early reproduction.

Interlocus sexual conflict is predicted to result in sexually antagonistic coevolution between male competitive traits, which are also female-detrimental, and mate harm resistance (MHR) in females. Little is known about the connection between life-history evolution and sexually antagonistic coevolution. Here, we investigated the evolution of MHR in a set of experimentally evolved populations, where mate-harming ability has been shown to have substantially reduced in males as a correlated response to the selection for faster development and early reproduction. We measured mortality and fecundity of females of these populations and those of their matched controls, under different male exposure conditions. We observed that the evolved females were more susceptible to mate harm - suffering from significantly higher mortality under continuous exposure to control males within the twenty-day assay period. Though these evolved females are known to have shorter lifespan, substantially higher mortality was not observed under virgin and single-mating conditions. We used fecundity data to show that this higher mortality in the experimentally evolved females was not due to the cost of egg production, and hence can only be attributed to reduced MHR. Further analysis indicated that this decreased MHR is unlikely to be due purely to the smaller size of these females. Instead, it is more likely to be an indirect experimentally evolved response attributable to the changed breeding ecology, and/or male trait evolution. Our results underline the implications of changes in life history traits, including lifespan, to the evolution of MHR in females.

A shared developmental genetic basis for sexually antagonistic male and female adaptations in the toothed water strider

Abstract Sexual conflict can drive the divergence of male and female phenotypes and cross-species comparative analyses have documented patterns of correlated evolution of sex-specific traits that promote the evolutionary interests of the sexes. However, male–female coevolution can be highly dynamic, particularly if the male and female traits share an underlying genetic program. Here, we use water striders, a well-studied model system for sexually antagonistic coevolution, and ask whether sex-specific phenotypic adaptations covary across populations and whether they share a common developmental genetic basis. Using comparative analyses both at the population and species levels, we document an association between a derived male mate-grasping trait and a putative female antigrasping counteradaptation in the toothed water strider Gerris odontogaster. Interestingly, in several populations where males have partly lost their derived grasping trait, females have also reduced their antigrasping adaptation. We used RNAi to show that these male and female traits are both linked to a common developmental genetic program involving Hox- and sex-determination genes, despite the fact that they are different structures on different abdominal segments. Our work illustrates the dynamic nature of sexually antagonistic coevolution and suggests that the pleiotropic nature of developmental genetic programs can blur the distinction between inter- and intralocus genetic conflict.

Asymmetric arms races between predators and prey: a tug of war between the life-dinner principle and the rare-enemy principle.

Antagonistic co-evolution can be asymmetric, where one species lags behind another. Asymmetry in a predator-prey context is expressed by the 'life-dinner principle', a classic informal model predicting that prey should be in some sense ahead in this arms race, since prey are running for their lives, while predators lag as they only run for their dinner. The model has undergone surprisingly little theoretical scrutiny. We derive analytical models that show coevolutionary outcomes do not always align with the life-dinner principle. Our results show that other important asymmetries can easily reverse the outcome, especially the rare-enemy principle: predators are usually outnumbered by their prey, sometimes substantially (trophic asymmetry), which can make selection on prey relatively weak. We additionally show that the antagonists typically exhibit different evolutionary responses to a situation where both predator and prey start out as equally fast runners. Although predators sometimes become so efficient that attacks always succeed, attack success often reaches a stable intermediate value. We conclude that the life-dinner principle has some validity as a metaphor, but its effect is of an 'all else being equal' type, which is surprisingly easily overridden by other features of the evolutionary dynamics.

Host and parasite intervality in differentially human‐modified habitats

Host–parasite interactions are influenced by present and past eco‐evolutionary interactions and the local environment. An ecological community defines the potential host range of each parasite and the potential parasite diversity of each host species. Past and present processes translate potential to realised interaction niches of parasite and host species. Host–parasite interactions are antagonistic, which may slow the saturation of their interaction niches. Intervality, a property of bipartite networks, measures saturation of interaction niches. Intervality of a community increases as the interaction niches of species of one guild (e.g. hosts) become saturated for their interactions with another guild (e.g. parasites). Characteristics driving intervality in host and parasite communities are largely unknown, as well as the effect of environmental change on intervality of these communities. In our study, we assess if the characteristics ‘phylogenetic relatedness' and ‘overlap in ecological interactions' explain intervality of rodent host–helminth parasite communities. In addition, we contrast intervality of these communities from habitats that differ in their history of human‐driven modification. We performed the analyses for the interaction niches of both parasites and hosts, independently. Our results indicated that host and parasite communities were non‐interval or significantly less interval than expected by chance. Phylogenetic relatedness and overlap in ecological interactions did not explain the maximum values of intervality. We speculate that antagonistic coevolution in host–parasite communities may hinder communities to reach saturation, which would explain why it is difficult to find the characteristics that explain intervality of a community. Interestingly, intervality of the interaction niche of parasites (host range) increased with habitat modification (i.e. saturation increased), whereas intervality of the interaction niche of hosts (parasite diversity) decreased as habitat modification increased. These opposite trends suggest that interaction niches of parasites and hosts respond differently to habitat modification.

Viral plasticity facilitates host diversity in challenging environments

The antagonistic coevolution of microbes and viruses influences fundamentally the diversity of microbial communities. Information on how environmental variables interact with emergent defense-counterdefense strategies and community composition is, however, still scarce. Following biological intuition, diversity should increase with improved growth conditions, which offset evolutionary costs; however, laboratory and regional data suggest that microbial diversity decreases in nutrient-rich conditions. Moreover, global oceanic data show that microbial and viral diversity decline for high latitudes, although the underlying mechanisms are unknown. This article addresses these gaps by introducing an eco-evolutionary model for bacteria-virus antagonistic coevolution. The theory presented here harmonizes the observations above and identifies negative density dependence and viral plasticity (dependence of virus performance on host physiological state) as key drivers: environmental conditions selecting for slow host growth also limit viral performance, facilitating the survival of a diverse host community; host diversity, in turn, enables viral portfolio effects and bet-hedging strategies that sustain viral diversity. From marine microbes to phage therapy against antibiotic-resistant bacteria or cancer cells, the ubiquity of antagonistic coevolution highlights the need to consider eco-evolutionary interactions across a gradient of growth conditions.

Sexually antagonistic coevolution of the male nuptial gift and female feeding behaviour in decorated crickets.

The evolution of nuptial gifts has traditionally been considered a harmonious affair, providing benefits to both mating partners. There is growing evidence, however, that receiving a nuptial gift can be actively detrimental to the female. In decorated crickets (Gryllodes sigillatus), males produce a gelatinous spermatophylax that enhances sperm transfer but provides little nutritional benefit and hinders female post-copulatory mate choice. Here, we examine the sexually antagonistic coevolution of the spermatophylax and the female feeding response to this gift in G. sigillatus maintained in experimental populations with either a male-biased or female-biased adult sex ratio. After 25 generations, males evolving in male-biased populations produced heavier spermatophylaxes with a more manipulative combination of free amino acids than those evolving in female-biased populations. Moreover, when the spermatophylax originated from the same selection regime, females evolving in male-biased populations always had shorter feeding durations than those evolving in female-biased populations, indicating the evolution of greater resistance. Across populations, female feeding duration increased with the mass and manipulative combination of free amino acids in the spermatophylax, suggesting sexually antagonistic coevolution. Collectively, our work demonstrates a key role for interlocus sexual conflict and sexually antagonistic coevolution in the mating system of G. sigillatus.

Long-term balancing selection for pathogen resistance maintains trans-species polymorphisms in a planktonic crustacean

Balancing selection is an evolutionary process that maintains genetic polymorphisms at selected loci and strongly reduces the likelihood of allele fixation. When allelic polymorphisms that predate speciation events are maintained independently in the resulting lineages, a pattern of trans-species polymorphisms may occur. Trans-species polymorphisms have been identified for loci related to mating systems and the MHC, but they are generally rare. Trans-species polymorphisms in disease loci are believed to be a consequence of long-term host-parasite coevolution by balancing selection, the so-called Red Queen dynamics. Here we scan the genomes of three crustaceans with a divergence of over 15 million years and identify 11 genes containing identical-by-descent trans-species polymorphisms with the same polymorphisms in all three species. Four of these genes display molecular footprints of balancing selection and have a function related to immunity. Three of them are located in or close to loci involved in resistance to a virulent bacterial pathogen, Pasteuria, with which the Daphnia host is known to coevolve. This provides rare evidence of trans-species polymorphisms for loci known to be functionally relevant in interactions with a widespread and highly specific parasite. These findings support the theory that specific antagonistic coevolution is able to maintain genetic diversity over millions of years.

Burying in lake sediments: A potential tactic used by female northern map turtles to avoid male harassment

AbstractHow often males and females need to mate to maximize their fitness is a source of sexual conflict in animals. Sexual conflict over mating frequency can lead to antagonistic coevolution in which males employ tactics to coerce females into mating, while females resist or evade mating attempts by males. Here, we report on a novel burying behavior observed in female northern map turtles (Graptemys geographica) in Opinicon Lake, Ontario, Canada that appears to function as a tactic to avoid male detection during the mating season. Underwater videos indicated that females are heavily solicited during the mating season with over half the females being actively pursued by males. Biologgers indicated that females are less active and remain deeper than males during the mating season. Our data strongly suggest that female northern map turtles avoid intense solicitation and potential harassment by males by burying themselves in lake sediments. This behavior appears to be a low‐cost solution for females to reduce the costs of resistance and mating while they are constrained to habitats with high male densities for overwintering.

Coevolution-induced selection for and against phenotypic novelty shapes species richness in clade co-diversification.

Coevolution can occur because of species interactions. However, it remains unclear how coevolutionary processes translate into the accumulation of species richness over macroevolutionary timescales. Assuming speciation occurs as a result of genetic differentiation across space due to dispersal limitation, we examine the effects of coevolution-induced phenotypic selection on species diversification. Based on the idea that dispersers often carry novel phenotypes, we propose and test two hypotheses. (1) Stability hypothesis: selection against phenotypic novelty enhances species diversification by strengthening dispersal limitation. (2) Novelty hypothesis: selection for phenotypic novelty impedes species diversification by weakening dispersal limitation. We simulate clade co-diversification using an individual-based model, considering scenarios where phenotypic selection is shaped by neutral dynamics, mutualistic coevolution, or antagonistic coevolution, where coevolution operates through trait matching or trait difference, and where the strength of coevolutionary selection is symmetrical or asymmetrical. Our key assumption that interactions occur between an independent party (whose individuals can establish or persist independently, e.g. hosts) and a dependent party (whose individuals cannot establish or persist independently, e.g. parasites or obligate mutualists) yields two contrasting results. The stability hypothesis is supported in the dependent clade but not in the independent clade. Conversely, the novelty hypothesis is supported in the independent clade but not in the dependent clade. These results are partially corroborated by empirical dispersal data, suggesting that these mechanisms might potentially explain the diversification of some of the most species-rich clades in the Tree of Life.

Recurrent Duplication and Diversification of a Vital DNA Repair Gene Family Across Drosophila.

Maintaining genome integrity is vital for organismal survival and reproduction. Essential, broadly conserved DNA repair pathways actively preserve genome integrity. However, many DNA repair proteins evolve adaptively. Ecological forces like UV exposure are classically cited drivers of DNA repair evolution. Intrinsic forces like repetitive DNA, which also imperil genome integrity, have received less attention. We recently reported that a Drosophila melanogaster-specific DNA satellite array triggered species-specific, adaptive evolution of a DNA repair protein called Spartan/MH. The Spartan family of proteases cleave hazardous, covalent crosslinks that form between DNA and proteins ("DNA-protein crosslink repair"). Appreciating that DNA satellites are both ubiquitous and universally fast-evolving, we hypothesized that satellite DNA turnover spurs adaptive evolution of DNA-protein crosslink repair beyond a single gene and beyond the D. melanogaster lineage. This hypothesis predicts pervasive Spartan gene family diversification across Drosophila species. To study the evolutionary history of the Drosophila Spartan gene family, we conducted population genetic, molecular evolution, phylogenomic, and tissue-specific expression analyses. We uncovered widespread signals of positive selection across multiple Spartan family genes and across multiple evolutionary timescales. We also detected recurrent Spartan family gene duplication, divergence, and gene loss. Finally, we found that ovary-enriched parent genes consistently birthed functionally diverged, testis-enriched daughter genes. To account for Spartan family diversification, we introduce a novel mechanistic model of antagonistic coevolution that links DNA satellite evolution and adaptive regulation of Spartan protease activity. This framework promises to accelerate our understanding of how DNA repeats drive recurrent evolutionary innovation to preserve genome integrity.

A new species of Eocene soldier beetle, a Malthodes (Coleoptera: Cantharidae: Malthininae) in Baltic amber

ABSTRACT A new species of soldier beetle (Cantharidae) from Eocene Baltic amber, Malthodes maierae sp. nov., is described and illustrated from a male specimen discovered in Russia. The new species differs from the hundreds of known extant and extinct species of Malthodes Kiesenwetter, 1852. The last abdominal segments, which are substantially modified on the male to hold the female during mating, differ considerably in Malthodes species and are very important diagnostic elements for this genus. The exact evolutionary forces driving these manifold modifications are unknown, but they are likely related to sexual selection, mate recognition, antagonistic coevolution, or varying habitats, or a combination of two or more of these factors. The Zoobank LSID for this is: urn:lsid:zoobank.org:pub:DC13FC31-BD71-4C3D-9536-B70AF65FB699

How flexible parasites can outsmart their hosts for evolutionary dominance

Antagonistic coevolution between hosts and parasites substantially impacts community structure, with parasites displaying fluctuating selection or arms race dynamics during coevolution. The traditional matching alleles (MA) and gene-for-gene (GFG) models have been used to describe the dynamics and interaction of host-parasite coevolution, with these models assuming that parasites adopt a single strategy when competing with other parasites. We present a nonlinear dynamic population model that challenges this assumption, showing how a parasite that is disadvantaged under either the MA or the GFG model can win the competition by switching between the two losing strategies based on an external environmental cue, internal processes, or stochastic decision-making. This counterintuitive outcome is analogous to Parrondo's paradox, a game-theoretic concept that shows how alternating between two losing strategies can result in a winning outcome. Our numerical experiments support the validity of this model, suggesting that parasites can greatly benefit from maximum flexibility in their interactions with hosts. The flexibility of successful parasites puts an extra burden on the host defenses that have to adapt to different strategies of the parasites. These findings contribute to a deeper understanding of the coevolution of parasites and hosts, with broad implications for the evolution of complex ecological systems. Published by the American Physical Society 2024

Ectopical expression of bacterial collagen-like protein supports its role as adhesin in host-parasite coevolution.

For a profound understanding of antagonistic coevolution, it is necessary to identify the coevolving genes. The bacterium Pasteuria and its host, the microcrustacean Daphnia, are a well-characterized paradigm for co-evolution, but the underlying genes remain largely unknown. A genome-wide association study suggested a Pasteuria collagen-like protein 7 (Pcl7) as a candidate mediating parasite attachment and driving its coevolution with the host. Since Pasteuria ramosa cannot currently be genetically manipulated, we used Bacillus thuringiensis to express a fusion protein of a Pcl7 carboxy-terminus from P. ramosa and the amino-terminal domain of a B. thuringiensis collagen-like protein (CLP). Mutant B. thuringiensis (Pcl7-Bt) spores but not wild-type B. thuringiensis (WT-Bt) spores attached to the same site of susceptible hosts as P. ramosa. Furthermore, Pcl7-Bt spores attached readily to susceptible host genotypes, but only slightly to resistant host genotypes. These findings indicated that the fusion protein was properly expressed and folded and demonstrated that indeed the C-terminus of Pcl7 mediates attachment in a host genotype-specific manner. These results provide strong evidence for the involvement of a CLP in the coevolution of Daphnia and P. ramosa and open new avenues for genetic epidemiological studies of host-parasite interactions.

Phage-driven coevolution reveals trade-off between antibiotic and phage resistance in Salmonella anatum.

Phage therapy faces challenges against multidrug-resistant (MDR) Salmonella due to rapid phage-resistant mutant emergence. Understanding the intricate interplay between antibiotics and phages is essential for shaping Salmonella evolution and advancing phage therapy. In this study, MDR Salmonella anatum (S. anatum) 2089b coevolved with phage JNwz02 for 30 passages (60days), then the effect of coevolution on the trade-off between phage and antibiotic resistance in bacteria was investigated. Our results demonstrated antagonistic coevolution between bacteria and phages, transitioning from arms race dynamics (ARD) to fluctuating selection dynamics (FSD). The fitness cost of phage resistance, manifested as reduced competitiveness, was observed. Bacteria evolved phage resistance while simultaneously regaining sensitivity to amoxicillin, ampicillin, and gentamicin, influenced by phage selection pressure and bacterial competitiveness. Moreover, the impact of phage selection pressure on the trade-off between antibiotic and phage resistance was more pronounced in the ARD stage than in the FSD stage. Whole genome analysis revealed mutations in the btuB gene in evolved S. anatum strains, with a notably higher mutation frequency in the ARD stage compared to the FSD stage. Subsequent knockout experiments confirmed BtuB as a receptor for phage JNwz02, and the deletion of btuB resulted in reduced bacterial competitiveness. Additionally, the mutations identified in the phage-resistant strains were linked to multiple single nucleotide polymorphisms (SNPs) associated with membrane components. This correlation implies a potential role of these SNPs in reinstating antibiotic susceptibility. These findings significantly advance our understanding of phage-host interactions and the impact of bacterial adaptations on antibiotic resistance.

Parallel evolution and enhanced virulence upon in vivo passage of an RNA virus in Drosophila melanogaster.

Virus evolution is strongly affected by antagonistic co-evolution of virus and host. Host immunity positively selects for viruses that evade the immune response, which in turn may drive counter-adaptations in host immune genes. We investigated how host immune pressure shapes virus populations, using the fruit fly Drosophila melanogaster and its natural pathogen Drosophila C virus (DCV), as a model. We performed an experimental evolution study in which DCV was serially passaged for ten generations in three fly genotypes differing in their antiviral RNAi response: wild-type flies and flies in which the endonuclease gene Dicer-2 was either overexpressed or inactivated. All evolved virus populations replicated more efficiently in vivo and were more virulent than the parental stock. The number of polymorphisms increased in all three host genotypes with passage number, which was most pronounced in Dicer-2 knockout flies. Mutational analysis showed strong parallel evolution, as mutations accumulated in a specific region of the VP3 capsid protein in every lineage in a host genotype-independent manner. The parental tyrosine at position ninety-five of VP3 was substituted with either one of five different amino acids in fourteen out of fifteen lineages. However, no consistent amino acid changes were observed in the viral RNAi suppressor gene 1A, nor elsewhere in the genome in any of the host backgrounds. Our study indicates that the RNAi response restricts the sequence space that can be explored by viral populations. Moreover, our study illustrates how evolution towards higher virulence can be a highly reproducible, yet unpredictable process.

Host-pathogen coevolution promotes the evolution of general, broad-spectrum resistance and reduces foreign pathogen spillover risk.

Genetic variation for disease resistance within host populations can strongly impact the spread of endemic pathogens. In plants, recent work has shown that within-population variation in resistance can also affect the transmission of foreign spillover pathogens if that resistance is general. However, most hosts also possess specific resistance mechanisms that provide strong defenses against coevolved endemic pathogens. Here we use a modeling approach to ask how antagonistic coevolution between hosts and their endemic pathogen at the specific resistance locus can affect the frequency of general resistance, and therefore a host's vulnerability to foreign pathogens. We develop a two-locus model with variable recombination that incorporates both general resistance (effective against all pathogens) and specific resistance (effective against endemic pathogens only). With coevolution, when pathogens can evolve to evade specific resistance, we find that the regions where general resistance can evolve are greatly expanded, decreasing the risk of foreign pathogen invasion. Furthermore, coevolution greatly expands the conditions that maintain polymorphisms at both resistance loci, thereby driving greater genetic diversity within host populations. This genetic diversity often leads to positive correlations between host resistance to foreign and endemic pathogens, similar to those observed in natural populations. However, if resistance loci become linked, the resistance correlations can shift to negative. If we include a third linkage-modifying locus in our model, we find that selection often favors complete linkage. Our model demonstrates how coevolutionary dynamics with an endemic pathogen can mold the resistance structure of host populations in ways that affect its susceptibility to foreign pathogen spillovers, and that the nature of these outcomes depends on resistance costs, as well as the degree of linkage between resistance genes.

The maintenance of genetic diversity under host-parasite coevolution in finite, structured populations.

As a corollary to the Red Queen hypothesis, host-parasite coevolution has been hypothesized to maintain genetic variation in both species. Recent theoretical work, however, suggests that reciprocal natural selection alone is insufficient to maintain variation at individual loci. As highlighted by our brief review of the theoretical literature, models of host-parasite coevolution often vary along multiple axes (e.g. inclusion of ecological feedbacks or abiotic selection mosaics), complicating a comprehensive understanding of the effects of interacting evolutionary processes on diversity. Here we develop a series of comparable models to explore the effect of interactions between spatial structures and antagonistic coevolution on genetic diversity. Using a matching alleles model in finite populations connected by migration, we find that, in contrast to panmictic populations, coevolution in a spatially structured environment can maintain genetic variation relative to neutral expectations with migration alone. These results demonstrate that geographic structure is essential for understanding the effect of coevolution on biological diversity.

Haemoproteus parasites and passerines: the effect of local generalists on inferences of host-parasite co-phylogeny in the British Isles.

Host–parasite associations provide a benchmark for investigating evolutionary arms races and antagonistic coevolution. However, potential ecological mechanisms underlying such associations are difficult to unravel. In particular, local adaptations of hosts and/or parasites may hamper reliable inferences of host–parasite relationships and the specialist–generalist definitions of parasite lineages, making it problematic to understand such relationships on a global scale. Phylogenetic methods were used to investigate co-phylogenetic patterns between vector-borne parasites of the genus Haemoproteus and their passeriform hosts, to infer the ecological interactions of parasites and hosts that may have driven the evolution of both groups in a local geographic domain. As several Haemoproteus lineages were only detected once, and given the occurrence of a single extreme generalist, the effect of removing individual lineages on the co-phylogeny pattern was tested. When all lineages were included, and when all singly detected lineages were removed, there was no convincing evidence for host–parasite co-phylogeny. However, when only the generalist lineage was removed, strong support for co-phylogeny was indicated, and ecological interactions could be successfully inferred. This study exemplifies the importance of identifying locally abundant lineages when sampling host–parasite systems, to provide reliable insights into the precise mechanisms underlying host–parasite interactions.

An emerging view of coevolution in the legume-rhizobium mutualism.

Mutualisms are often framed as 'delicately balanced antagonisms' (Bronstein, 1994), with the net fitness benefits to both partners potentially masking underlying conflicts of interest. How commonly symbionts evolve to 'cheat' their hosts and hosts evolve to 'sanction' or 'control' uncooperative symbionts is the subject of debate, especially in legume-rhizobium interactions (Frederickson, 2013; Kiers et al., 2003). This kind of antagonistic coevolution should result in either arms-race dynamics characterized by repeated selective sweeps or fluctuating selection dynamics that leave signatures of balancing selection in host and symbiont genomes (Frederickson, 2013; Kortright et al., 2022; O'Brien et al., 2021). In a From the Cover article in this issue of Molecular Ecology, Epstein et al. (2022) combine GWAS and population genomic analyses to assess the evidence for positive or balancing selection consistent with ongoing, antagonistic coevolution between legumes and rhizobia. They found few genomic signatures of fitness conflicts between mutualistic partners, suggesting that legume and rhizobium fitness interests are largely aligned and symbiotic traits are mostly under stabilizing selection. In combination with other recent work (e.g. Batstone et al., 2020), the results of Epstein et al. (2022) indicate that there is little ongoing fitness conflict between legumes and rhizobia that shapes host and symbiont genomes in this system. It may be time to move beyond symbiont 'cheating' and host 'control' as the dominant paradigm for understanding how partners in mutualism coevolve.