Should we hail the Red King? Evolutionary consequences of a mutualistic lifestyle in genomes of lichenized ascomycetes

The Red Queen dynamic is often brought into play for antagonistic relationships. However, the coevolutionary effects of mutualistic interactions, which predict slower evolution for interacting organisms (Red King), have been investigated to a lesser extent. Lichens are a stable, mutualistic relationship of fungi and cyanobacteria and/or algae, which originated several times independently during the evolution of fungi. Therefore, they represent a suitable system to investigate the coevolutionary effect of mutualism on the fungal genome. We measured substitution rates and selective pressure of about 2000 protein‐coding genes (plus the rDNA region) in two different classes of Ascomycota, each consisting of closely related lineages of lichenized and non‐lichenized fungi. Our results show that independent lichenized clades are characterized by significantly slower rates for both synonymous and non‐synonymous substitutions. We hypothesize that this evolutionary pattern is connected to the lichen life cycle (longer generation time of lichenized fungi) rather than a result of different selection strengths, which is described as the main driver for the Red Kind dynamic. This first empirical evidence of slower evolution in lichens provides an important insight on how biotic cooperative interactions are able to shape the evolution of symbiotic organisms.     

A slowly evolving host moves first in symbiotic interactions

Symbiotic relationships, both parasitic and mutualistic, are ubiquitous in nature. Understanding how these symbioses evolve, from bacteria and their phages to humans and our gut microflora, is crucial in understanding how life operates. Often, symbioses consist of a slowly evolving host species with each host only interacting with its own subpopulation of symbionts. The Red Queen hypothesis describes coevolutionary relationships as constant arms races with each species rushing to evolve an advantage over the other, suggesting that faster evolution is favored. Here, we use a simple game theoretic model of host-symbiont coevolution that includes population structure to show that if the symbionts evolve much faster than the host, the equilibrium distribution is the same as it would be if it were a sequential game where the host moves first against its symbionts. For the slowly evolving host, this will prove to be advantageous in mutualisms and a handicap in antagonisms. The result follows from rapid symbiont adaptation to its host and is robust to changes in the parameters, even generalizing to continuous and multiplayer games. Our findings provide insight into a wide range of symbiotic phenomena and help to unify the field of coevolutionary theory.     

Kin selection and the Evolution of Mutualisms between Species

Hamilton's theory of kin selection has revolutionized and inspired fifty years of additional theories and experiments on social evolution. Whereas Hamilton's broader intent was to explain the evolutionary stability of cooperation, his focus on shared genetic history appears to have limited the application of his theory to populations within a single species rather than across interacting species. The evolutionary mechanisms for cooperation between species require both spatial and temporal correlations among interacting partners for the benefits to be not only predictable but of sufficient duration to be reliably delivered. As a consequence when the benefits returned by mutualistic partners are redirected to individuals other than the original donor, cooperation usually becomes unstable and parasitism may evolve. However, theoretically, such redirection of mutualistic benefits may actually reinforce, rather than undermine, mutualisms between species when the recipients of these redirected benefits are genetically related to the original donor. Here, I review the few mathematical models that have used Hamilton's theory of kin selection to predict the evolution of mutualisms between species. I go on to examine the applicability of these models to the most well‐studied case of mutualism, pollinating seed predators, where the role of kin selection may have been previously overlooked. Future detailed studies of the direct, and indirect, benefits of mutualism are likely to reveal additional possibilities for applying Hamilton's theory of kin selection to mutualisms between species.     

Whose trait is it anyways? Coevolution of joint phenotypes and genetic architecture in mutualisms

Evolutionary biologists typically envision a trait’s genetic basis and fitness effects occurring within a single species. However, traits can be determined by and have fitness consequences for interacting species, thus evolving in multiple genomes. This is especially likely in mutualisms, where species exchange fitness benefits and can associate over long periods of time. Partners may experience evolutionary conflict over the value of a multi-genomic trait, but such conflicts may be ameliorated by mutualism’s positive fitness feedbacks. Here, we develop a simulation model of a host–microbe mutualism to explore the evolution of a multi-genomic trait. Coevolutionary outcomes depend on whether hosts and microbes have similar or different optimal trait values, strengths of selection and fitness feedbacks. We show that genome-wide association studies can map joint traits to loci in multiple genomes and describe how fitness conflict and fitness feedback generate different multi-genomic architectures with distinct signals around segregating loci. Partner fitnesses can be positively correlated even when partners are in conflict over the value of a multi-genomic trait, and conflict can generate strong mutualistic dependency. While fitness alignment facilitates rapid adaptation to a new optimum, conflict maintains genetic variation and evolvability, with implications for applied microbiome science.     

Upstream reciprocity and the evolution of gratitude

If someone is nice to you, you feel good and may be inclined to be nice to somebody else. This every day experience is borne out by experimental games: the recipients of an act of kindness are more likely to help in turn, even if the person who benefits from their generosity is somebody else. This behaviour, which has been called ‘upstream reciprocity’, appears to be a misdirected act of gratitude: you help somebody because somebody else has helped you. Does this make any sense from an evolutionary or a game theoretic perspective? In this paper, we show that upstream reciprocity alone does not lead to the evolution of cooperation, but it can evolve and increase the level of cooperation if it is linked to either direct or spatial reciprocity. We calculate the random walks of altruistic acts that are induced by upstream reciprocity. Our analysis shows that gratitude and other positive emotions, which increase the willingness to help others, can evolve in the competitive world of natural selection.     

Chaotic Red Queen coevolution in three-species food chains

Coevolution between two antagonistic species follows the so-called ‘Red Queen dynamics’ when reciprocal selection results in an endless series of adaptation by one species and counteradaptation by the other. Red Queen dynamics are ‘genetically driven’ when selective sweeps involving new beneficial mutations result in perpetual oscillations of the coevolving traits on the slow evolutionary time scale. Mathematical models have shown that a prey and a predator can coevolve along a genetically driven Red Queen cycle. We found that embedding the prey–predator interaction into a three-species food chain that includes a coevolving superpredator often turns the genetically driven Red Queen cycle into chaos. A key condition is that the prey evolves fast enough. Red Queen chaos implies that the direction and strength of selection are intrinsically unpredictable beyond a short evolutionary time, with greatest evolutionary unpredictability in the superpredator. We hypothesize that genetically driven Red Queen chaos could explain why many natural populations are poised at the edge of ecological chaos. Over space, genetically driven chaos is expected to cause the evolutionary divergence of local populations, even under homogenizing environmental fluctuations, and thus to promote genetic diversity among ecological communities over long evolutionary time.     

Information processing in multigame environments modeling the evolution of sex via punctuated equilibria

Uncertain environments are properly described by probability distributions which, as usual, can be collapsed or conditioned into distributions with reduced uncertainty through the processing of environmental information. Organisms which force this collapse gain evolutionary advantage by being able to employ strategies in a known environment rather than in a merely probable one. The accrued benefit gained from processing information can be precisely quantified by comparing benefits returned using distributions prior to, and after collapse, and these often large and immediate benefits can amply justify the evolutionary cost of information processing systems. More importantly, the evolution of information processing systems must necessarily occur in a predictable evolutionary sequence from less complex to more complex. Practical applications include modeling the evolution of sex modeled here as a sequence from asexual reproduction, to single gene exchange, to gene packet exchange, to same species packet exchange, and finally to sexual reproduction, sexual selection, Red Queen contests and so on. Modeling this sequence requires extensions to game theory originally designed to model a single game, to allow the simultaneous operation of many games. This extension is called a multigame environment. The dynamical evolution of the development sequence shows punctuated equilibria.     

Evolution of transmission mode in conditional mutualisms with spatial variation in symbiont quality

Many symbioses have costs and benefits to their hosts that vary with the environmental context, which itself may vary in space. The same symbiont may be a mutualist in one location and a parasite in another. Such spatially conditional mutualisms pose a dilemma for hosts, who might evolve (higher or lower) horizontal or vertical transmission to increase their chances of being infected only where the symbiont is beneficial. To determine how transmission in hosts might evolve, we modeled transmission evolution where the symbiont had a spatially conditional effect on either host lifespan or fecundity. We found that over ecological time, symbionts that affected lifespan but not fecundity led to high frequencies of infected hosts in areas where the symbiont was beneficial and low frequencies elsewhere. In response, hosts evolved increased horizontal transmission only when the symbiont affected lifespan. We also modeled transmission evolution in symbionts, which evolved high horizontal and vertical transmission, indicating a possible host–symbiont conflict over transmission mode. Our results suggest an eco‐evolutionary feedback where the component of host fitness affected by a conditionally mutualistic symbiont in turn determines its distribution in the population, and, through this, the transmission mode that evolves.     

The Evolution of Different Forms of Sociality: Behavioral Mechanisms and Eco-Evolutionary Feedback

Different forms of sociality have evolved via unique evolutionary trajectories. However, it remains unknown to what extent trajectories of social evolution depend on the specific characteristics of different species. Our approach to studying such trajectories is to use evolutionary case-studies, so that we can investigate how grouping co-evolves with a multitude of individual characteristics. Here we focus on anti-predator vigilance and foraging. We use an individual-based model, where behavioral mechanisms are specified, and costs and benefits are not predefined. We show that evolutionary changes in grouping alter selection pressures on vigilance, and vice versa. This eco-evolutionary feedback generates an evolutionary progression from “leader-follower” societies to “fission-fusion” societies, where cooperative vigilance in groups is maintained via a balance between within- and between-group selection. Group-level selection is generated from an assortment that arises spontaneously when vigilant and non-vigilant foragers have different grouping tendencies. The evolutionary maintenance of small groups, and cooperative vigilance in those groups, is therefore achieved simultaneously. The evolutionary phases, and the transitions between them, depend strongly on behavioral mechanisms. Thus, integrating behavioral mechanisms and eco-evolutionary feedback is critical for understanding what kinds of intermediate stages are involved during the evolution of particular forms of sociality.     

Physiological evolution during adaptive radiation: A test of the island effect in Anolis lizards

Phenotypic evolution is often exceptionally rapid on islands, resulting in numerous, ecologically diverse species. Although adaptive radiation proceeds along various phenotypic axes, the island effect of faster evolution has been mostly tested with regard to morphology. Here, we leveraged the physiological diversity and species richness of Anolis lizards to examine the evolutionary dynamics of three key traits: heat tolerance, body temperature, and cold tolerance. Contrary to expectation, we discovered slower heat tolerance evolution on islands. Additionally, island species evolve toward higher optimal body temperatures than mainland species. Higher optima and slower evolution in upper physiological limits are consistent with the Bogert effect, or evolutionary inertia due to thermoregulation. Correspondingly, body temperature is higher and more stable on islands than on the American mainland, despite similarity in thermal environments. Greater thermoregulation on islands may occur due to ecological release from competitors and predators compared to mainland environments. By reducing the costs of thermoregulation, ecological opportunity on islands may actually stymie, rather than hasten, physiological evolution. Our results emphasize that physiological diversity is an important axis of ecological differentiation in the adaptive radiation of anoles, and that behavior can impart distinct macroevolutionary footprints on physiological diversity on islands and continents.     

The evolution of cooperative breeding through group augmentation

Some individuals (helpers) in cooperatively breeding species provide alloparental care and often suppress their own reproduction. Kin selection is clearly an important explanation for such behaviour, but a possible alternative is group augmentation where individuals survive or reproduce better in large groups and where it therefore pays to recruit new members to the group. The evolutionary stability of group augmentation is currently disputed. We model evolutionarily stable helping strategies by following the dynamics of social groups with varying degrees of subordinate help. We also distinguish between passive augmentation, where a group member benefits from the mere presence of others, and active augmentation, where their presence as such is neutral or harmful, but where helping to recruit new group members may still be beneficial if they in turn actively provide help for the current reproductives ('delayed reciprocity'). The results show that group augmentation (either passive or active) can be evolutionarily stable and explain costly helping by non-reproductive subordinates, either alone or leading to elevated help levels when acting in concert with kin selection. Group augmentation can thus potentially explain the weak relationships between relatedness and helping behaviour that are observed in some cooperatively breeding species. In some cases, the superior mutualistic performance of cooperatively behaving groups can generate an incentive to stay and help which is strong enough to make ecological constraints unnecessary for explaining the stability of cooperatively breeding groups.     

Phylogenetic and Experimental Tests of Interactions among Mutualistic Plant Defense Traits in Viburnum (Adoxaceae)

Abstract Plant traits that mediate mutualistic interactions are widespread, yet few studies have linked their macroevolutionary patterns with the ecological interactions they mediate. Here we merged phylogenetic and experimental approaches to investigate the evolution of two common mutualistic plant traits, extrafloral nectaries (EFNs) and leaf domatia. By using the flowering plant clade Viburnum, we tested whether macroevolutionary patterns support adaptive hypotheses and conducted field surveys and manipulative experiments to examine whether ecological interactions are concordant with evolutionary predictions. Phylogenetic reconstructions suggested that EFN-bearing species are monophyletic, whereas the evolution of domatia correlated with leaf production strategy (deciduous or evergreen) and climate. Domatia were also more common in the EFN clade, suggesting that the two traits may jointly mediate ecological interactions. This result was further investigated in a common-garden survey, where plants with domatia and EFNs on the leaf blade had more mutualistic mites than plants with other trait combinations, and in manipulative field experiments, where the traits additively increased mutualist abundance. Taken together, our results suggest that mutualistic traits in Viburnum are not ecologically independent, as they work in concert to attract and retain mutualists, and their long-term evolution may be influenced by complex interactions among multiple traits, mutualists, and geography.     

Sex,competition and mimicry: an eco-evolutionary model reveals unexpected impacts of ecological interactions on the evolution of phenotypes in sympatry

Phenotypic evolution in sympatric species can be strongly impacted by species interactions, either mutualistic or antagonistic. Heterospecific reproductive behaviours between sympatric species have been shown to favour phenotypic divergence of traits used as sexual cues. Those traits may also be involved in local adaptation or in other types of species interactions and, as a result, undergo complex evolutions across sympatric species. Here we focus on mimicry and study how reproductive interference may impair phenotypic convergence between species with various levels of defence. We use a deterministic model assuming two sympatric species where individuals can display two different warning colour patterns. This eco-evolutionary model explores how ecological interactions shape phenotypic evolution within sympatric species. We investigate the effect of 1) the opposing density-dependent selections exerted on colour patterns by predation and reproductive behaviour and 2) the impact of relative species and phenotype abundances on the fitness costs faced by each individual depending on their species and phenotype. Our model shows that reproductive interference may limit the convergent effect of mimetic interactions and may promote phenotypic divergence between Müllerian mimics. The divergent and convergent evolution of traits also strongly depends on the relative species and phenotype abundances and levels of trophic competition, highlighting how the eco-evolutionary feedbacks between phenotypic evolution and species abundances may result in strikingly different evolutionary routes.     

Extrapolating Weak Selection in Evolutionary Games

In evolutionary games, reproductive success is determined by payoffs. Weak selection means that even large differences in game outcomes translate into small fitness differences. Many results have been derived using weak selection approximations, in which perturbation analysis facilitates the derivation of analytical results. Here, we ask whether results derived under weak selection are also qualitatively valid for intermediate and strong selection. By “qualitatively valid” we mean that the ranking of strategies induced by an evolutionary process does not change when the intensity of selection increases. For two-strategy games, we show that the ranking obtained under weak selection cannot be carried over to higher selection intensity if the number of players exceeds two. For games with three (or more) strategies, previous examples for multiplayer games have shown that the ranking of strategies can change with the intensity of selection. In particular, rank changes imply that the most abundant strategy at one intensity of selection can become the least abundant for another. We show that this applies already to pairwise interactions for a broad class of evolutionary processes. Even when both weak and strong selection limits lead to consistent predictions, rank changes can occur for intermediate intensities of selection. To analyze how common such games are, we show numerically that for randomly drawn two-player games with three or more strategies, rank changes frequently occur and their likelihood increases rapidly with the number of strategies . In particular, rank changes are almost certain for , which jeopardizes the predictive power of results derived for weak selection.     

Life-history differences among coral reef sponges promote mutualism or exploitation of mutualism by influencing partner fidelity feedback

Mutualism can be favored over exploitation of mutualism when interests of potential heterospecific partners are aligned so that individual organisms are beneficial to each others' continued growth, survival, and reproduction, that is, when exploitation of a particular partner individual is costly. A coral reef sponge system is particularly amenable to field experiments probing how costs of exploitation can be influenced by life-history characteristics. Pairwise associations among three of the sponge species are mutually beneficial. A fourth species, Desmapsamma anchorata, exploits these mutualisms. Desmapsamma also differs from the other species by growing faster, fragmenting more readily, and suffering higher mortality rates. Evaluating costs and benefits of association in the context of the complex life histories of these asexually fragmenting sponges shows costs of exploitation to be high for the mutualistic species but very low for this essentially weedy species. Although it benefits from association more than the mutualist species, by relying on their superior tensile strength and extensibility to reduce damage by physical disturbance, exploitation is favored because each individual host is of only ephemeral use. These sponges illustrate how life-history differences can influence the duration of association between individuals and, thus, the role of partner fidelity in promoting mutualism.     

Can the evolution of plant defense lead to plant-herbivore mutualism?

Moderate rates of herbivory can enhance primary production. This hypothesis has led to a controversy as to whether such positive effects can result in mutualistic interactions between plants and herbivores. We present a model for the ecology and evolution of plant-herbivore systems to address this question. In this model, herbivores have a positive indirect effect on plants through recycling of a limiting nutrient. Plants can evolve but are constrained by a trade-off between growth and antiherbivore defense. Although evolution generally does not lead to optimal plant performance, our evolutionary analysis shows that, under certain conditions, the plant-herbivore interaction can be considered mutualistic. This requires in particular that herbivores efficiently recycle nutrients and that plant reproduction be positively correlated with primary production. We emphasize that two different definitions of mutualism need to be distinguished. A first ecological definition of mutualism is based on the short-term response of plants to herbivore removal, whereas a second evolutionary definition rests on the long-term response of plants to herbivore removal, allowing plants to adapt to the absence of herbivores. The conditions for an evolutionary mutualism are more stringent than those for an ecological mutualism. A particularly counterintuitive result is that higher herbivore recycling efficiency results both in increased plant benefits and in the evolution of increased plant defense. Thus, antagonistic evolution occurs within a mutualistic interaction.     

Proteases hold the key to an exclusive mutualism

Mutualisms, cooperative interactions between species, generally involve an economic exchange: species exchange commodities that are cheap for them to provide, for ones that cannot be obtained affordably or at all. But these associations can only succeed if effective partners can be enticed to interact. In some mutualisms, partners can actively seek one another out. However, plants, which use mutualists for a wide array of essential life history functions, do not have this option. Instead, natural selection has repeatedly favoured the evolution of rewards – nutritional substances (such as sugar‐rich nectar and fleshy fruit) with which plants attract certain organisms whose feeding activities can then be co‐opted for their own benefit. The trouble with rewards, however, is that they are usually also attractive to organisms that confer no benefits at all. Losing rewards to ‘exploiters’ makes a plant immediately less attractive to the mutualists it requires; if the reward cannot be renewed quickly (or at all), then mutualistic service is precluded entirely. Thus, it is in plants' interests to either restrict rewards to only the most beneficial partners or somehow punish or deter exploiters. Yet, at least in cases where the rewards are highly nutritious, we can expect counter‐selection for exploiter traits that permit them to skirt such control. How, then, can mutualisms persist? In this issue, Orona‐Tamayo et al. ( 2013 ) describe a remarkable adaptation that safeguards one particularly costly reward from nonmutualists. Their study helps to explain the evolutionary success of an iconic interaction and illuminates one way in which mutualism as a whole can persist in the face of exploitation.     

Consequences of fluctuating group size for the evolution of cooperation

Studies of cooperation have traditionally focused on discrete games such as the well-known prisoner’s dilemma, in which players choose between two pure strategies: cooperation and defection. Increasingly, however, cooperation is being studied in continuous games that feature a continuum of strategies determining the level of cooperative investment. For the continuous snowdrift game, it has been shown that a gradually evolving monomorphic population may undergo evolutionary branching, resulting in the emergence of a defector strategy that coexists with a cooperator strategy. This phenomenon has been dubbed the ‘tragedy of the commune’. Here we study the effects of fluctuating group size on the tragedy of the commune and derive analytical conditions for evolutionary branching. Our results show that the effects of fluctuating group size on evolutionary dynamics critically depend on the structure of payoff functions. For games with additively separable benefits and costs, fluctuations in group size make evolutionary branching less likely, and sufficiently large fluctuations in group size can always turn an evolutionary branching point into a locally evolutionarily stable strategy. For games with multiplicatively separable benefits and costs, fluctuations in group size can either prevent or induce the tragedy of the commune. For games with general interactions between benefits and costs, we derive a general classification scheme based on second derivatives of the payoff function, to elucidate when fluctuations in group size help or hinder cooperation.     

Bipartite graphs as models of population structures in evolutionary multiplayer games

By combining evolutionary game theory and graph theory, "games on graphs" study the evolutionary dynamics of frequency-dependent selection in population structures modeled as geographical or social networks. Networks are usually represented by means of unipartite graphs, and social interactions by two-person games such as the famous prisoner's dilemma. Unipartite graphs have also been used for modeling interactions going beyond pairwise interactions. In this paper, we argue that bipartite graphs are a better alternative to unipartite graphs for describing population structures in evolutionary multiplayer games. To illustrate this point, we make use of bipartite graphs to investigate, by means of computer simulations, the evolution of cooperation under the conventional and the distributed N-person prisoner's dilemma. We show that several implicit assumptions arising from the standard approach based on unipartite graphs (such as the definition of replacement neighborhoods, the intertwining of individual and group diversity, and the large overlap of interaction neighborhoods) can have a large impact on the resulting evolutionary dynamics. Our work provides a clear example of the importance of construction procedures in games on graphs, of the suitability of bigraphs and hypergraphs for computational modeling, and of the importance of concepts from social network analysis such as centrality, centralization and bipartite clustering for the understanding of dynamical processes occurring on networked population structures.     

Faster-X Evolution of Gene Expression in Drosophila

DNA sequences on X chromosomes often have a faster rate of evolution when compared to similar loci on the autosomes, and well articulated models provide reasons why the X-linked mode of inheritance may be responsible for the faster evolution of X-linked genes. We analyzed microarray and RNA–seq data collected from females and males of six Drosophila species and found that the expression levels of X-linked genes also diverge faster than autosomal gene expression, similar to the “faster-X” effect often observed in DNA sequence evolution. Faster-X evolution of gene expression was recently described in mammals, but it was limited to the evolutionary lineages shortly following the creation of the therian X chromosome. In contrast, we detect a faster-X effect along both deep lineages and those on the tips of the Drosophila phylogeny. In Drosophila males, the dosage compensation complex (DCC) binds the X chromosome, creating a unique chromatin environment that promotes the hyper-expression of X-linked genes. We find that DCC binding, chromatin environment, and breadth of expression are all predictive of the rate of gene expression evolution. In addition, estimates of the intraspecific genetic polymorphism underlying gene expression variation suggest that X-linked expression levels are not under relaxed selective constraints. We therefore hypothesize that the faster-X evolution of gene expression is the result of the adaptive fixation of beneficial mutations at X-linked loci that change expression level in cis. This adaptive faster-X evolution of gene expression is limited to genes that are narrowly expressed in a single tissue, suggesting that relaxed pleiotropic constraints permit a faster response to selection. Finally, we present a conceptional framework to explain faster-X expression evolution, and we use this framework to examine differences in the faster-X effect between Drosophila and mammals.