Maintenance of variation in mutualism by screening

Models of partner choice leading to mutualism raise a conceptual problem: directional selection for high‐quality partners should ultimately erode variation in partner quality. How do we explain the persistence of variation in partner quality observed in nature? The problem arises in all models of partner choice, including screening models, in which a host induces potential symbionts of different quality to screen themselves by assigning them different costs and rewards. Using a screening model in which costs and rewards are sometimes assigned incorrectly, I show that a stable polymorphism can arise because rewards are higher when partners vary in quality than when there is only one type of partner. Partner quality, therefore, undergoes negative frequency‐dependent selection even though there is a preference for high‐quality partners. This also shows that partner choice by screening does not need to be totally accurate to be effective—inaccuracies enable both effective screening and the maintenance of variation.     

Contract theory for the evolution of cooperation: The right incentives attract the right partners

Partner choice is a critical stage of many biological interactions, from mating to cooperation. When the quality of the potential partners is unknown, one way to choose is to rely on signaling: costly signals can reveal the quality of the sender and allow the receiver to choose. In some cases, however, signaling (or an active choice based on signals) is not possible, for example in the initiation of the symbiosis between the squid Euprymna scolopes and the bioluminescent bacterium Vibrio fischeri. How is partner choice possible in this and other similar cases? I show that in a game with asymmetric information without signaling, imposing a deliberate cost for establishing the interaction allows the non-informed individual to attract the right partner if the cost induces only high quality individuals to accept the interaction. Furthermore, imposing different costs and rewards may induce the informed individuals to screen themselves according to their types, and therefore allow the non-informed individual to establish an association with the correct partners in the absence of signaling.     

Food, vigilance, and sperm: the role of male direct benefits in the evolution of female preference in a polygamous bird

The adaptive significance of female selection of copulationpartners remains unresolved, particularly in polygamous specieswhere males do not provide paternal care. In these species thepossibility that direct benefits other than paternal care mayplay an important role in the evolution of female choice hasreceived little attention. I tested whether direct benefitsare associated with female choice in the polygamous feral fowl,Gallus g. domesticus, where females prefer socially dominantcopulation partners and males do not care for the young butdo provide females with three commodities: food, vigilance,and sperm. I used a combination of empirical and experimentaldata to show that male propensity to offer food and vigilance,but not sperm, was positively associated with male social status,suggesting that the provision of these resources may be costlyand condition dependent in males. Copulation success was correlatedwith male status but not with the number of feedings a femalereceived from a male, indicating that a female preferred dominantpartners that in general provided any female with more food,rather than partners that provided only her with more food,consistent with the idea that females may use male resourceprovisioning as a proximate mechanism to assess male condition.Together, these results indicate that male resources provisioningis (1) tightly linked to male social status, (2) a potentialindicator of male condition and possibly genetic quality, and(3) a potential criterion for females to select dominant partners,thus playing an important role in the evolution of partner choiceeven in polygamous species lacking paternal care.     

The impact of transmission mode on the evolution of benefits provided by microbial symbionts

While past work has often examined the effects of transmission mode on virulence evolution in parasites, few studies have explored the impact of horizontal transmission on the evolution of benefits conferred by a symbiont to its host. Here, we identify three mechanisms that create a positive covariance between horizontal transmission and symbiont‐provided benefits: pleiotropy within the symbiont genome, partner choice by the host, and consumption of host waste by‐products by symbionts. We modify a susceptible‐infected model to incorporate the details of each mechanism and examine the evolution of symbiont benefits given variation in either the immigration rate of susceptible hosts or the rate of successful vertical transmission. We find conditions for each case under which greater opportunity for horizontal transmission (higher migration rate) favors the evolution of mutualism. Further, we find the surprising result that vertical transmission can inhibit the evolution of benefits provided by symbionts to hosts when horizontal transmission and symbiont‐provided benefits are positively correlated. These predictions may apply to a number of natural systems, and the results may explain why many mutualisms that rely on partner choice often lack a mechanism for vertical transmission.     

Cheating can stabilize cooperation in mutualisms

Mutualisms present a challenge for evolutionary theory. How is cooperation maintained in the face of selection for selfishness and cheating? Both theory and data suggest that partner choice, where one species preferentially directs aid to the more cooperative members of the other species, is central to cooperation in many mutualisms. However, the theory has only so far considered the evolutionary effects of partner choice on one of the species in a mutualism in isolation. Here, we investigate the co-evolution of cooperation and choice in a choosy host and its symbiont. Our model reveals that even though choice and cooperation may be initially selected, it will often be unstable. This is because choice reduces variation in the symbiont and, therefore, tends to remove the selective incentive for its own maintenance (a scenario paralleled in the lek paradox in female choice and policing in within-species cooperation). However, we also show that when variability is reintroduced into symbionts each generation, in the form of less cooperative individuals, choice is maintained. This suggests that the presence of cheaters and cheater species in many mutualisms is central to the maintenance of partner choice and, paradoxically, cooperation itself.     

Local and systemic N signaling are involved in Medicago truncatula preference for the most efficient Sinorhizobium symbiotic partners

? Responses of the Medicago truncatula-Sinorhizobium interaction to variation in N?-fixation of the bacterial partner were investigated. ? Split-root systems were used to discriminate between local responses, at the site of interaction with bacteria, and systemic responses related to the whole plant N status. ? The lack of N acquisition by a half-root system nodulated with a nonfixing rhizobium triggers a compensatory response enabling the other half-root system nodulated with N?-fixing partners to compensate the local N limitation. This response is mediated by a stimulation of nodule development (number and size) and involves a systemic signaling mechanism related to the plant N demand. In roots co-infected with poorly and highly efficient strains, partner choice for nodule formation was not modulated by the plant N status. However, the plant N demand induced preferential expansion of nodules formed with the most efficient partners when the symbiotic organs were functional. The response of nodule expansion was associated with the stimulation of symbiotic plant cell multiplication and of bacteroid differentiation. ? A general model where local and systemic N signaling mechanisms modulate interactions between Medicago truncatula and its Sinorhizobium partners is proposed.     

Design of multi-specificity in protein interfaces

Interactions in protein networks may place constraints on protein interface sequences to maintain correct and avoid unwanted interactions. Here we describe a “multi-constraint” protein design protocol to predict sequences optimized for multiple criteria, such as maintaining sets of interactions, and apply it to characterize the mechanism and extent to which 20 multi-specific proteins are constrained by binding to multiple partners. We find that multi-specific binding is accommodated by at least two distinct patterns. In the simplest case, all partners share key interactions, and sequences optimized for binding to either single or multiple partners recover only a subset of native amino acid residues as optimal. More interestingly, for signaling interfaces functioning as network “hubs,” we identify a different, “multi-faceted” mode, where each binding partner prefers its own subset of wild-type residues within the promiscuous binding site. Here, integration of preferences across all partners results in sequences much more “native-like” than seen in optimization for any single binding partner alone, suggesting these interfaces are substantially optimized for multi-specificity. The two strategies make distinct predictions for interface evolution and design. Shared interfaces may be better small molecule targets, whereas multi-faceted interactions may be more “designable” for altered specificity patterns. The computational methodology presented here is generalizable for examining how naturally occurring protein sequences have been selected to satisfy a variety of positive and negative constraints, as well as for rationally designing proteins to have desired patterns of altered specificity.     

Partner choice in Gobiid fish Myersina macrostoma living in association with the alpheid shrimp Alpheus rapax

Partner choice is an important selective force in mutualistic partnerships. Although several aspects of mutualism have been well-studied, partner choice remains a novel aspect in the study of marine mutualists. Previous research on the goby-shrimp mutualism suggested that visual cues affect the ability of gobies to discriminate between potential shrimp partners but small sample sizes limited the generalization of that result. Here, primary partner choice in Myersina macrostoma was investigated in a series of ex situ experiments. Results indicated that shrimp-associated gobies relied on visual cues in partner choice. The goby M. macrostoma was clearly able to discern between different shelter types, demonstrating a preference for burrows compared to rocks. While they were attracted to larger burrows, they were not visually attracted to larger shrimp partners. This indicates that in wild populations, intraspecific competition for larger burrows might be the driving factor in size assortment in associated partners. Myersina macrostoma could also discern between species of shrimps in laboratory experimental set-ups, indicating a clear preference for A. rapax which they naturally occur with, but not to A. lobidens, which occurs at the same locality but with which they do not naturally associate. These findings offer fundamental building blocks towards the broader understanding of partnership formations in marine mutualists.     

Avoiding the bullies: The resilience of cooperation among unequals

Can egalitarian norms or conventions survive the presence of dominant individuals who are ensured of victory in conflicts? We investigate the interaction of power asymmetry and partner choice in games of conflict over a contested resource. Previous models of cooperation do not include both power inequality and partner choice. Furthermore, models that do include power inequalities assume a static game where a bully’s advantage does not change. They have therefore not attempted to model complex and realistic properties of social interaction. Here, we introduce three models to study the emergence and resilience of cooperation among unequals when interaction is random, when individuals can choose their partners, and where power asymmetries dynamically depend on accumulated payoffs. We find that the ability to avoid bullies with higher competitive ability afforded by partner choice mostly restores cooperative conventions and that the competitive hierarchy never forms. Partner choice counteracts the hyper dominance of bullies who are isolated in the network and eliminates the need for others to coordinate in a coalition. When competitive ability dynamically depends on cumulative payoffs, complex cycles of coupled network-strategy-rank changes emerge. Effective collaborators gain popularity (and thus power), adopt aggressive behavior, get isolated, and ultimately lose power. Neither the network nor behavior converge to a stable equilibrium. Despite the instability of power dynamics, the cooperative convention in the population remains stable overall and long-term inequality is completely eliminated. The interaction between partner choice and dynamic power asymmetry is crucial for these results: without partner choice, bullies cannot be isolated, and without dynamic power asymmetry, bullies do not lose their power even when isolated. We analytically identify a single critical point that marks a phase transition in all three iterations of our models. This critical point is where the first individual breaks from the convention and cycles start to emerge.     

Parabiotic ants: the costs and benefits of symbiosis

1. Mutualisms are important drivers of co‐evolution and speciation. However, they typically imply costs for one or both partners. Each partner consequently tries to maximise benefits and minimise costs. Mutualisms can therefore develop towards commensalism or parasitism if one partner fails to provide sufficient benefits. This is particularly likely in diffuse interactions, where multiple species can associate with each other. If costs and benefits of a species vary with the identity of the partner species, this may result in a geographical mosaic of co‐evolution. 2. In the present study, inter‐specific interactions in two parabiotic associations of ants were studied (Hymenoptera: Formicidae). One Crematogaster species was associated with one of two closely related Camponotus species. We assessed cost and benefits by studying behavioural interactions, foraging behaviour, and nest defence in the associations. 3. While parabioses had been shown to be mutualistic, evidence was found for exploitation and aggressive competition between species. In spite of apparent costs of being exploited, we found no benefits for one partner (Crematogaster). The magnitude of potential costs to Crematogaster varied between the two Camponotus species. 4. We conclude that the cost/benefit ratio for Crematogaster varies between the two Camponotus partners, and between environmental conditions. Parabiosis can thus fluctuate between mutualism, commensalism, and parasitism, with Crematogaster being the species that may have higher costs than benefits. 5. We suggest that geneflow in the Crematogaster population hinders local adaptation to the resulting mosaic of locally varying selection pressures. This study demonstrates how diffuse interactions and environmental variation can result in a complex of local selection pressures.     

Why mutual helping in most natural systems is neither conflict-free nor based on maximal conflict

Mutual helping for direct benefits can be explained by various game theoretical models, which differ mainly in terms of the underlying conflict of interest between two partners. Conflict is minimal if helping is self-serving and the partner benefits as a by-product. In contrast, conflict is maximal if partners are in a prisoner''s dilemma with both having the pay-off-dominant option of not returning the other''s investment. Here, we provide evolutionary and ecological arguments for why these two extremes are often unstable under natural conditions and propose that interactions with intermediate levels of conflict are frequent evolutionary endpoints. We argue that by-product helping is prone to becoming an asymmetric investment game since even small variation in by-product benefits will lead to the evolution of partner choice, leading to investments by the chosen class. Second, iterated prisoner''s dilemmas tend to take place in stable social groups where the fitness of partners is interdependent, with the effect that a certain level of helping is self-serving. In sum, intermediate levels of mutual helping are expected in nature, while efficient partner monitoring may allow reaching higher levels.     

Coevolutionary dynamics in one-to-many mutualistic systems

“One-to-many” mutualisms are often observed in nature. In this type of mutualism, each host individual can interact with many symbionts, whereas each individual symbiont can interact with only one host individual. Partner choice by the host is a potentially critical mechanism for maintaining such systems; however, its long-term effects on the coevolution between the hosts and symbionts have not been completely explored. In this study, I developed a simple mathematical model to describe the coevolutionary dynamics between hosts and symbionts in a one-to-many mutualism. I assumed that each host chooses a constant number of symbionts from a potential symbiont population, a fraction of which are chosen through preferential choice on the basis of the cooperativeness of the symbionts and the rest are chosen randomly. Using numerical calculations, I found that mutualism is maintained when the preferential choice is not very costly and the mutation rate of symbionts is large. I also found that symbionts that receive benefits from hosts without a return (cheater symbionts) and hosts that do not engage in preferential partner choice (indiscriminator hosts) can coexist with mutualist symbionts and discriminator hosts, respectively. The parameter domain of pure mutualism, i.e., free from cheater symbionts and indiscriminator hosts, can be narrower than the whole domain where the mutualism persists.     

Partner choice in human evolution: The role of cooperation,foraging ability,and culture in Hadza campmate preferences

The ability to choose the partners we interact with is thought to have been an important driver in the evolution of human social behavior, and in particular, our propensity to cooperate. Studies showing that humans prefer to interact with cooperative others is often cited as support for partner choice driving the evolution of cooperation. However, these studies are largely drawn from Western samples, where conditions for partner choice to operate may be especially favorable. Here, we investigate qualities associated with being a preferred partner (i.e., campmate) in Hadza hunter-gatherers of Tanzania in 2016 and 2019. A total of 156 Hadza participants from 17 camps ranked their campmates on generosity, foraging ability, and their preference for them as future campmates. In 2016, Hadza preferred more generous people and better hunters as campmates, with evidence suggesting a stronger preference for better hunters; however, the relationship between generosity and being a preferred campmate was greater in 2019 than in 2016, such that the preference for generous people was stronger than the preference for better foragers, suggesting that campmate preferences are changing. These new findings contrast with reports on data from nearly a decade ago, suggesting that the Hadza do not prefer more cooperative campmates. Further, in 2019, there was anecdotal evidence that Hadza with greater exposure to outside cultural institutions (e.g., schooling, having a job, or living in a village) had a stronger preference for generous campmates than those with less exposure. Taken together, the results suggest that preferences for social partners may, in part, be culturally shaped.     

No Short‐Term Contingency Between Grooming and Food Tolerance in Barbary Macaques (Macaca sylvanus)

The exchange of services such as allo‐grooming, allo‐preening, food tolerance and agonistic support has been observed in a range of species. Two proximate mechanisms have been proposed to explain the exchanges of services in animals. First, an animal can give a service to a partner depending on how the partner behaved towards it in the recent past. This mechanism is usually tested by examining the within‐dyad temporal relation between events given and received over short time periods. Second, the partner choice mechanism assumes that animals give favours towards specific partners but not others, by comparing how each partner behaved towards them over longer time frames. As such, the partner choice mechanism does not make specific predictions on a temporal contingency between services received and given over short time frames. While there is evidence for a long‐term positive correlation between services exchanged in animals, results for short‐term contingencies between services given and received are mixed. Our study investigated the exchange of grooming for food tolerance in a partially provisioned group of Barbary macaques, by analysing the short‐term contingency between these events. Tolerance over food was compared immediately after grooming and in control condition, using food of different shareability. We found no evidence that grooming increases food tolerance or decrease aggression around food in the short term. Food tolerance was affected by the shareability of the food and the sex of the partners. The exchanges of grooming and food tolerance in non‐human primates may be little affected by recent single events. We suggest that long‐term exchanges between services given and received and social partner choice may play a more important role in explaining social interactions than short‐term contingent events.     

Homology Search and Choice of Homologous Partner during Mitotic Recombination

Homologous recombination is an important DNA repair mechanism in vegetative cells. During the repair of double-strand breaks, genetic information is transferred between the interacting DNA sequences (gene conversion). This event is often accompanied by a reciprocal exchange between the homologous molecules, resulting in crossing over. The repair of DNA damage by homologous recombination with repeated sequences dispersed throughout the genome might result in chromosomal aberrations or in the inactivation of genes. It is therefore important to understand how the suitable homologous partner for recombination is chosen. We have developed a system in the yeast Saccharomyces cerevisiae that can monitor the fate of a chromosomal double-strand break without the need to select for recombinants. The broken chromosome is efficiently repaired by recombination with one of two potential partners located elsewhere in the genome. One of the partners has homology to the broken ends of the chromosome, whereas the other is homologous to sequences distant from the break. Surprisingly, a large proportion of the repair is carried out by recombination involving the sequences distant from the broken ends. This repair is very efficient, despite the fact that it requires the processing of a large chromosomal region flanking the break. Our results imply that the homology search involves extensive regions of the broken chromosome and is not carried out exclusively by sequences adjacent to the double-strand break. We show that the mechanism that governs the choice of homologous partners is affected by the length and sequence divergence of the interacting partners, as well as by mutations in the mismatch repair genes. We present a model to explain how the suitable homologous partner is chosen during recombinational repair. The model provides a mechanism that may guard the integrity of the genome by preventing recombination between dispersed repeated sequences.     

Gibt es einen „Duft der MHC‐Gene“?

MHC‐Genes: Do they influence the choice of partners via olfactory signals? Behavioral experiments in mice and humans suggest that genes of the major histocompatibilty complex (MHC) may be important for the differentiation of self and non‐self during mate choice. While this correlation is well documented for certain mouse strains, it is controversial for humans. Signal transfer between potential partners is considered to occur via the production of MHC‐dependent olfactory cues by a sender and their recognition by olfaction in the recipient. It is shown that in mice and humans the overall bouquet of volatiles is not and the pattern of peptides in mice is only marginally influenced by the MHC genes. However, in mice, olfactory cues without MHC contribution appear to play a role in mate choice, in that the profile learned from the parents during rearing is compared with the distinct profile of a potential partner, which is in turn selected for mating. Such olfactory differentiation between close relatives and potential mates without MHC‐contribution may also operate unconsciously in humans.     

A sex-specific trade-off between mating preferences for genetic compatibility and body size in a cichlid fish with mutual mate choice

Mating preferences for genetic compatibility strictly depend on the interplay of the genotypes of potential partners and are therein fundamentally different from directional preferences for ornamental secondary sexual traits. Thus, the most compatible partner is on average not the one with most pronounced ornaments and vice versa. Hence, mating preferences may often conflict. Here, we present a solution to this problem while investigating the interplay of mating preferences for relatedness (a compatibility criterion) and large body size (an ornamental or quality trait). In previous experiments, both sexes of Pelvicachromis taeniatus, a cichlid fish with mutual mate choice, showed preferences for kin and large partners when these criteria were tested separately. In the present study, test fish were given a conflicting choice between two potential mating partners differing in relatedness as well as in body size in such a way that preferences for both criteria could not simultaneously be satisfied. We show that a sex-specific trade-off occurs between mating preferences for body size and relatedness. For females, relatedness gained greater importance than body size, whereas the opposite was true for males. We discuss the potential role of the interplay between mating preferences for relatedness and body size for the evolution of inbreeding preference.     

Partner choice creates fairness in humans

Many studies demonstrate that partner choice has played an important role in the evolution of human cooperation, but little work has tested its impact on the evolution of human fairness. In experiments involving divisions of money, people become either over-generous or over-selfish when they are in competition to be chosen as cooperative partners. Hence, it is difficult to see how partner choice could result in the evolution of fair, equal divisions. Here, we show that this puzzle can be solved if we consider the outside options on which partner choice operates. We conduct a behavioural experiment, run agent-based simulations and analyse a game-theoretic model to understand how outside options affect partner choice and fairness. All support the conclusion that partner choice leads to fairness only when individuals have equal outside options. We discuss how this condition has been met in our evolutionary history, and the implications of these findings for our understanding of other aspects of fairness less specific than preferences for equal divisions of resources.     

The evolution of alternative cryptic female choice strategies in age-structured populations

Abstract.— Cryptic female choice is a potentially important aspect of the sexual selection process. According to the theory of sexual dialectics, postcopulation manipulation of relative male fertilization success can provide an avenue by which females can circumvent attempts by males to control female reproduction. Here I use stochastic models to investigate the evolution of cryptic female choice in populations with and without age structure. In populations without age structure, cryptic female choice will evolve only when (1) precopulatory mate choice by females is inefficient, (2) variation in male fitness is correlated with a trait upon which a female can base her choice of mates, and (3) the cost of multiple mating is not too high. In populations with age structure, similar conditions apply. However, selection sometimes favors females that employ alternative strategies of female choice at different ages. These results help to define the types of biological systems in which we should expect to see the evolution of cryptic female choice. They also illustrate that the evolution of choice strategies in females may be complex and may mirror in some important respects the evolution of alternative mating tactics in males.     

Phylogenetic structure of specialization: A new approach that integrates partner availability and phylogenetic diversity to quantify biotic specialization in ecological networks

Biotic specialization holds information about the assembly, evolution, and stability of biological communities. Partner availabilities can play an important role in enabling species interactions, where uneven partner availabilities can bias estimates of biotic specialization when using phylogenetic diversity indices. It is therefore important to account for partner availability when characterizing biotic specialization using phylogenies. We developed an index, phylogenetic structure of specialization (PSS), that avoids bias from uneven partner availabilities by uncoupling the null models for interaction frequency and phylogenetic distance. We incorporate the deviation between observed and random interaction frequencies as weights into the calculation of partner phylogenetic α‐diversity. To calculate the PSS index, we then compare observed partner phylogenetic α‐diversity to a null distribution generated by randomizing phylogenetic distances among the same number of partners. PSS quantifies the phylogenetic structure (i.e., clustered, overdispersed, or random) of the partners of a focal species. We show with simulations that the PSS index is not correlated with network properties, which allows comparisons across multiple systems. We also implemented PSS on empirical networks of host–parasite, avian seed‐dispersal, lichenized fungi–cyanobacteria, and hummingbird pollination interactions. Across these systems, a large proportion of taxa interact with phylogenetically random partners according to PSS, sometimes to a larger extent than detected with an existing method that does not account for partner availability. We also found that many taxa interact with phylogenetically clustered partners, while taxa with overdispersed partners were rare. We argue that species with phylogenetically overdispersed partners have often been misinterpreted as generalists when they should be considered specialists. Our results highlight the important role of randomness in shaping interaction networks, even in highly intimate symbioses, and provide a much‐needed quantitative framework to assess the role that evolutionary history and symbiotic specialization play in shaping patterns of biodiversity. PSS is available as an R package at https://github.com/cjpardodelahoz/pss.