Emily I. Jones

Cheaters must prosper: reconciling theoretical and empirical perspectives on cheating in mutualism

Cheating is a focal concept in the study of mutualism, with the majority of researchers considering cheating to be both prevalent and highly damaging. However, current definitions of cheating do not reliably capture the evolutionary threat that has been a central motivation for the study of cheating. We describe the development of the cheating concept and distill a relative-fitness-based definition of cheating that encapsulates the evolutionary threat posed by cheating, i.e. that cheaters will spread and erode the benefits of mutualism. We then describe experiments required to conclude that cheating is occurring and to quantify fitness conflict more generally. Next, we discuss how our definition and methods can generate comparability and integration of theory and experiments, which are currently divided by their respective prioritisations of fitness consequences and traits. To evaluate the current empirical evidence for cheating, we review the literature on several of the best-studied mutualisms. We find that although there are numerous observations of low-quality partners, there is currently very little support from fitness data that any of these meet our criteria to be considered cheaters. Finally, we highlight future directions for research on conflict in mutualisms, including novel research avenues opened by a relative-fitness-based definition of cheating.

The fundamental role of competition in the ecology and evolution of mutualisms

Abstract  Mutualisms are interspecific interactions that yield reciprocal benefits. Here, by adopting a consumer–resource perspective, we show how considering competition is necessary in order to understand the evolutionary and ecological dynamics of mutualism. We first review the ways in which competition shapes the ecology of mutualisms, using a graphical framework based on resource flows rather than net effects to highlight the opportunities for competition. We then describe the known mechanisms of competition and show how it is a critical driver of the evolutionary dynamics, persistence, and diversification of mutualism. We argue that empirical and theoretical research on the ecology and evolution of mutualisms will jointly progress by addressing four key points: (i) the existence and shape of physiological trade‐offs among cooperation, competition, and other life‐history and functional traits; (ii) the capacity for individuals to express conditional responses to variation in their mutualistic and competitive environment; (iii) the existence of heritable variation for mutualistic and competitive traits and their potentially conditional expression; and (iv) the structure of the network of consumer–resource interactions in which individuals are embedded.

Eco‐Evolutionary Dynamics of Mutualists and Exploiters

With the growing recognition of exploiters as a prominent and enduring feature of many mutualisms, there is a need to understand the ecological and evolutionary dynamics of mutualisms in the context of exploitation. Here, we model coevolution between mutualist and exploiter birth rates, using an obligate pollinating seed parasite mutualism associated with a nonpollinating exploiter as a reference system. In this system, mutualist and exploiter larvae parasitize the host plant, competing for and consuming seeds. Evolution of the mutualist determines which exploiters can invade successfully. Subsequent coevolution with an exploiter has a strong, predictable influence on mutualist‐exploiter coexistence, mutualist and exploiter phenotypes, and species abundances. Weak mutualist competition promotes “evolutionary purging” of the exploiter, while weak exploiter competition leads to “evolutionary suicide” of the system. When stable, long‐term coexistence occurs, we identify two main “trait‐abundance syndromes” that have three novel implications. (1) Persistent, highly parasitic exploiters can be favored by coevolution. (2) Even then, the density of coevolved mutualists can be high. (3) Low plant density results primarily from the evolution of mutualist, not exploiter, birth rate and density. To evaluate these predictions, studies are needed that identify and compare populations with and without exploiters and compare life‐history traits of mutualists and exploiters.

Biotic Interactions, Rapid Evolution, and the Establishment of Introduced Species

The biotic environment can pose a challenge to introduced species; however, it is not known how rapid evolution in introduced and resident species influences the probability that the introduced species will become established. Here, we analyze the establishment phase of invasion with eco-evolutionary models of introduced species involved in predator-prey, mutualistic, or competitive interactions with a resident species. We find that, depending on the strength of the biotic interaction, establishment is impossible, guaranteed, or, in a narrow range, determined by genetic variation. Over this narrow range, rapid evolution of the introduced species always favors establishment, whereas resident evolution may either inhibit or facilitate establishment, depending on the interaction type. Coevolution can also either increase or decrease the chance of establishment, depending on the initial genotype frequencies as well as the interaction type. Our results suggest that the conditions under which genetic variation influences establishment success are limited, but they highlight the importance of considering the resident community’s evolutionary response to introduced species as a component of its invasibility.

Segregate or cooperate- a study of the interaction between two species of Dictyostelium

BackgroundA major challenge for evolutionary biology is explaining altruism, particularly when it involves death of one party and occurs across species. Chimeric fruiting bodies of Dictyostelium discoideum and Dictyostelium purpureum develop from formerly independent amoebae, and some die to help others. Here we examine co-aggregation between D. discoideum and D. purpureum, determine its frequency and which party benefits, and the extent of fair play in contribution to the altruistic caste.ResultsWe mixed cells from both species in equal proportions, and then we analyzed 198 individual fruiting bodies, which always had either a D. discoideum or D. purpureum phenotype (D. discoideum- 98, D. purpureum- 100). Fifty percent of the fruiting bodies that looked like D. discoideum and 22% of the fruiting bodies that looked like D. purpureum were chimeric, though the majority of spores in any given fruiting body belonged to one species (D. discoideum fruiting bodies- 0.85 ± 0.03, D. purpureum fruiting bodies- 0.94 ± 0.02). Clearly, there is species level recognition occurring that keeps the cells mostly separate. The number of fruiting bodies produced with the D. discoideum phenotype increased from 225 ± 32 fruiting bodies when D. discoideum was alone to 486 ± 61 in the mix treatments. However, the number of D. discoideum spores decreased, although not significantly, from 2.75e7 ± 1.29e7 spores in the controls to 2.06e7 ± 8.33e6 spores in the mix treatments. D. purpureum fruiting body and spore production decreased from 719 ± 111 fruiting bodies and 5.81e7 ± 1.26e7 spores in the controls to 394 ± 111 fruiting bodies and 9.75e6 ± 2.25e6 spores in the mix treatments.ConclusionBoth species appear to favor clonality but can cooperate with each other to produce fruiting bodies. Cooperating amoebae are able to make larger fruiting bodies, which are advantageous for migration and dispersal, but both species here suffer a cost in producing fewer spores per fruiting body.

The Trail Less Traveled: Individual Decision-Making and Its Effect on Group Behavior

Social insect colonies are complex systems in which the interactions of many individuals lead to colony-level collective behaviors such as foraging. However, the emergent properties of collective behaviors may not necessarily be adaptive. Here, we examine symmetry breaking, an emergent pattern exhibited by some social insects that can lead colonies to focus their foraging effort on only one of several available food patches. Symmetry breaking has been reported to occur in several ant species. However, it is not clear whether it arises as an unavoidable epiphenomenon of pheromone recruitment, or whether it is an adaptive behavior that can be controlled through modification of the individual behavior of workers. In this paper, we used a simulation model to test how symmetry breaking is affected by the degree of non-linearity of recruitment, the specific mechanism used by individuals to choose between patches, patch size, and forager number. The model shows that foraging intensity on different trails becomes increasingly asymmetric as the recruitment response of individuals varies from linear to highly non-linear, supporting the predictions of previous work. Surprisingly, we also found that the direction of the relationship between forager number (i.e., colony size) and asymmetry varied depending on the specific details of the decision rule used by individuals. Limiting the size of the resource produced a damping effect on asymmetry, but only at high forager numbers. Variation in the rule used by individual ants to choose trails is a likely mechanism that could cause variation among the foraging behaviors of species, and is a behavior upon which selection could act.

Revisiting Darwin's conundrum reveals a twist on the relationship between phylogenetic distance and invasibility

Significance The application of phylogenetics is rapidly growing in many areas of biology. In invasion biology, phylogenetic information is now being used in an attempt to understand and predict species invasions. However, there is only a weak foundation for the prevalent predictions of how the phylogenetic distance between native and nonnative species should be related to the invasion success of the nonnative species. In this paper, a mechanistic model of species interactions and evolution is used to generate a unique set of predictions. These predictions deviate significantly from those assumed previously, suggesting that current explanations of phylogenetic distance–invasion relationships must be reevaluated. More generally, the results highlight the importance of considering the details of community processes when interpreting phylogenetic patterns. A key goal of invasion biology is to identify the factors that favor species invasions. One potential indicator of invasiveness is the phylogenetic distance between a nonnative species and species in the recipient community. However, predicting invasiveness using phylogenetic information relies on an untested assumption: that both biotic resistance and facilitation weaken with increasing phylogenetic distance. We test the validity of this key assumption using a mathematical model in which a novel species is introduced into communities with varying ecological and phylogenetic relationships. Contrary to what is generally assumed, we find that biotic resistance and facilitation can either weaken or intensify with phylogenetic distance, depending on the mode of interspecific interactions (phenotype matching or phenotype differences) and the resulting evolutionary trajectory of the recipient community. Thus, we demonstrate that considering the mechanisms that drive phenotypic divergence between native and nonnative species can provide critical insight into the relationship between phylogenetic distance and invasibility.

Synthesizing perspectives on the evolution of cooperation within and between species

Cooperation is widespread both within and between species, but are intraspecific and interspecific cooperation fundamentally similar or qualitatively different phenomena? This review evaluates this question, necessary for a general understanding of the evolution of cooperation. First, we outline three advantages of cooperation relative to noncooperation (acquisition of otherwise inaccessible goods and services, more efficient acquisition of resources, and buffering against variability), and predict when individuals should cooperate with a conspecific versus a heterospecific partner to obtain these advantages. Second, we highlight five axes along which heterospecific and conspecific partners may differ: relatedness and fitness feedbacks, competition and resource use, resource‐generation abilities, relative evolutionary rates, and asymmetric strategy sets and outside options. Along all of these axes, certain asymmetries between partners are more common in, but not exclusive to, cooperation between species, especially complementary resource use and production. We conclude that cooperation within and between species share many fundamental qualities, and that differences between the two systems are explained by the various asymmetries between partners. Consideration of the parallels between intra‐ and interspecific cooperation facilitates application of well‐studied topics in one system to the other, such as direct benefits within species and kin‐selected cooperation between species, generating promising directions for future research.