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.

Microbial Inoculants: Silver Bullet or Microbial Jurassic Park?

The appeal of using microbial inoculants to mediate plant traits and productivity in managed ecosystems has increased over the past decade, because microbes represent an alternative to fertilizers, pesticides, and direct genetic modification of plants. Using microbes bypasses many societal and environmental concerns because microbial products are considered a more sustainable and benign technology. In our desire to harness the power of plant-microbial symbioses, are we ignoring the possibility of precipitating microbial invasions, potentially setting ourselves up for a microbial Jurassic Park? Here, we outline potential negative consequences of microbial invasions and describe a set of practices (Testing, Regulation, Engineering, and Eradication, TREE) based on the four stages of invasion to prevent microbial inoculants from becoming invasive. We aim to stimulate discussion about best practices to proactively prevent microbial invasions.

Rapid evolution of Medicago polymorpha during invasion shifts interactions with the soybean looper.

The Enemy Release Hypothesis posits that invasion of novel habitats can be facilitated by the absence of coevolved herbivores. However, a new environment and interactions with unfamiliar herbivores may impose selection on invading plants for traits that reduce their attractiveness to herbivores or for enhanced defenses compared to native host plants, leading to a pattern similar to enemy release but driven by evolutionary change rather than ecological differences. The Shifting Defense Hypothesis posits that plants in novel habitats will shift from specialized defense mechanisms to defense mechanisms effective against generalist herbivores in the new range. We tested these ideas by comparing herbivore preference and performance of native (Eurasia)- and invasive (New World)-range Medicago polymorpha, using a generalist herbivore, the soybean looper, that co-occurs with M. polymorpha in its New World invaded range. We found that soybean loopers varied in preference and performance depending on host genotype and that overall the herbivore preferred to consume plant genotypes from naïve populations from Eurasia. This potentially suggests that range expansion of M. polymorpha into the New World has led to rapid evolution of a variety of traits that have helped multiple populations become established, including those that may allow invasive populations to resist herbivory. Thus, enemy release in a novel range can occur through rapid evolution by the plant during invasion, as predicted by the Shifting Defense Hypothesis, rather than via historical divergence.

A high-throughput method of analyzing multiple plant defensive compounds in minimized sample mass.

PREMISE OF THE STUDY: Current methods for quantifying herbivore-induced alterations in plant biochemistry are often unusable by researchers due to practical constraints. We present a cost-effective, high-throughput protocol to quantify multiple biochemical responses from small plant tissue samples using spectrophotometric techniques. METHODS AND RESULTS: Using Solanum lycopersicum and Medicago polymorpha leaves pre- and post-herbivory, we demonstrate that our protocol quantifies common plant defense responses: peroxidase production, polyphenol oxidase production, reactive oxygen species production, total protein production, and trypsin-like protease inhibition activity. CONCLUSIONS: Current protocols can require 500 mg of tissue, but our assays detect activity in less than 10 mg. Our protocol takes two people 6 h to run any of the assays on 300 samples in triplicate, or all of the assays on 20 samples. Our protocol enables researchers to plan complex experiments that compare local versus systemic plant responses, quantify environmental and genetic variation, and measure population-level variation.

Migration in the social stage of Dictyostelium discoideum amoebae impacts competition.

Interaction conditions can change the balance of cooperation and conflict in multicellular groups. After aggregating together, cells of the social amoeba Dictyostelium discoideum may migrate as a group (known as a slug) to a new location. We consider this migration stage as an arena for social competition and conflict because the cells in the slug may not be from a genetically homogeneous population. In this study, we examined the interplay of two seemingly diametric actions, the solitary action of kin recognition and the collective action of slug migration in D. discoideum, to more fully understand the effects of social competition on fitness over the entire lifecycle. We compare slugs composed of either genetically homogenous or heterogeneous cells that have migrated or remained stationary in the social stage of the social amoeba Dictyostelium discoideum. After migration of chimeric slugs, we found that facultative cheating is reduced, where facultative cheating is defined as greater contribution to spore relative to stalk than found for that clone in the clonal state. In addition our results support previous findings that competitive interactions in chimeras diminish slug migration distance. Furthermore, fruiting bodies have shorter stalks after migration, even accounting for cell numbers at that time. Taken together, these results show that migration can alleviate the conflict of interests in heterogeneous slugs. It aligns their interest in finding a more advantageous place for dispersal, where shorter stalks suffice, which leads to a decrease in cheating behavior.

Structured growth and genetic drift raise relatedness in the social amoeba Dictyostelium discoideum.

One condition for the evolution of altruism is genetic relatedness between altruist and beneficiary, often achieved through active kin recognition. Here, we investigate the power of a passive process resulting from genetic drift during population growth in the social amoeba Dictyostelium discoideum. We put labelled and unlabelled cells of the same clone in the centre of a plate, and allowed them to proliferate outward. Zones formed by genetic drift owing to the small population of actively growing cells at the colony edge. We also found that single cells could form zones of high relatedness. Relatedness increased at a significantly higher rate when food was in short supply. This study shows that relatedness can be significantly elevated before the social stage without a small founding population size or recognition mechanism.

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

BACKGROUND: A 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. RESULTS: We 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. CONCLUSION: Both 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.

Social evolution: kin preference in a social microbe.

Kin recognition helps cooperation to evolve in many animals, but it is uncertain whether microorganisms can also use it to focus altruistic behaviour on relatives. Here we show that the social amoeba Dictyostelium purpureum prefers to form groups with its own kin in situations where some individuals die to assist others. By directing altruism towards kin, D. purpureum should generally avoid the costs of chimaerism experienced by the related D. discoideum.