Peter C. Zee

Rapid and widespread de novo evolution of kin discrimination

Significance Relatedness-dependent behavior modification is common among social organisms and has been a major feature of social evolution theory for decades. However, the evolutionary causes of kin discrimination are often unclear. Here, we document many spontaneous origins of kin discrimination in a social microbe that appear to arise as indirect byproducts of adaptation at other traits and we show that kin discrimination evolves by diverse genetic mechanisms. Diverse forms of kin discrimination, broadly defined as alteration of social behavior as a function of genetic relatedness among interactants, are common among social organisms from microbes to humans. However, the evolutionary origins and causes of kin-discriminatory behavior remain largely obscure. One form of kin discrimination observed in microbes is the failure of genetically distinct colonies to merge freely upon encounter. Here, we first use natural isolates of the highly social bacterium Myxococcus xanthus to show that colony-merger incompatibilities can be strong barriers to social interaction, particularly by reducing chimerism in multicellular fruiting bodies that develop near colony-territory borders. We then use experimental laboratory populations to test hypotheses regarding the evolutionary origins of kin discrimination. We show that the generic process of adaptation, irrespective of selective environment, is sufficient to repeatedly generate kin-discriminatory behaviors between evolved populations and their common ancestor. Further, we find that kin discrimination pervasively evolves indirectly between allopatric replicate populations that adapt to the same ecological habitat and that this occurs generically in many distinct habitats. Patterns of interpopulation discrimination imply that kin discrimination phenotypes evolved via many diverse genetic mechanisms and mutation-accumulation patterns support this inference. Strong incompatibility phenotypes emerged abruptly in some populations but strengthened gradually in others. The indirect evolution of kin discrimination in an asexual microbe is analogous to the indirect evolution of reproductive incompatibility in sexual eukaryotes and linguistic incompatibility among human cultures, the commonality being indirect, noncoordinated divergence of complex systems evolving in isolation.

Eco‐evolutionary dynamics in plant‐soil feedbacks

Summary In the past decade, ecologists have begun to more fully appreciate the role of evolution in explaining contemporary ecological processes. Evolution is most likely to affect ecological patterns when selection pressure is particularly strong, or when the generation time of at least one interacting species is relatively short. Interactions between plants and soil microbes are an excellent candidate for examining eco–evo interactions because interactions between organisms are tightly knit with the potential for species with relatively short generation times to impose strong selection on one another. Here, we examine the potential for eco–evolutionary dynamics in plant–soil feedbacks (PSFs). Genetic variation in plant traits and subsequent evolution of those traits can affect traits and species composition of soil microbial communities. Soil microbial communities can, in turn, alter the evolutionary trajectory of plant traits. Further, the direction and magnitude of PSFs can affect the plant community, which may alter the selection on plant traits via intra- and interspecific interactions. Finally, we consider how eco-evolutionary feedbacks might enhance or mitigate the effects of PSFs in driving the structure of natural plant communities.

MycoDB, a global database of plant response to mycorrhizal fungi

Plants form belowground associations with mycorrhizal fungi in one of the most common symbioses on Earth. However, few large-scale generalizations exist for the structure and function of mycorrhizal symbioses, as the nature of this relationship varies from mutualistic to parasitic and is largely context-dependent. We announce the public release of MycoDB, a database of 4,010 studies (from 438 unique publications) to aid in multi-factor meta-analyses elucidating the ecological and evolutionary context in which mycorrhizal fungi alter plant productivity. Over 10 years with nearly 80 collaborators, we compiled data on the response of plant biomass to mycorrhizal fungal inoculation, including meta-analysis metrics and 24 additional explanatory variables that describe the biotic and abiotic context of each study. We also include phylogenetic trees for all plants and fungi in the database. To our knowledge, MycoDB is the largest ecological meta-analysis database. We aim to share these data to highlight significant gaps in mycorrhizal research and encourage synthesis to explore the ecological and evolutionary generalities that govern mycorrhizal functioning in ecosystems.

Evolution in a Community Context: Trait Responses to Multiple Species Interactions*

Species that coexist in diverse natural communities interact in complex ways that alter each other’s abundances and affect selection on each other’s traits. Consequently, predicting trait evolution in natural communities may require understanding ecological and evolutionary dynamics involving a number of species. In August 2016, the American Society of Naturalists sponsored a symposium to explore evolution in a community context, focusing on microevolutionary processes. Here we provide an introduction to our perspectives on this topic by defining the context and describing some examples of when and how microevolutionary responses to multiple species may differ from evolution in isolation or in two-species communities. We find that indirect ecological and evolutionary effects can result in nonadditive selection and evolution that cannot be predicted from pairwise interactions. Genetic correlations of ecological traits in one species can alter trait evolution and adaptation as well as the abundances of other species. In general, evolution in multispecies communities can change ecological interactions, which then feed back to future evolutionary changes in ways that depend on these indirect effects. We suggest avenues for future research in this field, including determining the circumstances under which pairwise evolution does not adequately describe evolutionary trajectories.

A shift from magnitude to sign epistasis during adaptive evolution of a bacterial social trait

Although the importance of epistasis in evolution has long been recognized, remarkably little is known about the processes by which epistatic interactions evolve in real time in specific biological systems. Here, we have characterized how the epistatic fitness relationship between a social gene and an adapting genome changes radically over a short evolutionary time frame in the social bacterium Myxococcus xanthus. We show that a highly beneficial effect of this social gene in the ancestral genome is gradually reduced—and ultimately reversed into a deleterious effect—over the course of an experimental adaptive trajectory in which a primitive form of novel cooperation evolved. This reduction and reversal of a positive social allelic effect is driven solely by changes in the genetic context in which the gene is expressed as new mutations are sequentially fixed during adaptive evolution, and explicitly demonstrates a significant evolutionary change in the genetic architecture of an ecologically important social trait.

Evolutionary history shapes patterns of mutualistic benefit in Acacia-rhizobial interactions.

The ecological and evolutionary factors that drive the emergence and maintenance of variation in mutualistic benefit (i.e., the benefits provided by one partner to another) in mutualistic symbioses are not well understood. In this study, we evaluated the role that host and symbiont phylogeny might play in determining patterns of mutualistic benefit for interactions among nine species of Acacia and 31 strains of nitrogen‐fixing rhizobial bacteria. Using phylogenetic comparative methods we compared patterns of variation in mutualistic benefit (host response to inoculation) to rhizobial phylogenies constructed from housekeeping and symbiosis genes; and a multigene host phylogeny. We found widespread genotype‐by‐genotype variation in patterns of plant growth. A relatively large component of this variation (21–28%) was strongly influenced by the interacting evolutionary histories of both partners, such that phylogenetically similar host species had similar growth responses when inoculated with phylogenetically similar rhizobia. We also found a relatively large nonphylogenetic effect for the average mutualistic benefit provided by rhizobia to plants, such that phylogenetic relatedness did not predict the overall benefit provided by rhizobia across all hosts. We conclude that phylogenetic relatedness should frequently predict patterns of mutualistic benefit in acacia‐rhizobial mutualistic interactions; but that some mutualistic traits also evolve independently of the phylogenies.

Pervasive, yet idiosyncratic, epistatic pleiotropy during adaptation in a behaviourally complex microbe

Understanding how multiple mutations interact to jointly impact multiple ecologically important traits is critical for creating a robust picture of organismal fitness and the process of adaptation. However, this is complicated by both environmental heterogeneity and the complexity of genotype‐to‐phenotype relationships generated by pleiotropy and epistasis. Moreover, little is known about how pleiotropic and epistatic relationships themselves change over evolutionary time. The soil bacterium Myxococcus xanthus employs several distinct social traits across a range of environments. Here, we use an experimental lineage of M. xanthus that evolved a novel form of social motility to address how interactions between epistasis and pleiotropy evolve. Specifically, we test how mutations accumulated during selection on soft agar pleiotropically affect several other social traits (hard agar motility, predation and spore production). Relationships between changes in swarming rate in the selective environment and the four other traits varied greatly over time in both direction and magnitude, both across timescales of the entire evolutionary lineage and individual evolutionary time steps. We also tested how a previously defined epistatic interaction is pleiotropically expressed across these traits. We found that phenotypic effects of this epistatic interaction were highly correlated between soft and hard agar motility, but were uncorrelated between soft agar motility and predation, and inversely correlated between soft agar motility and spore production. Our results show that ‘epistatic pleiotropy’ varied greatly in magnitude, and often even in sign, across traits and over time, highlighting the necessity of simultaneously considering the interacting complexities of pleiotropy and epistasis when studying the process of adaptation.

Parallel emergence of negative epistasis across experimental lineages

Epistatic interactions can greatly impact evolutionary phenomena, particularly the process of adaptation. Here, we leverage four parallel experimentally evolved lineages to study the emergence and trajectories of epistatic interactions in the social bacterium Myxococcus xanthus. A social gene (pilA) necessary for effective group swarming on soft agar had been deleted from the common ancestor of these lineages. During selection for competitiveness at the leading edge of growing colonies, two lineages evolved qualitatively novel mechanisms for greatly increased swarming on soft agar, whereas the other two lineages evolved relatively small increases in swarming. By reintroducing pilA into different genetic backgrounds along the four lineages, we tested whether parallel lineages showed similar patterns of epistasis. In particular, we tested whether a pattern of negative epistasis between accumulating mutations and pilA previously found in the fastest lineage would be found only in the two evolved lineages with the fastest and most striking swarming phenotypes, or rather was due to common epistatic structure across all lineages arising from the generic fixation of adaptive mutations. Our analysis reveals the emergence of negative epistasis across all four independent lineages. Further, we present results showing that the observed negative epistasis is not due exclusively to evolving populations approaching a maximum phenotypic value that inherently limits positive effects of pilA reintroduction, but rather involves direct antagonistic interactions between accumulating mutations and the reintroduced social gene.

Rapid evolution slows extinctions in food webs

Historically, evolutionary changes have been thought to act on much longer time scales than ecological dynamics. However, a recent body of research has demonstrated that evolution that is rapid enough to dramatically affect ecological dynamics can lead to feedbacks between ecological and evolutionary processes. Thus, to understand the stability of ecological communities, we must also consider evolutionary change in the component species. Here, we use individual-based simulations of a quantitative genetic eco-evolutionary model to describe how trait evolution influences the stability of ecological communities. On short time scales, faster evolutionary rates decreased the probability of species extinctions as populations at low densities were rescued via trait evolution. However, on longer time scales, evolutionary had little effect on the number of extinctions. The extent of short-term evolutionary rescue depended on the source of trait variation; populations with variation generated through mutation experienced more rescue events and were less prone to extinction, relative to populations with only standing trait variation. Trait evolution leading to more rescued populations increased the stability of the community on timescales relevant to conservation. Our work highlights the importance of intraspecific trait variation and the evolutionary mechanisms maintaining this variation for community ecology, as well as management of declining populations in a community context.

Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism

Most plants engage in symbioses with mycorrhizal fungi in soils and net consequences for plants vary widely from mutualism to parasitism. However, we lack a synthetic understanding of the evolutionary and ecological forces driving such variation for this or any other nutritional symbiosis. We used meta-analysis across 646 combinations of plants and fungi to show that evolutionary history explains substantially more variation in plant responses to mycorrhizal fungi than the ecological factors included in this study, such as nutrient fertilization and additional microbes. Evolutionary history also has a different influence on outcomes of ectomycorrhizal versus arbuscular mycorrhizal symbioses; the former are best explained by the multiple evolutionary origins of ectomycorrhizal lifestyle in plants, while the latter are best explained by recent diversification in plants; both are also explained by evolution of specificity between plants and fungi. These results provide the foundation for a synthetic framework to predict the outcomes of nutritional mutualisms.Jason Hoeksema et al. report a meta-analysis of the drivers of outcomes in mycorrhizal mutualisms across 646 plant–fungi combinations. They find that evolutionary history explains substantially more variation in the strength of mycorrhizal mutualisms than do ecological factors.