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July 2011 - present
Publications
Publications (462)
Generalist predators often live in environments that vary in the type and abundance of prey species. The prey species in turn vary in their susceptibility and suitability to predation. How do generalists navigate this variation in prey abundance and profitability and seek out their preferred prey. We investigated this in the soil protist Dictyostel...
Predation is likely to influence the function of bacterial communities and the evolution of bacterial pathogens, because characteristics that permit escape from predators often overlap with traits used for biocontrol of plant pathogens, virulence, or even bioremediation. Soil bacteria are preyed upon by a variety of microorganisms, including the am...
Symbiotic interactions may change depending on third parties like predators or prey. Third-party interactions with prey bacteria are central to the symbiosis between Dictyostelium discoideum social amoeba hosts and Paraburkholderia bacterial symbionts. Symbiosis with inedible Paraburkholderia allows host D. discoideum to carry prey bacteria through...
The evolution of symbiotic interactions may be affected by unpredictable conditions. However, a link between prevalence of these conditions and symbiosis has not been widely demonstrated. We test for these associations using Dictyostelium discoideum social amoebae and their bacterial endosymbionts. D. discoideum commonly hosts endosymbiotic bacteri...
Selection for cooperation or conflict in multicellular organisms that develop from a mixture of cells has been widely appreciated, but unselected effects of mixing could also have important fitness consequences to the resulting chimeras. We formalized this idea as the developmental incompatibility hypothesis and empirically tested it in the social...
Cooperation is widespread across life, but its existence can be threatened by exploitation. The rise of obligate social cheaters that are incapable of contributing to a necessary cooperative function can lead to the loss of that function. In the social amoeba Dictyostelium discoideum , obligate social cheaters cannot form dead stalk cells and in ch...
Consumers range from specialists that feed on few resources to generalists that feed on many. Generalism has the clear advantage of having more resources to exploit, but the costs that limit generalism are less clear. We explore two understudied costs of generalism in a generalist amoeba predator, Dictyostelium discoideum , feeding on naturally co-...
Many microbes interact with one another, but the difficulty of directly observing these interactions in nature makes interpreting their adaptive value complicated. The social amoeba Dictyostelium discoideum forms aggregates wherein some cells are sacrificed for the benefit of others. Within chimaeric aggregates containing multiple unrelated lineage...
The soil amoeba Dictyostelium discoideum acts as both a predator and potential host for diverse bacteria. We tested fifteen Pseudomonas strains that were isolated from transiently infected wild D. discoideum for ability to escape predation and infect D. discoideum fruiting bodies. Three predation-resistant strains frequently caused extracellular in...
Aggregative multicellularity relies on cooperation among formerly independent cells to form a multicellular body. Previous work with Dictyostelium discoideum showed that experimental evolution under low relatedness profoundly decreased cooperation, as indicated by the loss of fruiting body formation in many clones and an increase of cheaters that c...
Microbes adapt to the presence of other species, but the fitness consequences of specific interactions are difficult to study in their natural context. We experimentally evolved symbiotic microbes in an artificial environment without access to the partners with whom they interact in nature. As organisms will tend to lose adaptations that they do no...
The soil amoeba Dictyostelium discoideum acts as both a predator and potential host for diverse bacteria. We tested fifteen Pseudomonas strains that were isolated from transiently infected wild D. discoideum for ability to escape predation and infect D. discoideum fruiting bodies. Three predation-resistant strains frequently caused extracellular in...
Many microbes interact with one another, but the difficulty of directly observing these interactions in nature makes interpreting their adaptive value complicated. The social amoeba Dictyostelium discoideum forms aggregates wherein some cells are sacrificed for the benefit of others. Within chimeric aggregates containing multiple unrelated lineages...
Cooperation is widespread across life, but its existence can be threatened by exploitation. The rise of obligate social cheaters that are incapable of contributing to a necessary cooperative function can lead to the loss of that function and to the extinction of populations. In the social amoeba Dictyostelium discoideum , obligate social cheaters c...
Some endosymbionts living within a host must modulate their hosts' immune systems in order to infect and persist. We studied the effect of a bacterial endosymbiont on a facultatively multicellular social amoeba host. Aggregates of the amoeba Dictyostelium discoideum contain a subpopulation of sentinel cells that function akin to the immune systems...
Organisms can be classified as diet specialists or generalists based on the number of prey types they eat. Since different prey species have different constitutions and defenses, eating a wide variety of prey presents challenges. We explore three potential costs of generalism in a super-generalist amoeba predator, Dictyostelium discoideum , feeding...
The social amoeba Dictyostelium discoideum engages in a complex relationship with bacterial endosymbionts in the genus Paraburkholderia, which can benefit their host by imbuing it with the ability to carry prey bacteria throughout its life cycle. The relationship between D. discoideum and Paraburkholderia has been shown to take place across many st...
The evolution of symbiotic interactions may be affected by unpredictable conditions. However, a link between prevalence of symbiosis and these conditions has not been widely demonstrated. We test for these associations using Dictyostelium discoideum social amoebae and their bacterial symbionts. D. discoideum are host to endosymbiotic bacteria from...
Some endosymbionts living within a host must modulate their hosts' immune systems in order to infect and persist. We studied the effect of a bacterial endosymbiont on a facultatively multicellular social amoeba host. Aggregates of the amoeba Dictyostelium discoideum contain a subpopulation of sentinel cells that function akin to the immune systems...
Bacterial endosymbionts can provide benefits for their eukaryotic hosts, but it is often unclear if endosymbionts benefit from these relationships. The social amoeba Dictyostelium discoideum associates with three species of Paraburkholderia endosymbionts, including P. agricolaris and P. hayleyella. These endosymbionts can be costly to host but are...
Cooperation is widespread across life, but its existence can be threatened by exploitation. Social cheaters can be obligate, incapable of contributing to a necessary function, so that spread of the cheater leads to loss of the function. In the social amoeba Dictyostelium discoideum , obligate social cheaters cannot become dead stalk cells that lift...
Symbiotic interactions change depending on the abundance of third parties like predators, prey, or pathogens. Third-party interactions with food bacteria are central to the symbiosis between Dictyostelium discoideum social amoeba hosts and inedible Paraburkholderia bacterial symbionts. Symbiosis with Paraburkholderia allows host D. discoideum to ca...
Aggregative multicellularity relies on cooperation among individual cells to form a multicellular body. In Dictyostelium discoideum this cooperation is maintained by high relatedness. Previous work showed that experimental evolution under low-relatedness resulted in an increase of cheaters (cells that contribute proportionally more to viable spores...
Protists are a diverse group of typically single cell eukaryotes. Bacteria and archaea that form long-term symbiotic relationships with protists may evolve in additional ways than those in relationships with multicellular eukaryotes such as plants, animals, or fungi.
Encouraging students to engage in self-driven problem solving early in their educational career is necessary for them to be able to conduct hypothesis-driven research in the future. However, a fundamental obstacle is finding a topic and activity that is both tangible for students to understand and intelligible. Here we present a classroom activity...
The social amoeba Dictyostelium discoideum is a predatory soil protist frequently used for studying host-pathogen interactions. A subset of D. discoideum strains isolated from soil persistently carry symbiotic Paraburkholderia, recently formally described as P. agricolaris, P. bonniea, and P. hayleyella. The three facultative symbiont species of D....
Aggregative multicellularity occurs when dispersed cells join together to form a highly cooperative unit, in contrast to clonal multicellular organisms formed by cells that remain in contact after descent from a single cell. Because aggregative groups may include non-relatives, aggregative multicellular organisms should be particularly vulnerable t...
Abstract Symbiotic interactions change with environmental context. Measuring these context‐dependent effects in hosts and symbionts is critical to determining the nature of symbiotic interactions. We investigated context dependence in the symbiosis between social amoeba hosts and their inedible Paraburkholderia bacterial symbionts, where the contex...
Kin selection is a core aspect of social evolution theory, but a small number of critics have recently challenged it. Here I address these criticisms and show that kin selection remains an important explanation for much (though not all) social evolution. I show how many of the criticisms rest on historical idiosyncrasies of the way the field happen...
Symbiotic interactions change with environmental context. Measuring these context-dependent effects in hosts and symbionts is critical to determining the nature of symbiotic interactions. We investigated context-dependence in the symbiosis between social amoeba hosts and their inedible Paraburkholderia bacterial symbionts, where the context is the...
Amoebae interact with bacteria in multifaceted ways. Amoeba predation can serve as a selective pressure for the development of bacterial virulence traits. Bacteria may also adapt to life inside amoebae, resulting in symbiotic relationships. Indeed, particular lineages of obligate bacterial endosymbionts have been found in different amoebae. Here, w...
Aggregative multicellularity occurs when dispersed cells join together to form a highly cooperative unit, in contrast to clonal multicellular organisms formed by cells that remain in contact after descent from a single cell. Because aggregative groups may include non-relatives, aggregative multicellular organisms should be particularly vulnerable t...
Microbes must adapt to the presence of other species, but it can be difficult to recreate the natural context for these interactions in the laboratory. We describe a method for inferring the existence of symbiotic adaptations by experimentally evolving microbes that would normally interact in an artificial environment without access to other specie...
Amoebae are protists that have complicated relationships with bacteria, which cover the whole spectrum of symbiosis. Amoeba-bacteria interactions contribute to the study of predation, symbiosis, pathogenesis, and human health. Given the complexity of their relationships, it is necessary to understand the ecology and evolution of their interactions....
Anthropogenic global change is increasingly raising concerns about collapses of symbiotic interactions worldwide. Therefore, understanding how climate change affects symbioses remains a challenge and demands more study. Here, we look at how simulated warming affects the social ameba Dictyostelium discoideum and its relationship with its facultative...
Amoebae interact with bacteria in diverse and multifaceted ways. Amoeba predation can serve as a selective pressure for the development of bacterial virulence traits. Bacteria may also adapt to life inside amoebae, resulting in symbiotic relationships (pathogenic or mutualistic). Indeed, amoebae are often infected with bacterial endosymbionts. Acan...
We describe the rate and spectrum of spontaneous mutations for the social amoeba Dictyostelium discoideum , a key model organism in molecular, cellular, evolutionary, and developmental biology. Whole-genome sequencing of 37 mutation accumulation lines of D. discoideum after an average of 1,500 cell divisions yields a base-substitution mutation rate...
Here we give names to three new species of Paraburkholderia that can remain in symbiosis indefinitely in the spores of a soil dwelling eukaryote, Dictyostelium discoideum . The new species P. agricolaris sp. nov. , P. hayleyella sp. nov. , and P. bonniea sp. nov . are widespread across the eastern USA and were isolated as internal symbionts of wild...
The biological units-of-selection debate has centred on questions of which units experience selection and adaptation. Here, I use a causal framework and the Price equation to develop the gene's eye perspective. Genes are causally special in being both replicators and interactors. Gene effects are tied together in a complex Gouldian knot of interact...
Abstract When multiple strains of microbes form social groups, such as the multicellular fruiting bodies of Dictyostelium discoideum, conflict can arise regarding cell fate. Both fixed and plastic differences among strains can contribute to cell fate, and plastic responses may be particularly important if social environments frequently change. We u...
Evolutionary conflict and arms races are important drivers of evolution in nature. During arms races, new abilities in one party select for counterabilities in the second party. This process can repeat and lead to successive fixations of novel mutations, without a long‐term increase in fitness. Models of co‐evolution rarely address successive fixat...
Hosts and their associated microbes can enter into different relationships, which can range from mutualism, where both partners benefit, to exploitation, where one partner benefits at the expense of the other. Many host-microbe relationships have been presumed to be mutualistic, but frequently only benefits to the host, and not the microbial symbio...
Some forms of stable cooperation can evolve though pleiotropy with a beneficial private trait. This Formal Comment addresses a recent challenge to this idea, arguing that for synergistic, frequency-dependent cooperation, pleiotropy can raise the frequency up to a point where cooperation is favoured on its own.
Evolutionary conflict can drive rapid adaptive evolution, sometimes called an arms race, because each party needs to respond continually to the adaptations of the other. Evidence for such arms races can sometimes be seen in morphology, in behavior, or in the genes underlying sexual interactions of host−pathogen interactions, but is rarely predicted...
The social amoeba Dictyostelium discoideum has provided considerable insight into the evolution of cooperation and conflict. Under starvation, D. discoideum amoebas cooperate to form a fruiting body comprised of hardy spores atop a stalk. The stalk development is altruistic because stalk cells die to aid spore dispersal. The high relatedness of cel...
Recent symbioses, particularly facultative ones, are well suited for unravelling the evolutionary give and take between partners. Here we look at variation in natural isolates of the social amoeba Dictyostelium discoideum and their relationships with bacterial symbionts, Burkholderia hayleyella and Burkholderia agricolaris. Only about a third of fi...
The establishment of symbioses between eukaryotic hosts and bacterial symbionts in nature is a dynamic process. The formation of such relationships depends on the life history of both partners. Bacterial symbionts of amoebae may have unique evolutionary trajectories to the symbiont lifestyle, because bacteria are typically ingested as prey. To pers...
A small subset of bacteria in soil interact directly with eukaryotes. Which ones do so can reveal what is important to a eukaryote and how eukaryote defenses might be breached. Soil amoebae are simple eukaryotic organisms and as such could be particularly good for understanding how eukaryote microbiomes originate and are maintained. One such amoeba...
Evolutionary conflict occurs when two parties can each affect a joint phenotype, but they gain from pushing it in opposite directions. Conflicts occur across many biological levels and domains but share many features. They are a major source of biological maladaptation. They affect biological diversity, often increasing it, at almost every level. B...
Recent symbioses, particularly facultative ones, are well suited for unravelling the evolutionary give and take between partners. Here we look at variation in wild-collected samples of the social amoeba Dictyostelium discoideum and their relationships with bacterial symbionts, Burkholderia hayleyella and Burkholderia agricolaris. Only about a third...
A key question in cooperation is how to find the right partners and maintain cooperative relationships. This is especially challenging for horizontally transferred bacterial symbionts where relationships must be repeatedly established anew. In the social amoeba Dictyostelium discoideum farming symbiosis, two species of inedible Burkholderia bacteri...
Interactions between species and their environment play a key role in the evolution of diverse communities, and numerous studies have emphasized that interactions among microbes and among trophic levels play an important role in maintaining microbial diversity and ecosystem functioning. In this study, we investigate how two of these types of intera...
Here we name three species of Burkholderia that can defeat the mechanisms by which bacteria are normally excluded from the spores of a soil dwelling eukaryote Dictyostelium discoideum , which is predatory on bacteria. They are B. agricolaris sp. nov., B. hayleyella sp. nov., and B. bonniea sp. nov. These new species are widespread across the easter...
Significance
Bacterially produced small molecules are indispensable leads in the development of antibiotics, anticancer therapeutics, or immunomodulators. To unveil novel aspects in the biosynthetic potential of bacteria, a consideration of the ecological context in which the adapted producers thrive is extremely insightful. Here, we describe two n...
Significance
Microbes are surprisingly social organisms and are providing model systems for the study of the evolution of cooperation and conflict. Despite their many advantages in the laboratory, such as experimental evolution, it is rarely possible to study them in the field. We therefore know little about whether cooperation and conflict are ada...
In our paper (Douglas et al. 2017), we tested the hypothesis that mating types differentially contribute to macrocyst production in Dictyostelium discoideum. Macrocysts are the result of the sexual union and subsequent meiosis of any two of the three mating types of D. discoideum. In the macrocyst process, many amoebae of the two mating types come...
Traditional morphology-based taxonomy of dictyostelids is rejected by molecular phylogeny. A new classification is presented based on monophyletic entities with consistent and strong molecular phylogenetic support and that are, as far as possible, morphologically recognizable. All newly named clades are diagnosed with small subunit ribosomal RNA (1...
The evolution of multicellularity is one of the key transitions in evolution and requires extreme levels of cooperation between cells. However, even when cells are genetically identical, non-cooperative cheating mutants can arise that cause a breakdown in cooperation. How then, do multicellular organisms maintain cooperation between cells? A number...
Evolutionary biology is undergirded by an extensive and impressive set of mathematical models. Yet only one result, Fisher’s theorem about selection and fitness, is generally accorded the status of a fundamental theorem. I argue that although its fundamental status is justified by its simplicity and scope, there are additional results that seem sim...
Unequal investment by different sexes in their progeny is common and includes differential investment in the zygote and differential care of the young. The social amoeba Dictyostelium discoideum has a sexual stage in which isogamous cells of any two of the three mating types fuse to form a zygote which then attracts hundreds of other cells to the m...
Background. Interactions between eukaryotic amoebae and bacteria are understudied and important. Bacteria inside of amoebae are protected from external forces including antibiotics. An excellent model for bacteria-amoeba interactions is the social amoeba Dictyostelium discoideum and its associated bacteria. A third of wild-collected clones of the s...
Background. Interactions between eukaryotic amoebae and bacteria are understudied and important. Bacteria inside of amoebae are protected from external forces including antibiotics. An excellent model for bacteria-amoeba interactions is the social amoeba Dictyostelium discoideum and its associated bacteria. A third of wild-collected clones of the s...
Kin selection is a core aspect of social evolution theory, but a small number of critics have recently challenged it. Here I address these criticisms and show that kin selection remains an important explanation for much (though not all) social evolution. I show how many of the criticisms rest on historical idiosyncrasies of the way the field happen...
Kin selection is a core aspect of social evolution theory, but a small number of critics have recently challenged it. Here I address these criticisms and show that kin selection remains an important explanation for much (though not all) social evolution. I show how many of the criticisms rest on historical idiosyncrasies of the way the field happen...
The organism is one of the fundamental concepts of biology and has been at the center of many discussions about biological individuality, yet what exactly it is can be confusing. The definition that we find generally useful is that an organism is a unit in which all the subunits have evolved to be highly cooperative, with very little conflict. We f...
The social amoeba Dictyostelium discoideum is unusual among eukaryotes in having both unicellular and multicellular stages. In the multicellular stage, some cells, called sentinels, ingest toxins, waste and bacteria. The sentinel cells ultimately fall away from the back of the migrating slug, thus removing these substances from the slug. However, s...
Theory indicates that numbers of mating types should tend towards infinity or remain at two. The social amoeba, Dictyostelium discoideum, however, has three mating types. It is therefore a mystery how this species has broken the threshold of two mating types, but has not increased towards a much higher number. Frequency dependent selection on rare...
The bacterial partners in symbiotic relationships with eukaryotes can have a powerful effect on the phenotypic traits of the host. Here we explore this issue using a simple model eukaryote, Dictyostelium discoideum, and its facultative bacterial symbionts. Some clones of the social amoeba D. discoideum, called farmers, maintain symbiotic relationsh...
Cooperation among microbes is important for traits as diverse as antibiotic resistance, pathogen virulence, and sporulation. The evolutionary stability of cooperation against “cheater” mutants depends critically on the extent to which microbes interact with genetically similar individuals. The causes of this genetic social structure in natural micr...
Significance
Strong support for the theory of kin selection can come from predicting outcomes under circumstances of within-family conflict. Genes inherited from mothers (matrigenes) and fathers (patrigenes) usually work harmoniously in the offspring. However, kin selection theory predicts these genes may be in conflict over interactions among rela...
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...
Significance
Symbionts can provide hosts with many advantages including defensive capabilities and novel nutrients. However, symbionts may begin as pathogens that only subsequently become beneficial. In the Dictyostelium discoideum farming symbiosis some amoebas stably associate with bacterial partners. We demonstrate that amoeba-associated Burkhol...