Microbial Social Behavior

Microbial systems offer a rich and powerful way to understand the evolution of social behaviors. These social behaviors allow microbes to exert dramatic effects on their environment, often constructing a niche that is favorable to them. Selfish and mutually beneficially behaviors can be understood through an individual fitness benefit, while altruism and spite have provided an evolutionary puzzle. Our lab is working to solve that puzzle. Spite has long been considered a theoretical possibility, but not a social behavior of any consequence in nature. After all, how can a behavior that is harmful to both the actor and the recipient persist? The answer lies in who is the recipient of the spiteful act and who might indirectly benefit. In other words, spite might more easily be understood as “indirect altruism,” whereby the actor’s kin benefit by the harm directed to unrelated individuals.

Antagonistic interactions among bacteria mediated via bacteriocins have been proposed as the premier example of spite in nature. Bacteriocins are bacteriocidal toxins, noted for their narrow killing spectrum. Bacteriocin production is costly, and often, the producer cell lyses to release the toxin. As a dead producer can receive no direct benefit from its action, bacteriocin production fits the definition of spite. Moreover, individuals closely related to the producer cell are often immune to the bacteriocin’s effect and thus may benefit by the destruction of competitors.

Xenorhabdus bacteria can inhibit each other’s growth by via the bacteriocin, xenorhabdicin. Xenorhabdicin is phage derived and similar to the R-type pyocins of Pseudomonas. Our work on natural isolates of Xenorhabdus was the first to show that intraspecific bacteriocin-based antagonisms can occur over a spatially relevant scale and thus support the existence of spite in nature. Moreover, by examining the genetic relatedness and spatial distance between interacting isolates, our studies support recent theoretical predictions suggesting that population structure is key to the evolution of spite and that spite benefits kin and can lower virulence. We are currently examining the genetic architecture underlying the phenotypic diversity in bacteriocin-based interactions of our natural isolates. We are also examining the regulation of bacteriocin production.

Research

We study insect-parasitic nematodes and their mutualist bacterial partners to address a variety of conceptual areas.

Evolution of Parasite Virulence and Life History

Parasite virulence has been modeled as a life-history problem, where parasites trade-off increased reproduction with lowered transmission success. When multiple parasites infect a host, the behavior of one parasite can influence the success of other co-infecting parasites. Thus, co-infections are predicted to have a profound impact on the evolution virulence. We were able to provide one of the first experimental tests of this theory, using the insect-parasitic nematode, Steinernema carpocapsae. We took an experimental evolution approach, manipulating migration to influence the relatedness of parasites co-infecting an insect host.

We found that restricted migration led to faster host exploitation and more rapid host death. We hypothesized that interference competition (such as bacteriocin-mediated antagonism) among unrelated parasites can reduce their ability to use host resources, and thus lessen the detrimental effect that they had on their hosts. That is, unrelated parasites fight each other (at the expense of their ability to exploit their host), while related parasites “cooperate” by not fighting.

We tested this hypothesis by isolating the Xenorhabdus bacteria from insects that had been killed by parasites from our low- and high-migration lines. We found inhibitions within hosts infected with parasites from the high-migration treatment, but none within hosts in the low-migration treatment. Our study was the first to document intraspecific antagonism in X. nematophila. Furthermore, it was the first empirical demonstration that parasite migration can affect within-host interference competition and virulence.

In addition to our work focusing on within-host competition, we have also examined the potential for among-host selection in the nematode S. carpocapsae. Selection among hosts is thought to be an important force shaping the evolution of parasite life histories; nevertheless, few studies have empirically examined among-host selection. We selected among insect hosts by propagating nematodes based on the total number of nematodes emerging from an insect. We found a direct response to this group-level selection as a forty percent difference in population size evolved between the low- and high-selected treatments. Moreover, selection on population size in our experiment affected the timing of nematode emergence and the size of emerging nematodes. The size of emerging nematodes is likely to influence their fitness, as they are non-feeding until they find a new host. Furthermore, we have found that large nematodes have a higher infection success than small nematodes and that aging in the transmission stage can alter species interactions. These results suggest that it is critical to examine both within and among-host selection in order to understand infection dynamics and the evolution of parasite life histories.

Beneficial Symbionts and the Evolution of Mutualisms

Organismal traits are often the product of interactions between the organism and its microbial symbionts. Symbionts can provide their host access to vital nutrients, increase abiotic tolerances of their host, and provide defense against pathogens and predators. Xenorhabdus symbionts of Steinernema nematodes produce many compounds which help in killing and digesting the insect host and are key for successful reproduction of the nematode. Xenorhabdus bacteria also produce a suite of secondary metabolites and defensive compounds that protect the insect cadaver from fungal and bacterial saprophytes.

In addition to the broad-spectrum defenses, the bacteriocins produced by Xenorhabdus can help their nematode partners gain a competitive advantage over co-infecting nematodes. Despite this benefit, several natural isolates of Xenorhabdus are not able to inhibit any sympatric isolates. Does this represent recent evolution of resistance? Or, could these isolates be following a different path to success? Evidence suggests that these isolates may be better at parasitizing the insect host, leading to a higher probability of successful emergence by the nematode and bacterial partners.

Maintenance of Diversity

General theoretical models predict that diversity can be maintained in the absence of environmental heterogeneity if all genotypes have equal fitness, or if each genotype has an advantage when rare.

Our work on natural isolates of Steinernema nematodes and their Xenorhabdus bacteria has shown that interactions among these clones may be nonhierarchical or non-transitive, meaning that no one clone is superior to all others. When interactions are non-transitive, such as in the rock-paper-scissors game, each player can be invaded by another strategy, thus allowing all three strategies to coexist. Non-transitive interactions are thought to be common in nature, but few studies have demonstrated their role in maintaining diversity, especially in relation to parasites. In our system, we have the ability to pair a highly tractable experimental system with observations in nature to test some of the key assumptions and predictions of this theory. We have begun by examining pairwise competitions among our natural isolates in the caterpillar host.

These studies demonstrate the importance of bacteriocin-based antagonisms in determining competitive outcomes and in altering infection dynamics. In addition, these studies also reinforce the importance of exploitative competition in within-host interactions. Specifically, we see that faster killing parasites are competitively dominant in the absence of bacteriocin-based interactions. These results suggest there may be multiple strategies for success in this community.


Untangling Nature

Darwin famously ends On the Origin of Species with a description of the diversity of plants and animals found in an “entangled bank” and he contemplates how these “endless forms most beautiful” have arisen from the simple process of evolution by natural selection. In our lab, we seek to untangle the interactions among different species and genotypes in order to better understand how selection shapes the expression and maintenance of the diversity of phenotypes we see in nature.

Maintenance of Diversity
Microbial Social Behavior
Parasite Virulence
Beneficial Symbionts