Benjamin Kerr | University of Washington (original) (raw)
Papers by Benjamin Kerr
Molecular Biology and Evolution
Genes that undergo horizontal gene transfer (HGT) evolve in different genomic backgrounds. Despit... more Genes that undergo horizontal gene transfer (HGT) evolve in different genomic backgrounds. Despite the ubiquity of cross-species HGT, the effects of switching hosts on gene evolution remains understudied. Here, we present a framework to examine the evolutionary consequences of host switching and apply this framework to an antibiotic resistance gene commonly found on conjugative plasmids. Specifically, we determined the adaptive landscape of this gene for a small set of mutationally connected genotypes in three enteric species. We uncovered that the landscape topographies were largely aligned with minimal host-dependent mutational effects. By simulating gene evolution over the experimentally gauged landscapes, we found that the adaptive evolution of the mobile gene in one species translated to adaptation in another. By simulating gene evolution over artificial landscapes, we found that sufficient alignment between landscapes ensures such “adaptive equivalency” across species. Thus, g...
PLOS Computational Biology, Dec 14, 2016
Epistatic interactions among genes can give rise to rugged fitness landscapes, in which multiple ... more Epistatic interactions among genes can give rise to rugged fitness landscapes, in which multiple "peaks" of high-fitness allele combinations are separated by "valleys" of low-fitness genotypes. How populations traverse rugged fitness landscapes is a long-standing question in evolutionary biology. Sexual reproduction may affect how a population moves within a rugged fitness landscape. Sex may generate new high-fitness genotypes by recombination, but it may also destroy high-fitness genotypes by shuffling the genes of a fit parent with a genetically distinct mate, creating low-fitness offspring. Either of these opposing aspects of sex require genotypic diversity in the population. Spatially structured populations may harbor more diversity than well-mixed populations, potentially amplifying both positive and negative effects of sex. On the other hand, spatial structure leads to clumping in which mating is more likely to occur between like types, diminishing the effects of recombination. In this study, we use computer simulations to investigate the combined effects of recombination and spatial structure on adaptation in rugged fitness landscapes. We find that spatially restricted mating and offspring dispersal may allow multiple genotypes inhabiting suboptimal peaks to coexist, and recombination at the "sutures" between the clusters of these genotypes can create genetically novel offspring. Sometimes such an offspring genotype inhabits a new peak on the fitness landscape. In such a case, spatially restricted mating allows this fledgling subpopulation to avoid recombination with distinct genotypes, as mates are more likely to be the same genotype. Such population "centers" can allow nascent peaks to establish despite recombination. Spatial structure may therefore allow an evolving population to enjoy the creative side of sexual recombination while avoiding its destructive side.
The British Journal for the Philosophy of Science, Mar 1, 2013
Formal methods developed for modeling levels of selection problems have recently been applied to ... more Formal methods developed for modeling levels of selection problems have recently been applied to the investigation of major evolutionary transitions. We discuss two new tools of this kind. First, the 'near-variant test' can be used to compare the causal adequacy of predictively equivalent representations. Second, 'state-variable gestalt-switching' can be used to gain a useful dual perspective on evolutionary processes that involve both higher and lower level populations.
Evolution, Dec 21, 2015
Model, Data, and Analysis Scripts for The Evolution of Cooperation by the Hankshaw Effect as subm... more Model, Data, and Analysis Scripts for The Evolution of Cooperation by the Hankshaw Effect as submitted
Black Queen Gene Loss in a Structured Environment The Black Queen Hypothesis (Morris et al. 2012)... more Black Queen Gene Loss in a Structured Environment The Black Queen Hypothesis (Morris et al. 2012): 1) All biological func/ons have a cost. If all things are equal, excluding a func/on causes a fitness advantage 2) Products of 'leaky' biological func/ons are unavoidably made available to the community, thus providing "public goods". Examples of leaky func/ons: 1) Detoxifica/on of an environment 2) Cross-feeding 3) 'Cheaters' are organisms that have lost a vital leaky func/on, but s/ll acquire the result of the func/on through the environment by comple/on of this func/on by 'helper' organisms 4) The fitness of cheaters and helpers is negaFvely frequency dependent, which means each has an advantage when rare. Therefore, they can coexist, preven/ng the loss of the Black Queen func/on in a "Tragedy of the Commons"
This repository contains the model, data, and analysis corresponding to <em>Negative Niche ... more This repository contains the model, data, and analysis corresponding to <em>Negative Niche Construction Favors the Evolution of Cooperation</em> by Brian D. Connelly, Katherine J. Dickinson, Sarah P. Hammarlund, and Benjamin Kerr after addressing feedback from two anonymous reviewers.
The American Naturalist, Jul 1, 2018
Organisms often modify their environments to their advantage through a process of niche construct... more Organisms often modify their environments to their advantage through a process of niche construction. Environments that are improved through positive niche construction can be viewed as a public good. If free riders appear that do not contribute to the shared resource and therefore do not incur any associated costs, the constructed niche may become degraded, resulting in a tragedy of the commons and the extinction of niche constructors. Niche construction can persist if free riders are excluded, for example, if niche constructors monopolize the resource they produce to a sufficient degree. We suggest, however, that the problem of free riders remains because it is possible that nonniche constructors with an enhanced ability to access the resource appear and invade a population of constructors. Using mathematical models we show that positive niche construction can be maintained if it is inextricably linked to a mechanism that makes free riding costly, such as a trait that confers a benefit to only niche constructors. We discuss this finding in terms of genetic interactions and illustrate the principle with a two-locus model. We conclude that positive niche construction can both evolve and be maintained when it has other beneficial effects via pleiotropy. This situation may apply generally to the evolutionary maintenance of cooperation.
Frontiers in Microbiology, Jul 28, 2015
Many bacteria secrete compounds which act as public goods. Such compounds are often under quorum ... more Many bacteria secrete compounds which act as public goods. Such compounds are often under quorum sensing (QS) regulation, yet it is not understood exactly when bacteria may gain from having a public good under QS regulation. Here, we show that the optimal public good production rate per cell as a function of population size (the optimal production curve, OPC) depends crucially on the cost and benefit functions of the public good and that the OPC will fall into one of two categories: Either it is continuous or it jumps from zero discontinuously at a critical population size. If, e.g., the public good has accelerating returns and linear cost, then the OPC is discontinuous and the best strategy thus to ramp up production sharply at a precise population size. By using the example of public goods with accelerating and diminishing returns (and linear cost) we are able to determine how the two different categories of OPSs can best be matched by production regulated through a QS signal feeding back on its own production. We find that the optimal QS parameters are different for the two categories and specifically that public goods which provide accelerating returns, call for stronger positive signal feedback.
Evolutionary Ecology Research, Nov 1, 1999
Using a two-locus diallelic population genetic model, we studied the evolution and impact of flam... more Using a two-locus diallelic population genetic model, we studied the evolution and impact of flammable traits in resprouting plants. A 'flammability locus' determines the flammable character of a plant and the frequency of alleles at this locus affects the probability that any plant in the population will burn. A linked 'disturbance locus' determines how a plant fares in the presence or absence of fire. Thus, the frequencies of alleles at the flammability locus influence evolution at the disturbance locus. The evolution of flammability-enhancing alleles is influenced by asymmetries in the genotypic fitnesses as well as by the base flammability of the population and the genetic structure of the system (with tighter linkage increasing the possibility that the population becomes more flammable). We demonstrate that stable polymorphisms of plants differing in flammability alleles are possible. The magnitude of the organism's impact on the flammable character of the environment influences where such polymorphisms are expected. Furthermore, predictions concerning the evolution of alleles at the disturbance locus based solely on fitness asymmetries may fail due to the influence of plants on their environment. Unusual population dynamics, including stable and unstable cycles of genotypes, are also presented. The relation of this model to the Mutch hypothesis and the recently developed theories of 'niche construction' and 'ecosystem engineering' is discussed.
Journal of Theoretical Biology, Sep 1, 2015
Cambridge University Press eBooks, May 1, 2008
Molecular Ecology, Dec 1, 2015
Populations of organisms routinely face abiotic selection pressures, and a central goal of evolut... more Populations of organisms routinely face abiotic selection pressures, and a central goal of evolutionary biology is to understand the mechanistic underpinnings of adaptive phenotypes. Ultraviolet radiation (UVR) is one of earth's most pervasive environmental stressors, potentially damaging DNA in any organism exposed to solar radiation. We explored mechanisms underlying differential survival following UVR exposure in genotypes of the water flea Daphnia melanica derived from natural ponds of differing UVR intensity. The UVR tolerance of a D. melanica genotype from a high-UVR habitat depended on the presence of visible and UV-A light wavelengths necessary for photoenzymatic repair of DNA damage, a repair pathway widely shared across the tree of life. We then measured the acquisition and repair of cyclobutane pyrimidine dimers, the primary form of UVR-caused DNA damage, in D. melanica DNA following experimental UVR exposure. We demonstrate that genotypes from high-UVR habitats repair DNA damage faster than genotypes from low-UVR habitats in the presence of visible and UV-A radiation necessary for photoenzymatic repair, but not in dark treatments. Because differences in repair rate only occurred in the presence of visible and UV-A radiation, we conclude that differing rates of DNA repair, and therefore differential UVR tolerance, are a consequence of variation in photoenzymatic repair efficiency. We then rule out a simple gene expression hypothesis for the molecular basis of differing repair efficiency, as expression of the CPD photolyase gene photorepair did not differ among D. melanica lineages, in both the presence and absence of UVR.
Current Opinion in Microbiology, Oct 1, 2014
In this review, we demonstrate how game theory can be a useful first step in modeling and underst... more In this review, we demonstrate how game theory can be a useful first step in modeling and understanding interactions among bacteria that produce and resist antibiotics. We introduce the basic features of evolutionary game theory and explore model microbial systems that correspond to some classical games. Each game discussed defines a different category of social interaction with different resulting population dynamics (exclusion, coexistence, bistability, cycling). We then explore how the framework can be extended to incorporate some of the complexity of natural microbial communities. Overall, the game theoretical perspective helps to guide our expectations about the evolution of some forms of antibiotic resistance and production because it makes clear the precise nature of social interaction in this context.
Environmental Microbiology, Oct 14, 2015
Microbes perform many costly biological functions that benefit themselves, and may also benefit n... more Microbes perform many costly biological functions that benefit themselves, and may also benefit neighbouring cells. Losing the ability to perform such functions can be advantageous due to cost savings, but when they are essential for growth, organisms become dependent on ecological partners to compensate for those losses. When multiple functions may be lost, the ecological outcomes are potentially diverse, including independent organisms only; oneway dependency, where one partner performs all functions and others none; or mutual interdependency where partners perform complementary essential functions. What drives these different outcomes? We develop a model where organisms perform 'leaky' functions that provide both private and public benefits to explore the consequences of privatization level, costs and essentiality on influencing these outcomes. We show that mutual interdependency is favoured at intermediate levels of privatization for a broad range of conditions. One-way dependency, in contrast, is only favoured when privatization is low and loss-of-function benefits are accelerating. Our results suggest an interplay between privatization level and shape of benefits from loss in driving microbial dependencies. Given the ubiquity of microbial functions that are inevitably leaked and the ease of mutational inactivation, our findings may help to explain why microbial interdependencies are common in nature.
American Journal of Human Biology, 2004
Skip to Main Content. ...
Bulletin of the American Physical Society, Mar 14, 2016
Sewall Wright introduced the metaphor of the adaptive landscape, a map from genotype to fitness, ... more Sewall Wright introduced the metaphor of the adaptive landscape, a map from genotype to fitness, more than 80 years ago to help describe his view of adaptive evolution. This metaphor has been immensely popular and has been used in a variety of incarnations. However, a systematic study of the genotype-fitness map presents significant problems. The space of possible genotypes is vast, and the mapping is likely dependent on both environment and the composition of genotypes in a population. In this talk, I will discuss some of these problems and present experimental strategies for uncovering features of adaptive landscapes. In particular, I will discuss how population structure can be used as an experimental variable to elucidate landscape topography and how a combination of experimental evolution and genetic engineering can reveal important landscape features in changing environments. I will also present some potential applications of this work to the problem of antibiotic resistance and potential implications for evolutionary rescue in the face of global climate change. For some of these topics, the classic notion of the adaptive landscape must itself be adapted; however, I propose that there are fruitful ways to continue to apply this metaphor.
Molecular Biology and Evolution
Genes that undergo horizontal gene transfer (HGT) evolve in different genomic backgrounds. Despit... more Genes that undergo horizontal gene transfer (HGT) evolve in different genomic backgrounds. Despite the ubiquity of cross-species HGT, the effects of switching hosts on gene evolution remains understudied. Here, we present a framework to examine the evolutionary consequences of host switching and apply this framework to an antibiotic resistance gene commonly found on conjugative plasmids. Specifically, we determined the adaptive landscape of this gene for a small set of mutationally connected genotypes in three enteric species. We uncovered that the landscape topographies were largely aligned with minimal host-dependent mutational effects. By simulating gene evolution over the experimentally gauged landscapes, we found that the adaptive evolution of the mobile gene in one species translated to adaptation in another. By simulating gene evolution over artificial landscapes, we found that sufficient alignment between landscapes ensures such “adaptive equivalency” across species. Thus, g...
PLOS Computational Biology, Dec 14, 2016
Epistatic interactions among genes can give rise to rugged fitness landscapes, in which multiple ... more Epistatic interactions among genes can give rise to rugged fitness landscapes, in which multiple "peaks" of high-fitness allele combinations are separated by "valleys" of low-fitness genotypes. How populations traverse rugged fitness landscapes is a long-standing question in evolutionary biology. Sexual reproduction may affect how a population moves within a rugged fitness landscape. Sex may generate new high-fitness genotypes by recombination, but it may also destroy high-fitness genotypes by shuffling the genes of a fit parent with a genetically distinct mate, creating low-fitness offspring. Either of these opposing aspects of sex require genotypic diversity in the population. Spatially structured populations may harbor more diversity than well-mixed populations, potentially amplifying both positive and negative effects of sex. On the other hand, spatial structure leads to clumping in which mating is more likely to occur between like types, diminishing the effects of recombination. In this study, we use computer simulations to investigate the combined effects of recombination and spatial structure on adaptation in rugged fitness landscapes. We find that spatially restricted mating and offspring dispersal may allow multiple genotypes inhabiting suboptimal peaks to coexist, and recombination at the "sutures" between the clusters of these genotypes can create genetically novel offspring. Sometimes such an offspring genotype inhabits a new peak on the fitness landscape. In such a case, spatially restricted mating allows this fledgling subpopulation to avoid recombination with distinct genotypes, as mates are more likely to be the same genotype. Such population "centers" can allow nascent peaks to establish despite recombination. Spatial structure may therefore allow an evolving population to enjoy the creative side of sexual recombination while avoiding its destructive side.
The British Journal for the Philosophy of Science, Mar 1, 2013
Formal methods developed for modeling levels of selection problems have recently been applied to ... more Formal methods developed for modeling levels of selection problems have recently been applied to the investigation of major evolutionary transitions. We discuss two new tools of this kind. First, the 'near-variant test' can be used to compare the causal adequacy of predictively equivalent representations. Second, 'state-variable gestalt-switching' can be used to gain a useful dual perspective on evolutionary processes that involve both higher and lower level populations.
Evolution, Dec 21, 2015
Model, Data, and Analysis Scripts for The Evolution of Cooperation by the Hankshaw Effect as subm... more Model, Data, and Analysis Scripts for The Evolution of Cooperation by the Hankshaw Effect as submitted
Black Queen Gene Loss in a Structured Environment The Black Queen Hypothesis (Morris et al. 2012)... more Black Queen Gene Loss in a Structured Environment The Black Queen Hypothesis (Morris et al. 2012): 1) All biological func/ons have a cost. If all things are equal, excluding a func/on causes a fitness advantage 2) Products of 'leaky' biological func/ons are unavoidably made available to the community, thus providing "public goods". Examples of leaky func/ons: 1) Detoxifica/on of an environment 2) Cross-feeding 3) 'Cheaters' are organisms that have lost a vital leaky func/on, but s/ll acquire the result of the func/on through the environment by comple/on of this func/on by 'helper' organisms 4) The fitness of cheaters and helpers is negaFvely frequency dependent, which means each has an advantage when rare. Therefore, they can coexist, preven/ng the loss of the Black Queen func/on in a "Tragedy of the Commons"
This repository contains the model, data, and analysis corresponding to <em>Negative Niche ... more This repository contains the model, data, and analysis corresponding to <em>Negative Niche Construction Favors the Evolution of Cooperation</em> by Brian D. Connelly, Katherine J. Dickinson, Sarah P. Hammarlund, and Benjamin Kerr after addressing feedback from two anonymous reviewers.
The American Naturalist, Jul 1, 2018
Organisms often modify their environments to their advantage through a process of niche construct... more Organisms often modify their environments to their advantage through a process of niche construction. Environments that are improved through positive niche construction can be viewed as a public good. If free riders appear that do not contribute to the shared resource and therefore do not incur any associated costs, the constructed niche may become degraded, resulting in a tragedy of the commons and the extinction of niche constructors. Niche construction can persist if free riders are excluded, for example, if niche constructors monopolize the resource they produce to a sufficient degree. We suggest, however, that the problem of free riders remains because it is possible that nonniche constructors with an enhanced ability to access the resource appear and invade a population of constructors. Using mathematical models we show that positive niche construction can be maintained if it is inextricably linked to a mechanism that makes free riding costly, such as a trait that confers a benefit to only niche constructors. We discuss this finding in terms of genetic interactions and illustrate the principle with a two-locus model. We conclude that positive niche construction can both evolve and be maintained when it has other beneficial effects via pleiotropy. This situation may apply generally to the evolutionary maintenance of cooperation.
Frontiers in Microbiology, Jul 28, 2015
Many bacteria secrete compounds which act as public goods. Such compounds are often under quorum ... more Many bacteria secrete compounds which act as public goods. Such compounds are often under quorum sensing (QS) regulation, yet it is not understood exactly when bacteria may gain from having a public good under QS regulation. Here, we show that the optimal public good production rate per cell as a function of population size (the optimal production curve, OPC) depends crucially on the cost and benefit functions of the public good and that the OPC will fall into one of two categories: Either it is continuous or it jumps from zero discontinuously at a critical population size. If, e.g., the public good has accelerating returns and linear cost, then the OPC is discontinuous and the best strategy thus to ramp up production sharply at a precise population size. By using the example of public goods with accelerating and diminishing returns (and linear cost) we are able to determine how the two different categories of OPSs can best be matched by production regulated through a QS signal feeding back on its own production. We find that the optimal QS parameters are different for the two categories and specifically that public goods which provide accelerating returns, call for stronger positive signal feedback.
Evolutionary Ecology Research, Nov 1, 1999
Using a two-locus diallelic population genetic model, we studied the evolution and impact of flam... more Using a two-locus diallelic population genetic model, we studied the evolution and impact of flammable traits in resprouting plants. A 'flammability locus' determines the flammable character of a plant and the frequency of alleles at this locus affects the probability that any plant in the population will burn. A linked 'disturbance locus' determines how a plant fares in the presence or absence of fire. Thus, the frequencies of alleles at the flammability locus influence evolution at the disturbance locus. The evolution of flammability-enhancing alleles is influenced by asymmetries in the genotypic fitnesses as well as by the base flammability of the population and the genetic structure of the system (with tighter linkage increasing the possibility that the population becomes more flammable). We demonstrate that stable polymorphisms of plants differing in flammability alleles are possible. The magnitude of the organism's impact on the flammable character of the environment influences where such polymorphisms are expected. Furthermore, predictions concerning the evolution of alleles at the disturbance locus based solely on fitness asymmetries may fail due to the influence of plants on their environment. Unusual population dynamics, including stable and unstable cycles of genotypes, are also presented. The relation of this model to the Mutch hypothesis and the recently developed theories of 'niche construction' and 'ecosystem engineering' is discussed.
Journal of Theoretical Biology, Sep 1, 2015
Cambridge University Press eBooks, May 1, 2008
Molecular Ecology, Dec 1, 2015
Populations of organisms routinely face abiotic selection pressures, and a central goal of evolut... more Populations of organisms routinely face abiotic selection pressures, and a central goal of evolutionary biology is to understand the mechanistic underpinnings of adaptive phenotypes. Ultraviolet radiation (UVR) is one of earth's most pervasive environmental stressors, potentially damaging DNA in any organism exposed to solar radiation. We explored mechanisms underlying differential survival following UVR exposure in genotypes of the water flea Daphnia melanica derived from natural ponds of differing UVR intensity. The UVR tolerance of a D. melanica genotype from a high-UVR habitat depended on the presence of visible and UV-A light wavelengths necessary for photoenzymatic repair of DNA damage, a repair pathway widely shared across the tree of life. We then measured the acquisition and repair of cyclobutane pyrimidine dimers, the primary form of UVR-caused DNA damage, in D. melanica DNA following experimental UVR exposure. We demonstrate that genotypes from high-UVR habitats repair DNA damage faster than genotypes from low-UVR habitats in the presence of visible and UV-A radiation necessary for photoenzymatic repair, but not in dark treatments. Because differences in repair rate only occurred in the presence of visible and UV-A radiation, we conclude that differing rates of DNA repair, and therefore differential UVR tolerance, are a consequence of variation in photoenzymatic repair efficiency. We then rule out a simple gene expression hypothesis for the molecular basis of differing repair efficiency, as expression of the CPD photolyase gene photorepair did not differ among D. melanica lineages, in both the presence and absence of UVR.
Current Opinion in Microbiology, Oct 1, 2014
In this review, we demonstrate how game theory can be a useful first step in modeling and underst... more In this review, we demonstrate how game theory can be a useful first step in modeling and understanding interactions among bacteria that produce and resist antibiotics. We introduce the basic features of evolutionary game theory and explore model microbial systems that correspond to some classical games. Each game discussed defines a different category of social interaction with different resulting population dynamics (exclusion, coexistence, bistability, cycling). We then explore how the framework can be extended to incorporate some of the complexity of natural microbial communities. Overall, the game theoretical perspective helps to guide our expectations about the evolution of some forms of antibiotic resistance and production because it makes clear the precise nature of social interaction in this context.
Environmental Microbiology, Oct 14, 2015
Microbes perform many costly biological functions that benefit themselves, and may also benefit n... more Microbes perform many costly biological functions that benefit themselves, and may also benefit neighbouring cells. Losing the ability to perform such functions can be advantageous due to cost savings, but when they are essential for growth, organisms become dependent on ecological partners to compensate for those losses. When multiple functions may be lost, the ecological outcomes are potentially diverse, including independent organisms only; oneway dependency, where one partner performs all functions and others none; or mutual interdependency where partners perform complementary essential functions. What drives these different outcomes? We develop a model where organisms perform 'leaky' functions that provide both private and public benefits to explore the consequences of privatization level, costs and essentiality on influencing these outcomes. We show that mutual interdependency is favoured at intermediate levels of privatization for a broad range of conditions. One-way dependency, in contrast, is only favoured when privatization is low and loss-of-function benefits are accelerating. Our results suggest an interplay between privatization level and shape of benefits from loss in driving microbial dependencies. Given the ubiquity of microbial functions that are inevitably leaked and the ease of mutational inactivation, our findings may help to explain why microbial interdependencies are common in nature.
American Journal of Human Biology, 2004
Skip to Main Content. ...
Bulletin of the American Physical Society, Mar 14, 2016
Sewall Wright introduced the metaphor of the adaptive landscape, a map from genotype to fitness, ... more Sewall Wright introduced the metaphor of the adaptive landscape, a map from genotype to fitness, more than 80 years ago to help describe his view of adaptive evolution. This metaphor has been immensely popular and has been used in a variety of incarnations. However, a systematic study of the genotype-fitness map presents significant problems. The space of possible genotypes is vast, and the mapping is likely dependent on both environment and the composition of genotypes in a population. In this talk, I will discuss some of these problems and present experimental strategies for uncovering features of adaptive landscapes. In particular, I will discuss how population structure can be used as an experimental variable to elucidate landscape topography and how a combination of experimental evolution and genetic engineering can reveal important landscape features in changing environments. I will also present some potential applications of this work to the problem of antibiotic resistance and potential implications for evolutionary rescue in the face of global climate change. For some of these topics, the classic notion of the adaptive landscape must itself be adapted; however, I propose that there are fruitful ways to continue to apply this metaphor.