Andrew D. Morgan

The effect of migration on local adaptation in a coevolving host¿parasite system

Antagonistic coevolution between hosts and parasites in spatially structured populations can result in local adaptation of parasites; that is, the greater infectivity of local parasites than foreign parasites on local hosts. Such parasite specialization on local hosts has implications for human health and agriculture. By contrast with classic single-species population-genetic models, theory indicates that parasite migration between subpopulations might increase parasite local adaptation, as long as migration does not completely homogenize populations. To test this hypothesis we developed a system-specific mathematical model and then coevolved replicate populations of the bacterium Pseudomonas fluorescens and a parasitic bacteriophage with parasite only, with host only or with no migration. Here we show that patterns of local adaptation have considerable temporal and spatial variation and that, in the absence of migration, parasites tend to be locally maladapted. However, in accord with our model, parasite migration results in parasite local adaptation, but host migration alone has no significant effect.

Host–parasite coevolutionary arms races give way to fluctuating selection

Host-parasite coevolution is a key driver of biological diversity and parasite virulence, but its effects depend on the nature of coevolutionary dynamics over time. We used phenotypic data from coevolving populations of the bacterium Pseudomonas fluorescens SBW25 and parasitic phage SBW25Φ2, and genetic data from the phage tail fibre gene (implicated in infectivity evolution) to show that arms race dynamics, typical of short-term studies, decelerate over time. We attribute this effect to increasing costs of generalism for phages and bacteria with increasing infectivity and resistance. By contrast, fluctuating selection on individual host and parasite genotypes was maintained over time, becoming increasingly important for the phenotypic properties of parasite and host populations. Given that costs of generalism are reported for many other systems, arms races may generally give way to fluctuating selection in antagonistically coevolving populations.

Estimate of the Spontaneous Mutation Rate in Chlamydomonas reinhardtii

The nature of spontaneous mutations, including their rate, distribution across the genome, and fitness consequences, is of central importance to biology. However, the low rate of mutation has made it difficult to study spontaneous mutagenesis, and few studies have directly addressed these questions. Here, we present a direct estimate of the mutation rate and a description of the properties of new spontaneous mutations in the unicellular green alga Chlamydomonas reinhardtii. We conducted a mutation accumulation experiment for ∼350 generations followed by whole-genome resequencing of two replicate lines. Our analysis identified a total of 14 mutations, including 5 short indels and 9 single base mutations, and no evidence of larger structural mutations. From this, we estimate a total mutation rate of 3.23 × 10−10/site/generation (95% C.I. 1.82 × 10−10 to 5.23 × 10−10) and a single base mutation rate of 2.08 × 10−10/site/generation (95% C.I., 1.09 × 10−10 to 3.74 × 10−10). We observed no mutations from A/T → G/C, suggesting a strong mutational bias toward A/T, although paradoxically, the GC content of the C. reinhardtii genome is very high. Our estimate is only the second direct estimate of the mutation rate from plants and among the lowest spontaneous base-substitution rates known in eukaryotes.

Selection on non‐social traits limits the invasion of social cheats

While the conditions that favour the maintenance of cooperation have been extensively investigated, the significance of non-social selection pressures on social behaviours has received little attention. In the absence of non-social selection pressures, patches of cooperators are vulnerable to invasion by cheats. However, we show both theoretically, and experimentally with the bacterium Pseudomonas fluorescens, that cheats may be unable to invade patches of cooperators under strong non-social selection (both a novel abiotic environment and to a lesser extent, the presence of a virulent parasite). This is because beneficial mutations are most likely to arise in the numerically dominant cooperator population. Given the ubiquity of novel selection pressures on microbes, these results may help to explain why cooperation is the norm in natural populations of microbes.

Extensive de novo mutation rate variation between individuals and across the genome of Chlamydomonas reinhardtii

Describing the process of spontaneous mutation is fundamental for understanding the genetic basis of disease, the threat posed by declining population size in conservation biology, and much of evolutionary biology. Directly studying spontaneous mutation has been difficult, however, because new mutations are rare. Mutation accumulation (MA) experiments overcome this by allowing mutations to build up over many generations in the near absence of natural selection. Here, we sequenced the genomes of 85 MA lines derived from six genetically diverse strains of the green alga Chlamydomonas reinhardtii. We identified 6843 new mutations, more than any other study of spontaneous mutation. We observed sevenfold variation in the mutation rate among strains and that mutator genotypes arose, increasing the mutation rate approximately eightfold in some replicates. We also found evidence for fine-scale heterogeneity in the mutation rate, with certain sequence motifs mutating at much higher rates, and clusters of multiple mutations occurring at closely linked sites. There was little evidence, however, for mutation rate heterogeneity between chromosomes or over large genomic regions of 200 kbp. We generated a predictive model of the mutability of sites based on their genomic properties, including local GC content, gene expression level, and local sequence context. Our model accurately predicted the average mutation rate and natural levels of genetic diversity of sites across the genome. Notably, trinucleotides vary 17-fold in rate between the most and least mutable sites. Our results uncover a rich heterogeneity in the process of spontaneous mutation both among individuals and across the genome.

Relative number of generations of hosts and parasites does not influence parasite local adaptation in coevolving populations of bacteria and phages

A potential consequence of host–parasite coevolution in spatially structured populations is parasite local adaptation: local parasites perform better than foreign parasites on their local host populations. It has been suggested that the generally shorter generation times of parasites compared with their hosts contributes to parasites, rather than hosts, being locally adapted. We tested the hypothesis that relative generation times of hosts and parasites affect local adaptation of hosts and parasites, using the bacterium Pseudomonas fluorescens and a lytic phage as host and parasite, respectively. Generation times were not directly manipulated, but instead one of the coevolving partners was regularly removed and replaced with a population from an earlier time point. Thus, one partner underwent more generations than the other. Manipulations were carried out at both early and later periods of coevolutionary interactions. At early stages of coevolution, host and parasites that underwent relatively more generations displayed higher levels of resistance and infectivity, respectively. However, the relative number of generations that bacteria and phages underwent did not change the level of local adaptation relative to control populations. This is likely because generalist hosts and parasites are favoured during early stages of coevolution, preventing local adaptation. By contrast, at later stages manipulations had no effect on either average levels of resistance or infectivity, or alter the level of local adaptation relative to the controls, possibly because traits other than resistance and infectivity were under strong selection. Taken together, these data suggest that the relative generation times of hosts and parasites may not be an important determinant of local adaptation in this system.

Higher resources decrease fluctuating selection during host–parasite coevolution

We still know very little about how the environment influences coevolutionary dynamics. Here, we investigated both theoretically and empirically how nutrient availability affects the relative extent of escalation of resistance and infectivity (arms race dynamic; ARD) and fluctuating selection (fluctuating selection dynamic; FSD) in experimentally coevolving populations of bacteria and viruses. By comparing interactions between clones of bacteria and viruses both within- and between-time points, we show that increasing nutrient availability resulted in coevolution shifting from FSD, with fluctuations in average infectivity and resistance ranges over time, to ARD. Our model shows that range fluctuations with lower nutrient availability can be explained both by elevated costs of resistance (a direct effect of nutrient availability), and reduced benefits of resistance when population sizes of hosts and parasites are lower (an indirect effect). Nutrient availability can therefore predictably and generally affect qualitative coevolutionary dynamics by both direct and indirect (mediated through ecological feedbacks) effects on costs of resistance.

Impact of bacterial mutation rate on coevolutionary dynamics between bacteria and phages.

Mutator bacteria are frequently found in natural populations of bacteria and although coevolution with parasitic viruses (phages) is thought to be one reason for their persistence, it remains unclear how the presence of mutators affects coevolutionary dynamics. We hypothesized that phages must themselves adapt more rapidly or go extinct, in the face of rapidly evolving mutator bacteria. We compared the coevolutionary dynamics of wild‐type Pseudomonas fluorescens SBW25 with a lytic phage to the dynamics of an isogenic mutator of P. fluorescens SBW25 together with the same phage. At the beginning of the experiment both wild‐type bacteria and mutator bacteria coevolved with phages. However, mutators rapidly evolved higher levels of sympatric resistance to phages. The phages were unable to “keep‐up” with the mutator bacteria, and these rates of coevolution declined to less than the rates of coevolution between the phages and wild‐type bacteria. By the end of the experiment, the sympatric resistance of the mutator bacteria was not significantly different to the sympatric resistance of the wild‐type bacteria. This suggests that the importance of mutators in the coevolutionary interactions with a particular phage population is likely to be short‐lived. More generally, the results demonstrate that coevolving enemies may escape from Red‐Queen dynamics.

SPONTANEOUS MUTATION ACCUMULATION IN MULTIPLE STRAINS OF THE GREEN ALGA, CHLAMYDOMONAS REINHARDTII

Estimates of mutational parameters, such as the average fitness effect of a new mutation and the rate at which new genetic variation for fitness is created by mutation, are important for the understanding of many biological processes. However, the causes of interspecific variation in mutational parameters and the extent to which they vary within species remain largely unknown. We maintained multiple strains of the unicellular eukaryote Chlamydomonas reinhardtii, for approximately 1000 generations under relaxed selection by transferring a single cell every ∼10 generations. Mean fitness of the lines tended to decline with generations of mutation accumulation whereas mutational variance increased. We did not find any evidence for differences among strains in any of the mutational parameters estimated. The overall change in mean fitness per cell division and rate of input of mutational variance per cell division were more similar to values observed in multicellular organisms than to those in other single‐celled microbes. However, after taking into account differences in genome size among species, estimates from multicellular organisms and microbes, including our new estimates from C. reinhardtii, become substantially more similar. Thus, we suggest that variation in genome size is an important determinant of interspecific variation in mutational parameters.

Effects of antagonistic coevolution on parasite‐mediated host coexistence

Parasites can promote diversity by mediating coexistence between a poorer and superior competitor, if the superior competitor is more susceptible to parasitism. However, hosts and parasites frequently undergo antagonistic coevolution. This process may result in the accumulation of pleiotropic fitness costs associated with host resistance, and could breakdown coexistence. We experimentally investigated parasite‐mediated coexistence of two genotypes of the bacterium Pseudomonas fluorescens, where one genotype underwent coevolution with a parasite (a virulent bacteriophage), whereas the other genotype was resistant to the evolving phages at all time points, but a poorer competitor. In the absence of phages, the resistant genotype was rapidly driven extinct in all populations. In the presence of the phages, the resistant genotype persisted in four of six populations and eventually reached higher frequencies than the sensitive genotype. The coevolving genotype showed a reduction in the growth rate, consistent with a cost of resistance, which may be responsible for a decline in its relative fitness. These results demonstrate that the stability of parasite‐mediated coexistence of resistant and susceptible species or genotypes is likely to be affected if parasites and susceptible hosts coevolve.