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Biology subjects

West, S. A.

Publications and source records attributed to West, S. A..

12 recordsLinked to original sources

Carbon-phosphorous exchange rate constrains growth of arbuscular mycorrhizal fungal networks

Symbiotic nutrient exchange between arbuscular mycorrhizal (AM) fungi and their host plants varies widely depending on their physical, chemical, and biological environment. Yet dissecting this context dependency remains challenging because we lack methods for tracking nutrients such as carbon (C) and phosphorus (P). Here, we developed a new approach to quantitatively estimate C and P fluxes in the AM symbiosis from comprehensive network morphology quantification, achieved by robotic imaging and machine learning based on roughly 100 million hyphal shape measurements. We found that rates of C transfer from the plant and P transfer from the fungus were, on average, related proportionally to one another. This ratio was nearly invariant across AM fungal strains despite contrasting growth phenotypes, but was strongly affected by plant host genotype. Fungal phenotype distributions were bounded by a Pareto front with a shape favoring specialization in an exploration-exploitation trade-off. This means AM fungi can be fast range expanders or fast resource extractors, but not both. Manipulating the C/P exchange rate by swapping the plant host genotype shifted this Pareto front, indicating that the exchange rate constrains possible AM fungal growth strategies. We show by mathematical modeling how AM fungal growth at fixed exchange rate leads to qualitatively different symbiotic outcomes depending on fungal traits and nutrient availability.

biophysics↗

The evolution of signalling and eavesdropping in plant-fungal networks

Experiments have shown that when one plant is attacked by a pathogen or herbivore, this can lead to other plants connected to the same mycorrhizal network upregulating their defence mechanisms. It has been hypothesised that this represents signalling, with attacked plants producing a signal to warn other plants of impending harm. We examined the evolutionary plausibility of this and other hypotheses theoretically. We found that the evolution of plant signalling about an attack requires restrictive conditions, and so will rarely be evolutionarily stable. The problem is that signalling about an attack provides a benefit to competing neighbours, even if they are kin, and so reduces the relative fitness of signalling plants. Indeed, selection is often more likely to push plant behaviour in the opposite direction - with plants signalling dishonestly about an attack that has not occurred, or by suppressing a cue that they have been attacked. Instead, we show that there are two viable alternatives that could explain the empirical data: (1) the process of being attacked leads to a cue (information about the attack) which is too costly for the attacked plant to fully suppress; (2) mycorrhizal fungi monitor their host plants, detect when they are attacked, and then the fungi signal this information to warn other plants in their network. Our results suggest the empirical work that would be required to distinguish between these possibilities. Significance statementExperiments have shown that when one plant is attacked by a herbivore, this can lead to other plants connected to the same mycorrhizal network upregulating their defence mechanisms. It has been hypothesised that this represents signalling, with attacked plants producing a signal to warn other plants of impending harm. We found theoretically that plant warning signals are rarely evolutionarily stable. Instead, we identify two viable alternatives that could explain the empirical data: (1) being attacked leads to a cue (information about the attack) which is too costly for the attacked plant to suppress; (2) mycorrhizal fungi monitor their host plants, detect when they are attacked, and then the fungi signal this information to warn other plants in their network.

evolutionary biology↗

Signatures of kin selection in a natural population of the bacteria Bacillus subtilis

Laboratory experiments have suggested that bacteria perform a range of cooperative behaviours, which are favoured because they are directed towards relatives (kin selection). However, there is a lack of evidence for cooperation and kin selection in natural bacterial populations. Molecular population genetics offers a promising method to study natural populations, because theory predicts that kin selection will lead to relaxed selection, which will result in increased polymorphism and divergence at cooperative genes. Examining a natural population of Bacillus subtilis, we found consistent evidence that putatively cooperative traits have higher polymorphism and greater divergence than putatively private traits expressed at the same rate. In addition, we were able to eliminate alternative explanations for these patterns, and found more deleterious mutations in genes controlling putatively cooperative traits. Overall, our results suggest cooperation favoured by kin selection, with an average relatedness of r=0.77 between interacting individuals.

evolutionary biology↗

The evolution of manipulative cheating

A social cheat is typically assumed to be an individual that does not perform a cooperative behaviour, or performs less of it, but can still exploit the cooperative behaviour of others. However, empirical data suggests that cheating can be more subtle, involving evolutionary arms races over the ability to both exploit and resist exploitation. These complications have not been captured by evolutionary theory, which lags behind empirical studies in this area. We bridge this gap with a mixture of game-theoretical models and individual-based simulations, examining what conditions favour more elaborate patterns of cheating. We found that as well as adjusting their own behaviour, individuals can be selected to manipulate the behaviour of others, which we term manipulative cheating. Further, we found that manipulative cheating can lead to dynamic oscillations (arms races), between selfishness, manipulation, and suppression of manipulation. Our results can help explain both variation in the level of cheating, and genetic variation in the extent to which individuals can be exploited by cheats.

evolutionary biology↗

Parental control: ecology drives plasticity in parental response to offspring signals

Different bird species have completely different parent-offspring interactions. When food is plentiful, the chicks that are begging the loudest are fed the most. When food is scarce, bird species instead feed the largest offspring. While this variation could be due to parents responding to signalling differently based on food availability, it could equally be due to offspring adjusting their behaviour, or to variation in information availability. We tested between these competing explanations experimentally, by manipulating food availability in a population of wild great tits, Parus major, while standardising offspring behaviour and size. We found that when food was more plentiful, parents were: (1) more likely to preferentially feed the chicks that were begging the most; and (2) less likely to preferentially feed larger chicks. In addition, we consistently found these same patterns, in a meta-analysis across 57 bird species. Overall, our results suggest that parents have more control over food distribution than offspring do, and that they flexibly adjust how they respond to both offspring signals and cues of offspring quality in response to food availability. Consequently, depending upon environmental conditions, predictably different signalling systems are favoured.

animal behavior and cognition↗

Solving the sex ratio scandal in Melittobia wasps

The scandalous sex ratio behaviour of Melittobia wasps has long posed one of the greatest problems for the field of sex allocation. In contrast to the predictions of theory, and the behaviour of numerous other organisms, laboratory experiments have found that Melittobia females do not produce less female-biased offspring sex ratios when more females lay eggs on a patch. We resolve this scandal, by showing that, in nature, females of M. australica have sophisticated sex ratio behaviour, where their strategy also depends upon whether they have dispersed from the patch where they emerged. When females have not dispersed, they will be laying eggs with close relatives, which keeps local mate competition high, even with multiple females, and so they are selected to produce consistently female-biased sex ratios. Laboratory experiments mimic these conditions. In contrast, when females disperse, they will be interacting with non-relatives, and so they adjust their sex ratio depending upon the number of females laying eggs. Consequently, females appear to use dispersal status as an indirect cue of relatedness, and whether they should adjust their sex ratio in response to the number of females laying eggs on the patch.

evolutionary biology↗

Dividing labour in social microorganisms: coordinated or random specialisation?

In bacteria and other microorganisms, the cells within a population often show extreme phenotypic variation. Different species use different mechanisms to determine how distinct phenotypes are allocated between individuals, including coordinated, random, and genetic determination. However, it is not clear if this diversity in mechanisms is adaptive--arising because different mechanisms are favoured in different environments--or is merely the result of non-adaptive artifacts of evolution. We use theoretical models to analyse the relative advantages of the two dominant mechanisms to divide labour between reproductives and helpers in microorganisms. We show that coordinated specialisation is more likely to evolve over random specialisation in well-mixed groups when: (i) social groups are small; (ii) helping is more "essential"; and (iii) there is a low metabolic cost to coordination. We find analogous results when we allow for spatial structure with a more detailed model of cellular filaments. More generally, this work shows how diversity in the mechanisms to produce phenotypic heterogeneity could have arisen as adaptations to different environments.

evolutionary biology↗

Can natural selection favour indiscriminate spite?

Spiteful behaviours occur when an actor harms its own fitness to inflict harm on the fitness of others. Several papers have predicted that spite can be favoured in sufficiently small populations, even when the harming behaviour is directed indiscriminately at others. However, it is not clear that truly spiteful behaviour could be favoured without the harm being directed at a subset of social partners with relatively low genetic similarity to the actor (kin discrimination). Using mathematical models, we show that: (1) the evolution of spite requires kin discrimination; (2) previous models suggesting indiscriminate spite involve scenarios where the actor gains a direct feedback benefit from harming others, and so the harming is selfish rather than spiteful; (3) extreme selfishness can be favoured in small populations (and in some cases small groups) because this is where the feedback benefit of harming is greatest.

evolutionary biology↗

Adaptation and the Parliament of Genes

Our modern understanding of adaptation by natural selection rests on assumptions about genes working together to produce organisms. However, there is considerable evidence for selfish genetic elements that distort the behaviour of individuals to increase their own transmission. How can we reconcile these opposing notions? We use a combination of population genetics, agent-based simulation, and game theory to model the evolution of both selfish genetic elements and genes that could suppress their distortion. We found that: (1) suppressor genes are more likely to be favoured when selfish genetic elements cause greater distortion; (2) selection on selfish genetic elements favours the evolution of greater distortion, making them more likely to be suppressed. We found these same results when examining an abstract model designed to illuminate the general principles, and models for three specific scenarios: an X chromosome driver, an imprinted gene, and a bacterial plasmid. Our results suggest that selection on selfish genetic elements will often drive coevolution with suppressors in a way that removes the impact of genetic conflict at the level of the individual.

evolutionary biology↗

The evolution of collective infectious units in viruses

Viruses frequently spread among cells or hosts in groups, with multiple viral genomes inside the same infectious unit. These collective infectious units can consist of multiple viral genomes inside the same virion, or multiple virions inside a larger structure such as a vesicle. Collective infectious units deliver multiple viral genomes to the same cell simultaneously, which can have important implications for viral pathogenesis, antiviral resistance, and social evolution. However, little is known about why some viruses transmit in collective infectious units, whereas others do not. We used a simple evolutionary approach to model the potential costs and benefits of transmitting in a collective infectious unit. We found that collective infectious units could be favoured if cells infected by multiple viral genomes were significantly more productive than cells infected by just one viral genome, and especially if there were also efficiency benefits to packaging multiple viral genomes inside the same infectious unit. We also found that if some viral sequences are defective, then collective infectious units could evolve to become very large, but that if these defective sequences interfered with wild-type virus replication, then collective infectious units were disfavoured.

evolutionary biology↗

Crystal Toxins and the volunteer’s dilemma in bacteria

1The growth and virulence of the bacteria Bacillus thuringiensis depends on the production of Cry toxins, which are used to perforate the gut of its host. Successful invasion of the host relies on producing a threshold amount of toxin, after which there is no benefit from producing more toxin. Consequently, the production of Cry toxin appears to be a different type of social problem compared with the public goods scenarios that bacteria often encounter. We show that selection for toxin production is a volunteers dilemma. We make the specific predictions that: (1) selection for toxin production depends upon an interplay between the number of bacterial cells that each host ingests, and the genetic relatedness between those cells; (2) cheats that do not produce toxin gain an advantage when at low frequencies, and at high bacterial density, allowing them to be maintained in a population alongside toxin producing cells. More generally, our results emphasise the diversity of the social games that bacteria play.

evolutionary biology↗

Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown

Cooperative interactions among species, termed mutualisms, have played a crucial role in the evolution of life on Earth. However, despite key potential benefits to partners, there are many cases where two species cease to cooperate, and mutualisms break down. What factors drive the evolutionary breakdown of mutualism? We examined the pathways towards breakdowns of the mutualism between plants and arbuscular mycorrhizal (AM) fungi. Using a comparative approach, we identify ~25 independent cases of complete mutualism breakdown across global seed plants. We found that breakdown of cooperation was only stable when host plants either: (i) partner with other root symbionts or (ii) evolve alternative resource acquisition strategies. Our results suggest that key mutualistic services are only permanently lost if hosts evolve alternative symbioses or adaptations.\n\nSignificance StatementCooperative interactions among species - mutualisms - are major sources of evolutionary innovation. However, despite their importance, two species that formerly cooperated sometimes cease their partnership. Why do mutualisms breakdown? We asked this question in the partnership between arbuscular mycorrhizal (AM) fungi and their plant hosts, one of the most ancient mutualisms. We analyse two potential trajectories towards evolutionary breakdown of their cooperation, symbiont switching and mutualism abandonment. We find evidence that plants stop interacting with AM fungi when they switch to other microbial mutualists or when they evolve alternative strategies to extract nutrients from the environment. Our results show vital cooperative interactions can be lost - but only if successful alternatives evolve.

evolutionary biology↗