Biology subjects

Ashby, B.

Publications and source records attributed to Ashby, B..

15 recordsLinked to original sources

bioRxiv2026

Spatial structure drives the evolution of parasites into host defense systems

Host defense systems in prokaryotes and eukaryotes often appear to be derived from the very parasites they now defend against, yet the evolutionary route for such a transition remains poorly understood. Based on the biology of integrating viruses such as temperate bacteriophages and retroviruses, we develop a multilevel eco-evolutionary framework in which within-host viral replication is treated as a public goods game over a costly, shared replication product. In well-mixed host populations, we predict convergence on a single viral strategy of intermediate replicative investment. However, when we impose spatial structure by restricting host reproduction and virus transmission to local events, the virus population diversifies into two lineages: a horizontally transmitted lineage that parasitises hosts, and a vertically transmitted hyperparasitic lineage that parasitises the horizontally transmitting viruses. The latter "hyperparasite" is a viral cheat that suppresses the replication and propagation of the parasitic virus, thereby acting as a defense system to the hosts. Local interactions concentrate the benefits of this suppression among neighbouring hosts that carry related proviruses, allowing selection on the proviral cheat as a host-level defense. Our results show that evolutionary cheating within parasite populations can drive the evolution of parasites into defense systems in spatially structured host populations.

evolutionary biology↗

bioRxiv2026

Sublethal immune resistance to parasites generates reaction-norm patterns indistinguishable from tolerance

Hosts defend themselves against parasites through resistance (reducing parasite burden) and tolerance (reducing the fitness cost of infection without affecting parasites). This distinction has important evolutionary implications: resistance is predicted to maintain polymorphism while tolerance tends to fix, and only resistance is expected to provoke parasite counter-adaptation. The reaction-norm framework, which infers tolerance from the slope of host fitness regressed on parasite burden, assumes that a shallow slope reflects parasite-independent host protection. We test this assumption using a within-host model in two variants: microparasites (Model 1, with within-host replication) and macroparasites (Model 2, without). Sublethal immunity impairs the parasites host-exploitation rate, reducing both growth and per-parasite virulence without killing them. We show that this generates systematic slope differences among host genotypes that the framework interprets as variation in tolerance. Furthermore, the ranking of genotypes slopes reverses between linear and sigmoidal damage functions: under linear damage, the strongest immune responder appears most tolerant; under sigmoidal damage, the weakest responder does. Decomposition of the damage reduction shows that virulence reduction accounts for the majority of the effect across both model variants. Thus, the reaction-norm slope cannot determine whether host fitness is maintained by parasite-independent tissue protection or by sublethal impairment of parasites.

evolutionary biology↗

bioRxiv2026

Guarding versus self-guarding in innate immunity

Hosts have evolved a variety of innate immune responses to pathogens. In many cases, hosts directly detect pathogen-associated molecular patterns (PAMPs) or pathogen effectors to trigger an immune response. However, hosts may also detect pathogens indirectly through guarding, whereby immune receptors ( guards) monitor the effects of pathogens (e.g., modification of target cells) rather than the pathogens themselves. Guarding poses a different evolutionary challenge for pathogens than direct recognition of PAMPs, as replication may necessitate the modification or disruption of guarded host proteins ( guardees). Recently, self-guarding has been discovered, in which the host target functions as both guard and guardee. Self-guarding appears to present an intractable problem for pathogens: modification of the host target may benefit replication, but also triggers an immune response. If self-guarding creates an apparently inescapable detection mechanism, why has self-guarding only recently been discovered? Here, we use mathematical models of within-host pathogen and immune dynamics to compare guarding and self-guarding architectures. We show that self-guarding leads to a more rapid immune response and faster pathogen suppression, but is also more prone to false-positive immune responses, likely imposing greater costs through autoimmunity. We therefore hypothesise that the greater potential for false-positive immune responses may limit the conditions under which self-guarding evolves.

evolutionary biology↗

bioRxiv2025

Coevolutionary cycling in allele frequencies and the evolution of virulence

Coevolutionary cycling in allele frequencies due to negative frequency-dependent selection--sometimes referred to as Red Queen Dynamics--is a key potential outcome of host-parasite coevolution. While many theoretical studies have focused on understanding the consequences of coevolutionary cycling for the evolution of sex and recombination, little is known about the impact of coevolutionary cycling on the evolution of other life history traits. It is therefore currently unknown how coevolutionary cycling in allele frequencies affects the evolution of key disease characteristics, such as virulence. Here, we combine population genetic and quantitative genetic approaches to theoretically determine the impacts of coevolutionary cycling in allele frequencies on the evolution of virulence in a free-living parasite. By varying the level of genetic specificity required for infection while controlling for the average infection rate, we induce coevolutionary cycles and examine their effects on virulence evolution. We show that coevolutionary cycling does indeed have a strong impact on virulence evolution, with more specific infection genetics and higher allelic diversity generally driving larger and more rapid cycles in allele frequencies, leading to selection for higher virulence. Our research provides new fundamental insights into the relationship between coevolutionary cycling and the evolution of virulence.

evolutionary biology↗

bioRxiv2023

Coevolution of age-structured tolerance and virulence

AO_SCPLOWBSTRACTC_SCPLOWHosts can evolve a variety of defences against parasitism, including resistance (which prevents or reduces the spread of infection) and tolerance (which protects against virulence). Some organisms have evolved different levels of tolerance at different life-stages, which is likely to be the result of coevolution with pathogens, and yet it is currently unclear how coevolution drives patterns of age-specific tolerance. Here, we use a model of tolerance-virulence coevolution to investigate how age structure influences coevolutionary dynamics. Specifically, we explore how coevolution unfolds when tolerance and virulence (disease-induced mortality) are age-specific compared to when these traits are uniform across the host lifespan. We find that coevolutionary cycling is relatively common when host tolerance is age-specific, but cycling does not occur when tolerance is the same across all ages. We also find that age-structured tolerance can lead to selection for higher virulence in shorter-lived than in longer-lived hosts, whereas non-age-structured tolerance always leads virulence to increase with host lifespan. Our findings therefore suggest that age structure can have substantial qualitative impacts on host-pathogen coevolution.

evolutionary biology↗

bioRxiv2023

Separation of Evolutionary Timescales in Coevolving Species

AO_SCPLOWBSTRACTC_SCPLOWMany coevolutionary processes, including host-parasite and host-symbiont interactions, involve one species or trait which evolves much faster than the other. Whether or not a coevolutionary trajectory converges depends on the relative rates of evolutionary change in the two species, and so current adaptive dynamics approaches generally either determine convergence stability by considering arbitrary (often comparable) rates of evolutionary change or else rely on necessary or sufficient conditions for convergence stability. We propose a method for determining convergence stability in the case where one species is expected to evolve much faster than the other. This requires a second separation of timescales, which assumes that the faster evolving species will reach its evolutionary equilibrium (if one exists) before a new mutation arises in the more slowly evolving species. This method, which is likely to be a reasonable approximation for many coevolving species, both provides straightforward conditions for convergence stability and is less computationally expensive than traditional analysis of coevolution models, as it reduces the trait space from a two-dimensional plane to a one-dimensional manifold. In this paper, we present the theory underlying this new separation of timescales and provide examples of how it could be used to determine coevolutionary outcomes from models.

evolutionary biology↗

bioRxiv2023

Hyperparasitism and the evolution of parasite virulence

AO_SCPLOWBSTRACTC_SCPLOWHyperparasites (species which parasitise other parasites) are common in natural populations, affecting many parasitic taxa, including: eukaryotic parasites; bacterial and fungal pathogens. Hyperparasitism is therefore likely to shape the ecology and evolution of many host-parasite systems, representing a promising method for biocontrol (e.g., treating antimicrobial resistant infections). However, the eco-evolutionary consequences of hyperparasitism have received little attention. We use a host-parasite-hyperparasite model to explore how introducing a hyperparasite drives the evolution of parasite virulence, and what impact this has on the host population. We show when the introduction of a hyperparasite selects for higher or lower parasite virulence, and the changes in virulence experienced by the host population. Crucially, we show that variation in the direct effects of hyperparasites on virulence and transmission, and the probability of co-transmission, can lead to a previously unseen hysteresis effect, whereby small shifts in hyperparasite characteristics can lead to sudden shifts in parasite virulence. We also show that hyperparasites can induce diversification in parasite virulence, leading to the coexistence of high and low virulence strains. Our results show hyperparasites can have dramatic effects on the evolution of parasite virulence, and that the use of hyperparasites in biocontrol should be approached with caution.

evolutionary biology↗

bioRxiv2022

Tolerance-conferring defensive symbionts and the evolution of parasite virulence

AO_SCPLOWBSTRACTC_SCPLOWDefensive symbionts in the host microbiome can confer protection from infection or reduce the harms of being infected by a parasite. Defensive symbionts are therefore promising agents of biocontrol that could be used to control or ameliorate the impact of infectious diseases. Previous theory has shown how symbionts can evolve along the parasitism-mutualism continuum to confer greater or lesser protection to their hosts, and in turn how hosts may coevolve with their symbionts to potentially form a mutualistic relationship. However, the consequences of introducing a defensive symbiont for parasite evolution and how the symbiont may coevolve with the parasite have received relatively little theoretical attention. Here, we investigate the ecological and evolutionary implications of introducing a tolerance-conferring defensive symbiont into an established host-parasite system. We show that while the defensive symbiont may initially have a positive impact on the host population, parasite and symbiont evolution tend to have a net negative effect on the host population in the long-term. This is because the introduction of the defensive symbiont always selects for an increase in parasite virulence and may cause diversification into high- and low-virulence strains. Even if the symbiont experiences selection for greater host protection, this simply increases selection for virulence in the parasite, resulting in a net negative effect on the host population. Our results therefore suggest that tolerance-conferring defensive symbionts may be poor biocontrol agents for population-level infectious disease control. LO_SCPLOWAYC_SCPLOW SO_SCPLOWUMMARYC_SCPLOWDefensive symbionts - microbes that confer protection to a host against a harmful parasite - are found throughout the natural world and represent promising candidates for biological control to combat infectious diseases. Symbionts can protect their hosts through a variety of mechanisms that may prevent infection (resistance) or increase survival following infection (tolerance), yet our understanding of the ecological and evolutionary impact of defensive symbionts on parasites is limited. Moreover, few theoretical predictions exist for how defensive symbionts are likely to evolve in the presence of parasites, and for the net effect on the host population. Using a mathematical model where defensive symbionts reduce parasite virulence (harm to the host), we investigate the impact of their introduction on the evolution of parasite virulence, how selection increases or decreases host protection, and whether such symbionts are beneficial for the host population. We find that this form of defensive symbiosis always selects for higher parasite virulence and that it can cause the parasite to diversify into high and low virulence strains which specialise on different host subpopulations. Crucially, we show that the introduction of a defensive symbiont will always lead to a long-term reduction in host population size even if they are beneficial in the short-term. Together, our results show that defensive symbionts can have a strong impact on the evolution of virulence and that this form of host protection is not robust, indicating that tolerance-conferring symbionts are likely to be poor candidates for biological control of infectious diseases at the population level.

evolutionary biology↗

bioRxiv2022

The Evolution of the Age of Onset of Resistance to Infectious Disease

AO_SCPLOWBSTRACTC_SCPLOWMany organisms experience an increase in disease resistance as they age but the time of life at which this change occurs varies. Increases in resistance are partially due to prior exposure and physiological constraints but these cannot fully explain the observed patterns of age-related resistance. An alternative explanation is that developing resistance at an earlier age incurs costs to other life-history traits. Here, we explore how trade-offs with host reproduction or mortality affect the evolution of the onset of resistance, depending on when during the hosts life-cycle the costs are paid (only when resistance is developing, only when resistant or throughout the lifetime). We find that the timing of the costs is crucial to determining evolutionary outcomes, often making the difference between resistance developing at an early or late age. Accurate modelling of biological systems therefore relies on knowing not only the shape of trade-offs but also when they take effect. We also find that the evolution of the rate of onset of resistance can result in evolutionary branching. This provides an alternative, possible evolutionary history of populations which are dimorphic in disease resistance, where the rate of onset of resistance has diversified rather than the level of resistance.

evolutionary biology↗

bioRxiv2022

The evolution of age-specific resistance to infectious disease

AO_SCPLOWBSTRACTC_SCPLOWInnate, infection-preventing resistance often varies between host life-stages. Juveniles are more resistant than adults in some species, whereas the opposite pattern is true in others. This variation cannot always be explained by prior exposure or physiological constraints and so it has been hypothesised that trade-offs with other life-history traits may be involved. However, little is known about how trade-offs between various life-history traits and resistance at different life-stages affect the evolution of age-specific resistance. Here, we use a mathematical model to explore how trade-offs with natural mortality, reproduction and maturation combine to affect the evolution of resistance at different life-stages. Our results show that certain combinations of trade-offs have substantial effects on whether adults or juveniles are more resistant, with trade-offs between juvenile resistance and adult reproduction inherently more costly than trade-offs involving maturation or mortality (all else being equal), resulting in consistent evolution of lower resistance at the juvenile stage even when infection causes a lifelong fecundity reduction. Our model demonstrates how the differences between patterns of age-structured resistance seen in nature may be explained by variation in the trade-offs involved and our results suggest conditions under which trade-offs tend to select for lower resistance in juveniles than adults.

evolutionary biology↗

bioRxiv2020

Social information use shapes the coevolution of sociality and virulence

AO_SCPLOWBSTRACTC_SCPLOWSocial contacts can facilitate the spread of both survival-related information and infectious diseases, but little is known about how these processes combine to shape host and parasite evolution. Here, we use a theoretical model that captures both infection and information transmission processes to investigate how host sociality (contact effort) and parasite virulence (disease-associated mortality rate) (co)evolve. We show that selection for sociality (and in turn, virulence) depends on both the intrinsic costs and benefits of social information and infection as well as their relative prevalence in the population. Specifically, greater sociality and lower virulence evolve when the risk of infection is either low or high and social information is neither very common nor too rare. Lower sociality and higher virulence evolve when the prevalence patterns are reversed. When infection and social information are both at moderate levels in the population, the direction of selection depends on the relative costs and benefits of being infected or informed. We also show that sociality varies inversely with virulence, and that parasites may be unable to prevent runaway selection for higher contact efforts. Together, these findings provide new insights for our understanding of group living and how apparently opposing ecological processes can influence the evolution of sociality and virulence in a range of ways.

evolutionary biology↗

bioRxiv2020

When does parasitism maintain sex in the absence of Red Queen Dynamics?

AO_SCPLOWBSTRACTC_SCPLOWParasites can select for sexual reproduction in host populations, preventing replacement by faster growing asexual lineages. This is usually attributed to so-called "Red Queen Dynamics" (RQD), where antagonistic coevolution causes fluctuating selection in allele frequencies, which provides sex with an advantage over asex. However, parasitism may also maintain sex in the absence of RQD when sexual populations are more genetically diverse - and hence more resistant, on average - than clonal populations, allowing sex and asex to stably coexist. While the maintenance of sex due to RQD has been studied extensively, the conditions that allow sex and asex to stably coexist have yet to be explored in detail. In particular, we lack an understanding of how host demography and parasite epidemiology affect the maintenance of sex in the absence of RQD. Here, I use an eco-evolutionary model to show that both population density and the type and strength of virulence are important for maintaining sex, which can be understood in terms of their effects on disease prevalence and severity. In addition, I show that even in the absence of heterozygote advantage, asexual heterozygosity affects coexistence with sex due to variation in niche overlap. These results reveal which host and parasite characteristics are most important for the maintenance of sex in the absence of RQD, and provide empirically testable predictions for how demography and epidemiology mediate competition between sex and asex.

evolutionary biology↗

bioRxiv2020

How do sex biases in demography and disease characteristics affect the spread of sexually transmitted infections?

The epidemiology of sexually transmitted infections (STIs) is inherently linked to host mating dynamics. Studies across many taxa show that adult sex ratio, a major determinant of host mating dynamics, is often skewed - sometimes strongly - toward males or females. However, few predictions exist for the effects of skewed sex ratio on STI epidemiology, and none when coupled with sex biased disease characteristics. Here we use mathematical modelling to examine how interactions between sex ratio and disease characteristics affect STI prevalence in males and females. Notably, we find that while overall disease prevalence peaks at equal sex ratios, prevalence per sex peaks at skewed sex ratios. Furthermore, disease characteristics, sex-biased or not, drive predictable differences in male and female STI prevalence as sex ratio varies, with higher transmission and lower virulence generally increasing differences between the sexes for a given sex ratio. These findings may be due to a balance between increased per-capita mating in the less common sex, and a reduction in mating rate - hence disease prevalence - at the population level. Our work reveals new insights into how STI prevalence in males and females depends on a complex interaction between host population sex ratio and disease characteristics.

animal behavior and cognition↗

bioRxiv2019

An inordinate fondness for species with intermediate dispersal abilities

AO_SCPLOWBSTRACTC_SCPLOWJBS Haldane is widely quoted to have quipped that the Creator, if one exists, has an inordinate fondness for beetles. Although Coleoptera may not be the most speciose order once Hymenopteran diversity is fully accounted for, as a whole the very clear differences in species diversity among taxa require an explanation. Here we show both analytically and through stochastic simulations that dispersal has eco-evolutionary effects that predict taxa to become particularly species-rich when dispersal is neither too low nor too high. Our models combine recent advances in understanding coexistence in niche space with previously verbally expressed ideas, where too low dispersal imposes biogeographic constraints that prevent a lineage from finding new areas to colonize (reducing opportunities for speciation), while too high dispersal impedes population divergence, leading to few but widely distributed species. We show that this logic holds for species richness and is robust to a variety of model assumptions, but peak diversification rate is instead predicted to increase with dispersal. Our work unifies findings of increasing and decreasing effects of dispersal rate on speciation, and explains why organisms with moderate dispersal abilities have the best prospects for high global species richness.

evolutionary biology↗

bioRxiv2019

Antagonistic coevolution between hosts and sexually transmitted infections

AO_SCPLOWBSTRACTC_SCPLOWSexually transmitted infections (STIs) are predicted to play an important role in the evolution of host mating strategies, and vice versa, yet our understanding of host-STI coevolution is limited. Here, I present a model of acute STI infection in populations with ephemeral mating dynamics, where hosts evolve their preference for healthy mates and STIs evolve mortality or sterility virulence. Mate choice readily evolves even though ephemeral mating and acute infections reduce the advantages of mate choice compared to previous theory based on serial monogamy and chronic infections. Selection for mate choice constrains both mortality and sterility virulence, leading to optimal strategies in each population, host polymorphism, or fluctuating selection. I show how the mode of virulence, costs associated with mate choice, recovery, and host lifespan impact on host-STI coevolution, with fluctuating selection most likely when hosts have intermediate lifespans, STIs cause sterility and longer infections, and costs of mate choice are not too high. The results reveal new insights into the evolution of mate choice and how coevolution unfolds for different host and STI life-history traits, providing increased support for parasite-mediated sexual selection as a potential driver of host mate choice, and mate choice as a constraint on STI virulence.

evolutionary biology↗