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Abstract Given their ubiquity in nature and their importance to human and agricultural health, it is important to gain a better understanding of the drivers of the evolution of infectious disease. Across vertebrates, invertebrates, and plants, defence mechanisms can be expressed either constitutively (always present and costly) or induced (activated and potentially costly only upon infection). Theory has shown that this distinction has important implications to the evolution of defence due to differences in their impact on both individual fitness and the feedback of the population-level epidemiological outcomes such as prevalence. However, despite the fact that pathogens evolve in response to host immunity and that this can have important implications to the evolution of host defence, the implications of coevolution on constitutive and induced immunity have not been examined. Here we show theoretically how and when incorporating host-parasite coevolution between host defences and parasite growth strategies plays an important role in determining the optimum outcome. A key result is that whether the parasite affects host reproduction critically impacts host-parasite coevolution; when the parasite impacts fecundity, selection on the host is largely geared towards minimizing reproductive costs, through reducing investment in reproductively costly constitutive defence when the parasite prevalence is low, but also by investing in immunity to avoid infection or recover when prevalence is high. Our work emphasizes the importance of coevolution and epidemiological feedbacks to the coevolution of hosts and parasites and provides testable predictions of the determinants of constitutive verses induced defence. 

Abstract There is overwhelming evidence that the microbiome can be important to host physiology and fitness. As such, there is interest in and some theoretical work on understanding when hosts and microbiomes (co)evolve so that microbes benefit hosts and hosts favour beneficial microbes. However, the outcome of evolution likely depends on how microbes benefit hosts. Here, we use adaptive dynamics to investigate how host and symbiont evolution depend on whether symbionts increase host lifespan or host reproduction in a simple model of host and symbiont dynamics. In addition, we investigate 2 ways hosts release (and transmit) symbionts: by releasing symbionts steadily during their lifetime or by releasing them at reproduction, potentially increasing symbionts’ chances of infecting the host’s offspring. The former is strict horizontal transmission, whereas the latter is also a form of indirect or “pseudovertical” transmission. Our first key result is that the evolution of symbionts that benefit host fecundity requires pseudovertical transmission, while the evolution of symbionts that benefit host lifespan does not. Furthermore, our second key result is that when investing in host benefits is costly to the free-living symbiont stage, intermediate levels of pseudovertical transmission are needed for selection to favour beneficial symbionts. This is true regardless of fitness effects because release at reproduction increases the free-living symbiont population, which increases competition for hosts. Consequently, hosts could evolve away from traits that favour beneficial symbionts. Generally, our work emphasizes the importance of different forms of vertical transmission and fitness benefits in host, microbiome, and holobiont evolution as highlighted by our prediction that the evolution of fecundity-increasing symbionts requires parent-to-offspring transmission. 

Abstract Mathematical models highlighted the importance of pathogen‐mediated invasion, with the replacement of red squirrels by squirrelpox virus (SQPV) carrying grey squirrels in the UK, a well‐known example.In this study, we combine new epidemiological models, with a range of infection characteristics, with recent longitudinal field and experimental studies on the SQPV dynamics in red and grey squirrel populations to better infer the mechanistic basis of the disease interaction.A key finding is that a model with either partial immunity or waning immunity and reinfection, where individuals become seropositive on the second exposure to infection, that up to now has been shown in experimental data only, can capture the key aspects of the field study observations.By fitting to SQPV epidemic observations in isolated red squirrel populations, we can infer that SQPV transmission between red squirrels is significantly (4×) higher than the transmission between grey squirrels and as a result our model shows that disease‐mediated replacement of red squirrels by greys is considerably more rapid than replacement in the absence of SQPV.Our findings recover the key results of the previous model studies, which highlights the value of simple strategic models that are appropriate when there are limited data, but also emphasise the likely complexity of immune interactions in wildlife disease and how models can help infer disease processes from field data. 

Abstract There is a clear need to understand the effect of human intervention on the evolution of infectious disease. In particular, culling and harvesting of both wildlife and managed livestock populations are carried out in a wide range of management practices, and they have the potential to impact the evolution of a broad range of disease characteristics. Applying eco‐evolutionary theory we show that once culling/harvesting becomes targeted on specific disease classes, the established result that culling selects for higher virulence is only found when sufficient infected individuals are culled. If susceptible or recovered individuals are targeted, selection for lower virulence can occur. An important implication of this result is that when culling to eradicate an infectious disease from a population, while it is optimal to target infected individuals, the consequent evolution can increase the basic reproductive ratio of the infection, , and make parasite eradication more difficult. We show that increases in evolved virulence due to the culling of infected individuals can lead to excess population decline when sustainably harvesting a population. In contrast, culling susceptible or recovered individuals can select for decreased virulence and a reduction in population decline through culling. The implications to the evolution of virulence are typically the same in wildlife populations, that are regulated by the parasite, and livestock populations, that have a constant population size where restocking balances the losses due to mortality. However, the well‐known result that vertical transmission selects for lower virulence and transmission in wildlife populations is less marked in livestock populations for parasites that convey long‐term immunity since restocking can enhance the density of the immune class. Our work emphasizes the importance of understanding the evolutionary consequences of intervention strategies and the different ecological feedbacks that can occur in wildlife and livestock populations. 

Abstract Understanding the interplay between ecological processes and the evolutionary dynamics of quantitative traits in natural systems remains a major challenge. Two main theoretical frameworks are used to address this question, adaptive dynamics and quantitative genetics, both of which have strengths and limitations and are often used by distinct research communities to address different questions. In order to make progress, new theoretical developments are needed that integrate these approaches and strengthen the link to empirical data. Here, we discuss a novel theoretical framework that bridges the gap between quantitative genetics and adaptive dynamics approaches. ‘Oligomorphic dynamics’ can be used to analyse eco‐evolutionary dynamics across different time scales and extends quantitative genetics theory to account for multimodal trait distributions, the dynamical nature of genetic variance, the potential for disruptive selection due to ecological feedbacks, and the non‐normal or skewed trait distributions encountered in nature. Oligomorphic dynamics explicitly takes into account the effect of environmental feedback, such as frequency‐ and density‐dependent selection, on the dynamics of multi‐modal trait distributions and we argue it has the potential to facilitate a much tighter integration between eco‐evolutionary theory and empirical data. 

Significance The clear need to mitigate zoonotic risk has fueled increased viral discovery in specific reservoir host taxa. We show that a combination of viral and reservoir traits can predict zoonotic virus virulence and transmissibility in humans, supporting the hypothesis that bats harbor exceptionally virulent zoonoses. However, pandemic prevention requires thinking beyond zoonotic capacity, virulence, and transmissibility to consider collective “burden” on human health. For this, viral discovery targeting specific reservoirs may be inefficient as death burden correlates with viral, not reservoir, traits, and depends on context-specific epidemiological dynamics across and beyond the human–animal interface. These findings suggest that longitudinal studies of viral dynamics in reservoir and spillover host populations may offer the most effective strategy for mitigating zoonotic risk. 

Abstract Theoretical models suggest that infectious diseases could play a substantial role in determining the spatial extent of host species, but few studies have collected the empirical data required to test this hypothesis. Pathogens that sterilize their hosts or spread through frequency‐dependent transmission could have especially strong effects on the limits of species' distributions because diseased hosts that are sterilized but not killed may continue to produce infectious stages and frequency‐dependent transmission mechanisms are effective even at very low population densities. We collected spatial pathogen prevalence data and population abundance data for alpine carnations infected by the sterilizing pathogenMicrobotryum dianthorum, a parasite that is spread through both frequency‐dependent (vector‐borne) and density‐dependent (aerial spore transmission) mechanisms. Our 13‐year study reveals rapid declines in population abundance without a compensatory decrease in pathogen prevalence. We apply a stochastic, spatial model of parasite spread that accommodates spatial habitat heterogeneity to investigate how the population dynamics depend on multimodal (frequency‐dependent and density‐dependent) transmission. We found that the observed rate of population decline could plausibly be explained by multimodal transmission, but is unlikely to be explained by either frequency‐dependent or density‐dependent mechanisms alone. Multimodal pathogen transmission rates high enough to explain the observed decline predicted that eventual local extinction of the host species is highly likely. Our results add to a growing body of literature showing how multimodal transmission can constrain species distributions in nature. 

Abstract How social behaviours evolve remains one of the most debated questions in evolutionary biology. An important theoretical prediction is that when organisms interact locally due to limited dispersal or strong social ties, the population structure that emerges may favour cooperation over antagonism. We carry out an experimental test of this theory by directly manipulating population spatial structure in an insect laboratory model system and measuring the impact on the evolution of the extreme selfish behaviour of cannibalism. We show that, as predicted by the theory, Indian meal moth larvae that evolved in environments with more limited dispersal are selected for lower rates of cannibalism. This is important because it demonstrates that local interactions select against selfish behaviour. Therefore, the ubiquitous variation in population structure that we see in nature is a simple mechanism that can help to explain the variation in selfish and cooperative behaviours that we see in nature. 

Bee declines have been partly attributed to the impacts of invasive or emerging parasite outbreaks. For western honeybees,Apis mellifera, major losses are associated with the virus-vectoring mite,Varroa destructor. In response, beekeepers have focused breeding efforts aimed at conferring resistance to this key parasite. One method of many is survival-based beekeeping where colonies that survive despite significantVarroainfestations produce subsequent colonies. We argue that this ‘hands-off’ approach will not always lead toVarroaresistance evolving but rather tolerance. Tolerance minimizes host fitness costs of parasitism without reducing parasite abundance, whereas resistance either prevents parasitism outright or keeps parasitism intensity low. With clear epidemiological distinctions, and as honeybee disease dynamics impact other wild bees owing to shared pathogens, we discuss why tolerance outcomes in honeybee breeding have important implications for wider pollinator health. Crucially, we argue that unintentional selection for tolerance will not only lead to more spillover from honeybees but may also select for pathogens that are more virulent in wild bees leading to ‘tragedies of tolerance’. These tragedies can be avoided through successful breeding regimes that specifically select for lowVarroa. We emphasize how insights from evolutionary ecology can be applied in ecologically responsible honeybee management. 

COVID-19 infections have underlined that there can be substantial impacts on health after recovery, including elevated mortality. While such post-infection mortality (PIM) is clearly widespread, we do not yet have any understanding of its evolutionary dynamics. To address this gap, we use an eco-evolutionary model to determine conditions where PIM is evolutionarily favoured. Importantly, from a pathogen perspective, there are two potential ‘resources’: never-infected susceptibles and previously infected susceptibles (provided some reinfection is possible), and PIM only occurs in the latter. A key insight is that unlike classic virulence (i.e. during-infection mortality, DIM) PIM is neutral and not selected against in the absence of other trade-offs. However, PIM modulates characteristics of endemicity, and may also vary with other pathogen-specific components. If PIM is only correlated with transmission, recovery or DIM, it simply acts to modulate their impacts on the evolutionary outcome. On the other hand, if PIM trades off with the relative susceptibility to reinfection, there are important evolutionary implications that contrast with DIM. We find settings where a susceptibility–mortality trade-off (i.e. an increase in mortality leads to higher relative susceptibility to reinfection) can select against DIM but favour PIM. This provides a potential explanation for the ubiquity of PIM. Overall, our work illustrates that PIM can readily evolve in certain settings and highlights the importance of considering different sources of mortality.