Life history and mating systems select for male biased parasitism mediated through natural selection and ecological feedbacks

Males are often the "sicker" sex with male biased parasitism found in a taxonomically diverse range of species. There is considerable interest in the processes that could underlie the evolution of sex-biased parasitism. Mating system differences along with differences in lifespan may play a key role. We examine whether these factors are likely to lead to male-biased parasitism through natural selection taking into account the critical role that ecological feedbacks play in the evolution of defence. We use a host-parasite model with two-sexes and the techniques of adaptive dynamics to investigate how mating system and sexual differences in competitive ability and longevity can select for a bias in the rates of parasitism. Male-biased parasitism is selected for when males have a shorter average lifespan or when males are subject to greater competition for resources. Male-biased parasitism evolves as a consequence of sexual differences in life history that produce a greater proportion of susceptible females than males and therefore reduce the cost of avoiding parasitism in males. Different mating systems such as monogamy, polygamy or polyandry did not produce a bias in parasitism through these ecological feedbacks but may accentuate an existing bias.Comment: 18 pages, 4 figure

Multi-mode fluctuating selection in host-parasite coevolution

Understanding fluctuating selection is important for our understanding of patterns of spatial and temporal diversity in nature. Host-parasite theory has classically assumed fluctuations either occur between highly specific genotypes (Matching Alleles: MA) or from specialism to generalism (Gene-for-Gene: GFG). However, while MA can only generate one mode of fluctuating selection, we show that GFG can in fact produce both rapid “within-range” fluctuations (among genotypes with identical levels of investment but which specialise on different subsets of the population) and slower cycling “between ranges” (different levels of investment), emphasising that MA is a subset of GFG. Our findings closely match empirical observations, although sampling rates need to be high to detect these novel dynamics empirically. Within-range cycling is an overlooked process by which fluctuating selection can occur in nature, suggesting that fluctuating selection may be a more common and important process than previously thought in generating and maintaining diversity

Spatial heterogeneity in ecology

This project predominantly investigated the implications of spatial heterogeneity in the ecological processes of competition and infection. Empirical analysis of spatial heterogeneity was carried out using the lepidopteran species Plodia interpunctella. Using differently viscous food media, it was possible to alter the movement rate of larvae. Soft Foods allow the movement rate of larvae to be high, so that individuals can disperse through the environment and avoid physical encounters with conspecifics. Harder foods lower the movement rate of larvae, restricting the ability of individuals to disperse away from birth sites and avoid conspecifics encounters. Increasing food viscosity and lowering movement rate therefore has the effect of making uniform distributed larval populations more aggregated and patchy. Different spatial structures changed the nature of intraspecific competition, with patchy populations characterised by individuals experiencing lower growth rates and greater mortality because of the reduced food and space available within densely packed aggregations. At the population scale, the increased competition for food individuals experience in aggregations emerges as longer generational cycles and reduced population densities. Aggregating individuals also altered the outcome of interspecific competition between Plodia and Ephestia cautella. In food media that allowed high movement rates, Plodia had a greater survival rate than Ephestia because the larger movement rate of Plodia allowed it to more effectively avoid intraspecific competition. Also the faster growth rate, and so larger size, of Plodia allowed it to dominate interspecific encounters by either predating or interfering with the feeding of Ephestia. In food that restricts movement, the resulting aggregations cause Plodia to experience more intraspecific encounters relative to interspecific, reducing its competitive advantage and levelling the survival of the two species. Spatial structure also affected the dynamics of a Plodia-granulosis virus interaction and the evolution of virus infectivity. Larval aggregation forced transmission to become limited to within host patches, making the overall prevalence of the virus low. However potentially high rates of cannibalism and multiple infections within overcrowded host aggregations caused virus-induced mortality to be high, as indicated by the low host population density when virus is presented. Also aggregated host populations cause the evolution of lower virus infectivity, where less infective virus strains maintain more susceptible hosts within the aggregation and so possess a greater transmission rate. The pattern of variation in resistance of Plodia interpunctella towards its granulosis virus was found using two forms of graphical analysis. There was a bimodal pattern of variation, with most individuals exhibiting either low or high levels of resistance. This pattern was related to a resistance mechanism that is decreasingly costly to host fitness.EThOS - Electronic Theses Online ServiceGBUnited Kingdo

Understanding the role of eco-evolutionary feedbacks in host-parasite coevolution

It is widely recognised that eco-evolutionary feedbacks can have important implications for evolution. However, many models of host-parasite coevolution omit eco-evolutionary feedbacks for the sake of simplicity, typically by assuming the population sizes of both species are constant. It is often difficult to determine whether the results of these models are qualitatively robust if eco-evolutionary feedbacks are included. Here, by allowing interspecific encounter probabilities to depend on population densities without otherwise varying the structure of the models, we provide a simple method that can test whether eco-evolutionary feedbacks per se affect evolutionary outcomes. Applying this approach to explicit genetic and quantitative trait models from the literature, our framework shows that qualitative changes to the outcome can be directly attributable to eco-evolutionary feedbacks. For example, shifting the dynamics between stable monomorphism or polymorphism and cycling, as well as changing the nature of the cycles. Our approach, which can be readily applied to many different models of host-parasite coevolution, offers a straightforward method for testing whether eco-evolutionary feedbacks qualitatively change coevolutionary outcomes.</p

Spatially structured eco-evolutionary dynamics in a host-pathogen interaction render isolated populations vulnerable to disease

While the negative effects that pathogens have on their hosts are well-documented in humans and agricultural systems, direct evidence of pathogen-driven impacts in wild host populations is scarce and mixed. Here, to determine how the strength of pathogen-imposed selection depends on spatial structure, we analyze growth rates across approximately 4000 host populations of a perennial plant through time coupled with data on pathogen presence-absence. We find that infection decreases growth more in the isolated than well-connected host populations. Our inoculation study reveals isolated populations to be highly susceptible to disease while connected host populations support the highest levels of resistance diversity, regardless of their disease history. A spatial eco-evolutionary model predicts that non-linearity in the costs to resistance may be critical in determining this pattern. Overall, evolutionary feedbacks define the ecological impacts of disease in spatially structured systems with host gene flow being more important than disease history in determining the outcome

Spatially structured eco-evolutionary dynamics in a host-pathogen interaction render isolated populations vulnerable to disease

While the negative effects that pathogens have on their hosts are well-documented in humans and agricultural systems, direct evidence of pathogen-driven impacts in wild host populations is scarce and mixed. Here, to determine how the strength of pathogen-imposed selection depends on spatial structure, we analyze growth rates across approximately 4000 host populations of a perennial plant through time coupled with data on pathogen presence-absence. We find that infection decreases growth more in the isolated than well-connected host populations. Our inoculation study reveals isolated populations to be highly susceptible to disease while connected host populations support the highest levels of resistance diversity, regardless of their disease history. A spatial eco-evolutionary model predicts that non-linearity in the costs to resistance may be critical in determining this pattern. Overall, evolutionary feedbacks define the ecological impacts of disease in spatially structured systems with host gene flow being more important than disease history in determining the outcome.Peer reviewe

Modelling disease spread in real landscapes: Squirrelpox spread in southern Scotland as a case study

PublishedJournal ArticleThis is the author accepted manuscript. The final version is available from Associazione Teriologica Italiana via the DOI in this record.© 2016 Associazione Teriologica Italiana.There is increasing evidence that invading species can gain an advantage over native species by introducing novel disease. A clear understanding of the role of disease in the expansion of introduced and invading species is therefore essential for the conservation of native species. In this study we focus on the case study system of the UK red and grey squirrel system in which disease-mediated competition has facilitated the replacement of red squirrels by greys. We modify a deterministic model of the squirrel system in which the competition and infection dynamics are well understood to produce a stochastic model which includes a realistic representation of the heterogeneous habitat in Southern Scotland. The model is used to examine the potential spread of infection (squirrelpox virus) through the squirrel system and to examine the impact of conservation measures that control grey squirrel numbers in an attempt to contain disease spread. The results have direct implications for conservation management and we discuss how they have helped shape current and future policy for red squirrel conservation in Scotland. The methods in this study can be readily adapted to represent different systems and since the stochastic population and disease dynamics are underpinned by classical deterministic modelling frameworks the results are applicable in general.AW and PL were supported in part by SNH. AW, MB and PL were supported in part by a NERC Innovations grant NE/M021319/1

Modelling the impact of forest design plans on an endangered mammal species: The eurasian red squirrel

PublishedJournal ArticleThis is the author accepted manuscript. The final version is available from Associazione Teriologica Italiana via the DOI in this record.© 2016 Associazione Teriologica Italiana.The Eurasian red squirrel (Sciurus vulgaris) is under threat in the UK from the introduced North American grey squirrel. National measures to save the species include large conifer forest reserves where management encompasses measures to bolster the native species. However, forests are multipurpose environments and foresters have to balance different timber production, amenity and conservation objectives. We present a mathematical modelling framework that examines the impacts of potential felling and restocking plans for two reserves, Kidland and Uswayford forests, in northern England. In collaboration with forest managers, we employed an iterative process that used the model to assess four forest design plans (felling and restocking scenarios) with the aim of improving red squirrel population viability. Overall, the model predicted that extinction in both forests at the same time was rare, but high in Uswayford (84%) alone. Survival could be drastically increased (from 16% to 70%) by felling and restocking adjustments, and improving dispersal between the two adjacent forests. This study provides an exemplar of how modelling can have a direct input to land management to help managers objectively balance the differing pressures of multipurpose forestry.AW, MB and PL are supported in part by a NERC Innovations grant NE/M021319/1

The importance of aggregation in the dynamics of host-parasite interaction in wildlife : a mathematical approach

This study examines, from a modelling point of view, the dynamics of infectious diseases in wildlife caused by macroparasites and by tick-borne infections. The overall aim was to investigate the important role played by parasite aggregation in the dynamics of both systems. For macroparasites we first developed some deterministic models that incorporate explicit mechanisms for generating aggregation in parasite distribution, specifically multiple infections and host heterogeneity. We explored the role of aggregation in host regulation and in determining a threshold value for parasite establishment. A large aggregation makes it more difficult for parasites both to regulate hosts, and to get established in a population at carrying capacity. Furthermore, the stabilization yielded by aggregation strongly depends on the mechanism that produces the aggregation. We then introduced some uncertainties into the host-macroparasite system, presenting an individual-based stochastic model that incorporated the same assumptions as the deterministic model. Stochastic simulations, using parameter values based on some real case studies, preserved many features of the deterministic model, like the average value of the variables and the approximate length of the cycles. An important difference is that, even when deterministic models yield damped oscillations, stochastic simulations yield apparently sustained oscillations. The amplitude of such oscillations may be so large as to threaten the parasites’ persistence. With respect to tick-borne diseases we presented a general model framework that incorporated both viraemic and non-viraemic routes of infections. We compute the threshold for disease persistence and study its dependence on the parameters and on host densities. The effects of tick aggregation and correlation between different tick stages on the host have both an important effect on infection persistence, if non-viraemic transmission occurred. In the case of Lyme Disease and Tick-borne Encephalitis (TBE) in Trentino (northern Italy) we showed some numerical results, using parameter estimates based on a detailed field study, and explored the effects of uncertainty on the endemic equilibrium of both diseases assuming only viraemic transmission for Lyme Disease while for TBE we permitted only non-viraemic transmission through co-feeding ticks. In conclusion we have examined the patterns and changes of aggregation in a number of contrasting systems and believe that these studies highlight both the importance of considering heterogeneities in modelling host-parasite interactions and, more specifically, modelling the biological mechanisms that produce aggregation in parasite distributions.EThOS - Electronic Theses Online ServiceProvincia Autonoma di Trento under Grant n. 1060 ECODISGBUnited Kingdo