Peter H. Thrall

SEXUALLY TRANSMITTED DISEASES IN ANIMALS: ECOLOGICAL AND EVOLUTIONARY IMPLICATIONS

Sexually transmitted diseases (STDs) have been generally thought of as a small subset of infectious diseases, rather than as an important group of diseases that occur in numerous species. In this paper, we have (1) briefly reviewed theoretical studies on the dynamics of STDs; (2) documented the distribution of STDs in the animal kingdom; and (3) investigated whether STDs have characteristics which distinguish them from other infectious diseases. The dynamics of STDs should differ from those of ordinary infectious diseases because their transmission depends on the frequency rather than density of infectives. With this type of transmission, there is no threshold density for disease spread, and the conditions for host-pathogen coexistence are more restrictive. Nevertheless, a wide variety of disease characteristics may allow a sexually transmitted pathogen to coexist with its host. We found over 200 diseases for which there was evidence of sexual transmission. They occurred in groups as diverse as mammals, reptiles, arachnids, insects, molluscs and nematodes. Sexually transmitted pathogens included protozoans, fungi, nematodes, helminths, and cancerous cell lines, as well as bacteria and viruses. Detailed comparison of the characteristics of sexually transmitted mammalian diseases with those that are transmitted by non-sexual means, showed that STDs cause less mortality, are longer-lived in their hosts, are less likely to invoke strong immune responses, have narrower host-ranges, and show less fluctuation in prevalence over time. These shared features are related to mode of transmission rather than either host or pathogen taxonomic affiliation. This suggests an evolutionary explanation based on shared ecologies rather than one based on phylogenetic history.

Life history determines genetic structure and evolutionary potential of host–parasite interactions

Measures of population genetic structure and diversity of disease-causing organisms are commonly used to draw inferences regarding their evolutionary history and potential to generate new variation in traits that determine interactions with their hosts. Parasite species exhibit a range of population structures and life-history strategies, including different transmission modes, life-cycle complexity, off-host survival mechanisms and dispersal ability. These are important determinants of the frequency and predictability of interactions with host species. Yet the complex causal relationships between spatial structure, life history and the evolutionary dynamics of parasite populations are not well understood. We demonstrate that a clear picture of the evolutionary potential of parasitic organisms and their demographic and evolutionary histories can only come from understanding the role of life history and spatial structure in influencing population dynamics and epidemiological patterns.

LOCAL ADAPTATION IN THE LINUM MARGINALE–MELAMPSORA LINI HOST-PATHOGEN INTERACTION

Abstract The potential for local adaptation between pathogens and their hosts has generated strong theoretical and empirical interest with evidence both for and against local adaptation reported for a range of systems. We use the Linum marginale—Melampsora lini plant‐pathogen system and a hierarchical spatial structure to investigate patterns of local adaptation within a metapopulation characterised by epidemic dynamics and frequent extinction of pathogen populations. Based on large sample sizes and comprehensive cross‐inoculation trials, our analyses demonstrate strong local adaptation by Melampsora to its host populations, with this effect being greatest at regional scales, as predicted from the broader spatial scales at which M. lini disperses relative to L. marginale. However, there was no consistent trend for more distant pathogen populations to perform more poorly. Our results further show how the coevolutionary interaction between hosts and pathogens can be influenced by local structure such that resistant hosts select for generally virulent pathogens, while susceptible hosts select for more avirulent pathogens. Empirically, local adaptation has generally been tested in two contrasting ways: (1) pathogen performance on sympatric versus allopatric hosts; and (2) sympatric versus allopatric pathogens on a given host population. In situations where no host population is more resistant or susceptible than others when averaged across pathogen populations (and likewise, no pathogen population is more virulent or avirulent than others), results from these tests should generally be congruent. We argue that this is unlikely to be the case in the metapopulation situations that predominate in natural host‐pathogen interactions, thus requiring tests that control simultaneously for variation in plant and pathogen populations.

A conceptual framework for the evolution of ecological specialisation

Ecology Letters (2011) 14: 841-851 ABSTRACT: Ecological specialisation concerns all species and underlies many major ecological and evolutionary patterns. Yet its status as a unifying concept is not always appreciated because of its similarity to concepts of the niche, the many levels of biological phenomena to which it applies, and the complexity of the mechanisms influencing it. The evolution of specialisation requires the coupling of constraints on adaptive evolution with covariation of genotype and environmental performance. This covariation itself depends upon organismal properties such as dispersal behaviour and life history and complexity in the environment stemming from factors such as species interactions and spatio-temporal heterogeneity in resources. Here, we develop a view on specialisation that integrates across the range of biological phenomena with the goal of developing a more predictive conceptual framework that specifically accounts for the importance of biotic complexity and coevolutionary events.

The Cost of Resistance and the Maintenance of Genetic Polymorphism in Host-Pathogen Systems

By using models which incorporate both numerical and gene-frequency dynamics, we investigate the conditions for a stable polymorphism in host disease resistance when there is a genetically uniform pathogen. We show that polymorphism is more likely when the difference in resistance conferred by alternative alleles is large rather than small. This conforms with the frequent observation of major gene effects on resistance. Moreover, when allelic differences in resistance are large, polymorphism is possible over a wide range of costs, including situations where costs approach values close to zero. The actual resistance cost that can be sustained in such polymorphic populations is dependent on the transmission mode and the intensity of disease-independent population regulation. Expectations regarding resistance costs in any particular host—pathogen system will be dependent on knowledge of the epidemiological and genetic characteristics of that system.

Host-pathogen dynamics in a metapopulation context:the ecological and evolutionary consequences of being spatial

1 The metapopulation concept is useful when considering ecological and evolutionary dynamics of spatially structured populations. However, debate has focused on genetic variation that is neutral rather than under selection. This distinction is particularly important in antagonistic or co-evolutionary interactions such as host-pathogen or predator-prey systems. Plant host-pathogen systems provide some of the best examples of studies in which numerical and genetic dynamics have been investigated in a spatially explicit context, and where genes under selection can be unambiguously identified. 2 Empirical studies of natural host-pathogen interactions have shown that, while in some cases pathogens appear to be locally adapted to their hosts, in others there is no local correspondence between resistance and virulence genes. Recent theory suggests that the dynamics (epidemic vs. endemic) and migration rates of host and pathogen will be important factors in the maintenance of genetic polymorphisms in resistance and virulence. 3 We argue that the relative spatial scales at which hosts and pathogens interact are crucial to understanding the evolution of resistance/virulence structure. Pathogens that disperse further than their hosts will be more likely to show gene-for-gene interactions than pathogens dispersing over spatial scales similar to or smaller than their hosts. 4 We predict that life-history features that influence encounter rates between specific host and pathogen genotypes will be important factors in determining the evolution of resistance-virulence structures. In particular, we would expect correlative and/or causal relationships between pathogen life-history features [e.g. local vs. systemic infection, type (fecundity vs. mortality) and severity of effects], and whether dynamics are endemic or epidemic. 5 Plant host-pathogen systems provide ideal models for investigating the evolution of non-neutral genetic variation in spatial systems. Understanding the co-evolution of such systems will require research programmes that integrate long-term descriptive and experimental studies of multiple populations, with analytical and computer simulation modelling and comparative/phylogenetic studies.

Plant life-history and disease susceptibility - the occurrence of Ustilago violacea on different species within the Caryophyllaceae

Simple models of host-pathogen systems suggest that the ranges of potential hosts for pathogens with no transmission across generations and no free-living stages are likely to be restricted to perennial species, especially longer-lived ones. Data from the empirical literature on the relationship between the presence of anther-smut diseases and host life span in the Caryophyllaceae shows that the distribution of Ustilago violacea among host species within the Caryophyllaceae is closely related to the life span of its host species (the proportion of perennial species on which anther-smuts have been reported is five times higher than the proportion of annuals). The distribution of anther-smuts is also related to host flower morphology and breeding system (...)

Sexually transmitted diseases in polygynous mating systems: prevalence and impact on reproductive success.

Studies of disease in relation to animal mating systems have focused on sexual selection and the evolution of sexual reproduction. Relatively little work has examined other aspects of ecological and evolutionary relationships between host social and sexual behaviour, and dynamics and prevalence of infectious diseases; this is particularly evident with respect to sexually transmitted diseases (STDs). Here, we use a simulation approach to investigate rates of STD spread in host mating systems ranging from permanent monogamy to serial polygyny or polyandry and complete promiscuity. The model assumes that one sex (female) is differentially attracted to the other, such that groups of varying size are formed within which mating and disease transmission occur. The results show that equilibrium disease levels are generally higher in females than males and are a function of variance in male mating success and the likelihood of a female switching groups between mating seasons. Moreover, initial rates of disease spread (determining whether an STD establishes in a population) depend on patterns of host movement between groups, variance in male mating success and host life history (e.g. mortality rates). Male reproductive success can be reduced substantially by a sterilizing STD and this reduction is greater in males that are more ‘attractive’ to females. In contrast, females that associate with more attractive males have lower absolute fitness than females associating with less attractive males. Thus, the potential for STDs to act as a constraint on directional selection processes leading to polygyny (or polyandry) is likely to depend on the details of mate choice and group dynamics.

Genetic erosion, inbreeding and reduced fitness in fragmented populations of the endangered tetraploid pea Swainsona recta.

Genetic variation and fixation coefficients were measured for 17 fragmented populations of the endangered tetraploid pea Swainsona recta ranging in size from 1 to 430 flowering plants. Allelic richness and fixation coefficient were correlated with the log population size, suggesting that reduced population size is accompanied by genetic erosion, primarily due to a loss of rare (q<0.1) alleles, and increased inbreeding. Comparative germination and growth studies of seed from five populations representing three different levels of inbreeding (low F=0.34, medium F=0.43, high F=0.57) showed a significant reduction in percentage seed germination at 2 weeks in the single high F treatment population. There were no effects on survivorship and growth beyond this up until 141 days. Results suggest that polyploidy has not prevented erosion of genetic variation at the population level, as has previously been suggested. However, the production of partial heterozygotes, e.g. AABC and AAAB, under inbreeding may be mitigating inbreeding depression assuming a partial dominance model of gene expression. Conservation effort should concentrate on populations larger than 50 sexually reproductive plants, as these appear capable of maintaining high genetic diversity and exhibit no immediate evidence of inbreeding depression, despite some elevation of the fixation coefficient.

Rapid genetic change underpins antagonistic coevolution in a natural host‐pathogen metapopulation

Antagonistic coevolution is a critical force driving the evolution of diversity, yet the selective processes underpinning reciprocal adaptive changes in nature are not well understood. Local adaptation studies demonstrate partner impacts on fitness and adaptive change, but do not directly expose genetic processes predicted by theory. Specifically, we have little knowledge of the relative importance of fluctuating selection vs. arms-race dynamics in maintaining polymorphism in natural systems where metapopulation processes predominate. We conducted cross-year epidemiological, infection and genetic studies of multiple wild host and pathogen populations in the Linum-Melampsora association. We observed asynchronous phenotypic fluctuations in resistance and infectivity among demes. Importantly, changes in allelic frequencies at pathogen infectivity loci, and in host recognition of these genetic variants, correlated with disease prevalence during natural epidemics. These data strongly support reciprocal coevolution maintaining balanced resistance and infectivity polymorphisms, and highlight the importance of characterising spatial and temporal dynamics in antagonistic interactions.