Biological rhythms are thought to have evolved to enable organisms to organise their activities according to the Earth’s predictable cycles, but quantifying the fitness advantages of rhythms is challenging and data revealing their costs and benefits are scarce. More difficult still is explaining why parasites that exclusively live within the bodies of other organisms have biological rhythms. Rhythms exist in the development and traits of parasites, in host immune responses, and in disease susceptibility. This raises the possibility that timing matters for how hosts and parasites interact and, consequently, for the severity and transmission of diseases. Despite their obvious importance in other fields, circadian rhythms are a neglected aspect of ecology and evolutionary biology. The ambitions of this thesis are to integrate chronobiology, parasitology and evolutionary theory with mathematical models to obtain a greater understanding about how and suggest why malaria parasites have rhythms as well as the effect of infection on host rhythms. First, I identify how malaria parasites lose their developmental rhythms in culture, when they lack any potential time cues from the host. Next, I characterise parasite rhythms inside the mammalian host in terms of synchrony and timing and demonstrate there is genotype by environment interactions for characteristics of parasite rhythms. Then, I investigate the effect that parasite infection has on host rhythms and show there is variation between parasite genotypes in their effect on host locomotor activity and body temperature rhythms during infections. Finally, I explore which host rhythms may be driving parasite synchrony and timing and demonstrate the importance of peripheral host rhythms for the timing of malaria parasite developmental rhythms. The data presented here provides novel and important information on the role of rhythms during disease and opens up a new arena for studying host-parasite coevolution.

Virtually all interacting species (such as hosts and parasites) are embedded within diverse communities. However, evolutionary interactions are typically considered in a pairwise species framework. Although coevolutionary theory suggests that multiple species interactions may provide greater opportunities for diversification, the impacts of community diversity on coevolution have not been directly tested. In this thesis I synthesize the findings from recent experimental work to assess the effects of increased species diversity on the patterns and processes of host and parasite evolution. I then investigate the effects of parasite diversity on host-parasite population dynamics and evolution using the pathogen Pseudomonas aeruginosa and five lytic bacteriophage parasites in a brief evolution experiment. Parasite diversity was manipulated by assembling phage communities with different number of species. Phage communities suppressed host populations more rapidly but also showed reduced phage density, likely due to inter-phage competition. The evolution of resistance allowed rapid bacterial recovery that was greater in magnitude with increases in phage diversity. These results were then followed up via longer term experimental coevolution of the same host and parasite communities. Here the data showed that greater parasite diversity accelerates coevolutionary arms races and drives more diversification among lineages. Coevolution between hosts and parasite communities drove more successive increases in host resistance coupled with increasingly frequent selective sweeps at the genomic level. Consistent with this, the most rapidly evolving host genes under coevolution with parasite communities were those involved in various host resistance strategies. These results demonstrate, at phenotypic and genomic levels, how areas of high community diversity may be hotspots for rapid evolution in interacting, antagonistic species. Finally, In the face of escalating antibiotic resistance, there is now an urgent need to develop alternative antimicrobials, these results may be relevant to the application of phages as therapeutics and they are discussed in that context.

Many bacteria, viruses and other parasites cause severe morbidity or mortality in their host populations, creating strong selection for physiological or behavioural mechanisms to avoid disease. Likewise, changes in host susceptibility and contact patterns can dramatically influence the spread of infectious diseases, and hence selection for traits such as virulence and infectivity range in parasites. Understanding how ecological and evolutionary changes in one population affect selection in another represents a key challenge for theoreticians and empiricists alike, and is essential for gaining further insights into host-parasite relationships. This thesis contains theoretical models that explore how genetic and environmental factors shape the evolutionary and coevolutionary dynamics of hosts and parasites. In particular, the roles of genetic specificity (i.e. genotype-by-genotype interactions) and population mixing patterns are investigated, using both mathematical models and computer simulations. A broad range of scenarios are covered, including the coevolution of broad resistance and infectivity ranges (generalism), the persistence of coevolutionary cycling and the maintenance of sex, the effects of mating behaviour on disease prevalence and evolution, and the evolution of sexual and social behaviour. The models presented herein develop our understanding of host-parasite relationships and highlight the importance of genetic interactions and ecological feedbacks.

Le degré de spécialisation d'hôte des parasites peut considérablement modifier la nature des interactions interspécifiques. Lorsque les parasites sont également vecteurs, leur capacité d'adaptation et leur réponse aux changements dans la communauté d'hôtes aura des conséquences importantes sur la dynamique de leurs populations, mais aussi sur les microparasites qu'ils transmettent. Une première étape pour mieux appréhender l'importance de ce phénomène sur l'écologie et l'évolution des systèmes vectoriels est d'étudier la divergence génétique associée à l'hôte. Nous avons utilisé cette approche dans le système hôte-vecteur-pathogène impliquant la tique européenne Ixodes ricinus, ses différents hôtes vertébrés et les bactéries responsables de la maladie de Lyme (Borrelia burgdorferi sl). Ce travail a notamment consisté à tester si les communautés les plus anciennes montraient des divergences associées à l'hôte plus importantes que celles récemment colonisées. Nous avons combiné des échantillonnages de terrain sur un transect européen (comprenant la distribution historique d'I. ricinus et des zones nouvellement colonisées) et, des analyses moléculaires basés sur 14 marqueurs microsatellites (dont 9 nouvellement développés). Comme un obstacle majeur pour aborder la question de la spécificité d'hôte dans le système I. ricinus, ainsi que chez d'autres vecteurs, est de déterminer l'utilisation des hôtes, nous avons également testé expérimentalement les biais rencontrés lors de la détection moléculaire de l'hôte. Nos résultats révèlent un schéma complexe de l'adaptation des tiques à travers l'Europe ; la spécialisation d'hôte peut évoluer, mais l'âge de la communauté ne semble pas être un facteur décisif. Plus généralement, les résultats de cette thèse soulignent que l'écologie des vecteurs en eux-mêmes (et pas seulement les interactions hôtes-pathogènes) doit être considérée avec attention si on veut améliorer notre compréhension de ces systèmes. / The degree of host specialization in parasites can greatly modify the nature of interspecific interactions. When parasites are also vectors, their ability to adapt to new hosts and their response to changes in the host community will have important consequences for both their population dynamics and evolution, but may also cascade down to the microparasites they transmit. A first step to better apprehend the importance of this phenomenon for the evolution and ecology of vector-borne disease systems is to study patterns of host-associated genetic divergence across diverse vector populations. We used this approach in the host-vector-pathogen system involving the European tick Ixodes ricinus, its various vertebrate hosts and the bacteria responsible for Lyme disease Borrelia burgdorferi sl. We predicted that longer established interactions would show stronger patterns of host-associated divergence than more recently established ones. We tested this prediction by combining field samples from a European-wide transect (including both historical and newly colonized zones) and molecular analyses based on 14 microsatellite markers (9 newly developed). As a major obstacle for tackling the question of host associations in the I. ricinus system is determining local host use, we also experimentally tested for biases in molecular host detection. Our results reveal a complex pattern of tick adaptation across the European landscape; host specialization does evolve, but not in a predictable way in relation to the evolutionary age of the interaction. More generally, the results of this thesis highlight that vector ecology (and not just host-pathogen interactions) require careful consideration, if we are to improve our understanding of these systems.