Evolutionary consequences of feedbacks between within-host competition and disease control

Lay Summary: Competition often occurs among diverse parasites within a single host, but control efforts could change its strength. We examined how the interplay between competition and control could shape the evolution of parasite traits like drug resistance and disease severity

Host Sexual Dimorphism and Parasite Adaptation

Disease expression and prevalence often vary in the different sexes of the host. This is typically attributed to innate differences of the two sexes but specific adaptations by the parasite to one or other host sex may also contribute to these observations

Varying Herbivore Population Structure Correlates with Lack of Local Adaptation in a Geographic Variable Plant-Herbivore Interaction

Local adaptation of parasites to their hosts due to coevolution is a central prediction of many theories in evolutionary biology. However, empirical studies looking for parasite local adaptation show great variation in outcomes, and the reasons for such variation are largely unknown. In a previous study, we showed adaptive differentiation in the arctiid moth Utetheisa ornatrix to its host plant, the pyrrolizidine alkaloid-bearing legume Crotalaria pallida, at the continental scale, but found no differentiation at the regional scale. In the present study, we sampled the same sites to investigate factors that may contribute to the lack of differentiation at the regional scale. We performed field observations that show that specialist and non-specialist polyphagous herbivore incidence varies among populations at both scales. With a series of common-garden experiments we show that some plant traits that may affect herbivory (pyrrolizidine alkaloids and extrafloral nectaries) vary at the regional scale, while other traits (trichomes and nitrogen content) just vary at the continental scale. These results, combined with our previous evidence for plant population differentiation based on larval performance on fresh fruits, suggest that U. ornatrix is subjected to divergent selection even at the regional scale. Finally, with a microsatellite study we investigated population structure of U. ornatrix. We found that population structure is not stable over time: we found population differentiation at the regional scale in the first year of sampling, but not in the second year. Unstable population structure of the herbivore is the most likely cause of the lack of regional adaptation

The evolutionary ecology of complex lifecycle parasites: linking phenomena with mechanisms

Many parasitic infections, including those of humans, are caused by complex lifecycle parasites (CLPs): parasites that sequentially infect different hosts over the course of their lifecycle. CLPs come from a wide range of taxonomic groups-from single-celled bacteria to multicellular flatworms-yet share many common features in their life histories. Theory tells us when CLPs should be favoured by selection, but more empirical studies are required in order to quantify the costs and benefits of having a complex lifecycle, especially in parasites that facultatively vary their lifecycle complexity. In this article, we identify ecological conditions that favour CLPs over their simple lifecycle counterparts and highlight how a complex lifecycle can alter transmission rate and trade-offs between growth and reproduction. We show that CLPs participate in dynamic host-parasite coevolution, as more mobile hosts can fuel CLP adaptation to less mobile hosts. Then, we argue that a more general understanding of the evolutionary ecology of CLPs is essential for the development of effective frameworks to manage the many diseases they cause. More research is needed identifying the genetics of infection mechanisms used by CLPs, particularly into the role of gene duplication and neofunctionalisation in lifecycle evolution. We propose that testing for signatures of selection in infection genes will reveal much about how and when complex lifecycles evolved, and will help quantify complex patterns of coevolution between CLPs and their various hosts. Finally, we emphasise four key areas where new research approaches will provide fertile opportunities to advance this field

Associations between Season and Gametocyte Dynamics in Chronic Plasmodium falciparum Infections

Introduction: In a markedly seasonal malaria setting, the transition from the transmission-free dry season to the transmission season depends on the resurgence of the mosquito population following the start of annual rains. The sudden onset of malaria outbreaks at the start of the transmission season suggests that parasites persist during the dry season and respond to either the reappearance of vectors, or correlated events, by increasing the production of transmission stages. Here, we investigate whether Plasmodium falciparum gametocyte density and the correlation between gametocyte density and parasite density show seasonal variation in chronic (largely asymptomatic) carriers in eastern Sudan. Materials and Methods: We recruited and treated 123 malaria patients in the transmission season 2001. We then followed them monthly during four distinct consecutive epidemiological seasons: transmission season 1, transmission-free season, pre-clinical period, and transmission season 2. In samples collected from 25 participants who fulfilled the selection criteria of the current analysis, we used quantitative PCR (qPCR) and RT-qPCR to quantify parasite and gametocyte densities, respectively. Results and Discussion: We observed a significant increase in gametocyte density and a significantly steeper positive correlation between gametocyte density and total parasite density during the pre-clinical period compared to the preceding transmission-free season. However, there was no corresponding increase in the density or prevalence of total parasites or gametocyte prevalence. The increase in gametocyte production during the pre-clinical period supports the hypothesis that P. falciparum may respond to environmental cues, such as mosquito biting, to modulate its transmission strategy. Thus, seasonal changes may be important to ignite transmission in unstable-malaria settings

Avoidance of host resistance in the oviposition-site preferences of rose bitterling

A contemporary outcome of dynamic host–parasite coevolution can be driven by the adaptation of a parasite to exploit its hosts at the population and species levels (parasite specialisation) or by local host adaptations leading to greater host resistance to sympatric parasite populations (host resistance). We tested the predominance of these two scenarios using cross-infection experiments with two geographically distant populations of the rose bitterling, Rhodeus ocellatus, a fish brood parasite of freshwater mussels, and four populations of their mussel hosts (two Anodonta woodiana and two Unio douglasiae populations) with varying degrees of geographic sympatry and local coexistence. Our data support predictions for host resistance at the species level but no effect of local coexistence between specific populations. Rhodeus ocellatus showed a preference for allopatric host populations, irrespective of host species. Host mussel response, in terms of ejection of R. ocellatus eggs, was stronger in the more widespread and abundant host species (A. woodiana) and this response tended to be higher in sympatric populations. These outcomes provide support for the importance of host resistance in bitterling oviposition-site decisions, demonstrating that host choice by R. ocellatus is adaptive by minimizing egg ejections. These findings imply that R. ocellatus, and potentially other bitterling species, may benefit from exploiting novel hosts, which may not possess appropriate adaptive responses to parasitism

Rethinking the extrinsic incubation period of malaria parasites

The time it takes for malaria parasites to develop within a mosquito, and become transmissible, is known as the extrinsic incubation period, or EIP. EIP is a key parameter influencing transmission intensity as it combines with mosquito mortality rate and competence to determine the number of mosquitoes that ultimately become infectious. In spite of its epidemiological significance, data on EIP are scant. Current approaches to estimate EIP are largely based on temperature-dependent models developed from data collected on parasite development within a single mosquito species in the 1930s. These models assume that the only factor affecting EIP is mean environmental temperature. Here, we review evidence to suggest that in addition to mean temperature, EIP is likely influenced by genetic diversity of the vector, diversity of the parasite, and variation in a range of biotic and abiotic factors that affect mosquito condition. We further demonstrate that the classic approach of measuring EIP as the time at which mosquitoes first become infectious likely misrepresents EIP for a mosquito population. We argue for a better understanding of EIP to improve models of transmission, refine predictions of the possible impacts of climate change, and determine the potential evolutionary responses of malaria parasites to current and future mosquito control tools

Variability of dense water formation in the Ross Sea

The paper presents results from a model study of the interannual variability of High Salinity Shelf Water (HSSW) properties in the Ross Sea.Salinity, potential temperature and volume of HSSW formed in the western Ross Sea show oscillatory behaviour at periods of 5-6 and 9 years superimposed on long-term fluctuations.While the shorter oscillations are induced by wind variability, variability on the scale of decades appears to be related to air temperature fluctuations.At least part of the strong decrease of HSSW salinities deduced from observations for the period 1963-2000 is shown to be an aliasing artefact due to an undersampling of the periodic signal.While sea ice formation is responsible for the yearly salinity increase that triggers the formation of High Salinity Shelf Water, interannual variability of net freezing rates hardly affects changes in the properties of the resulting water mass.Instead, results from model experiments indicate that the interannual variability of dense water characteristics is predominantly controlled by variations in the shelf inflow through a sub-surface salinity and a deep temperature signal.The origin of the variability of inflow characteristics to the Ross Sea continental shelf can be traced into the Amundsen and Bellingshausen Seas.The temperature anomalies are induced at the continental shelf break in the western Bellingshausen Sea by fluctuations of the meridional transport of Circumpolar Deep Water with the eastern cell of the Ross Gyre.Upwelling in the centre of this gyre carries the signal into the surface layer where it causes anomalies of brine release near the sea ice edge in the Amundsen Sea, which results in a sub-surface salinity anomaly.With the westward flowing coastal current, both the sub-surface salinity and deep temperature signals are advected onto the Ross Sea continental shelf.Convection carries the signal of salinity variability into the deep ocean, where it interacts with Modified Circumpolar Deep Water upwelled onto the continental shelf as the second source water mass of HSSW.Sea ice formation on the Ross Sea continental shelf thus drives the vertical propagation of the signal rather than determining the signal itself