A common multi-host parasite shows genetic structuring at the host species and population levels.

Although individual parasite species commonly infect many populations across physical space as well as multiple host species, the extent to which parasites traverse physical and phylogenetic distances is unclear. Population genetic analyses of parasite populations can reveal how parasites move across space or between host species, including helping assess whether a parasite is more likely to infect a different host species in the same location or the same host species in a different location. Identifying these transmission barriers could be exploited for effective disease control. Here, we analysed population genetic structuring of the parasite Pasteuria ramosa in daphniid host species from different lakes. Outbreaks occurred most often in the common host species Daphnia dentifera and Daphnia retrocurva. The genetic distance between parasite samples tended to be smaller when samples were collected from the same lake, the same host species and closer in time. Within lakes, the parasite showed structure by host species and sampling date; within a host species, the parasite showed structure by lake and sampling date. However, despite this structuring, we found the same parasite genotype infecting closely related host species, and we sometimes found the same genotype in nearby lakes. Thus, P. ramosa experiences challenges infecting different host species and moving between populations, but doing so is possible. In addition, the structuring by sampling date indicates potential adaptation to or coevolution with host populations and supports prior findings that parasite population structure is dynamic during outbreaks.

Rapid evolution of a bacterial parasite during outbreaks in two Daphnia populations.

Myriad ecological and evolutionary factors can influence whether a particular parasite successfully transmits to a new host during a disease outbreak, with consequences for the structure and diversity of parasite populations. However, even though the diversity and evolution of parasite populations are of clear fundamental and applied importance, we have surprisingly few studies that track how genetic structure of parasites changes during naturally occurring outbreaks in non-human populations. Here, we used population genetic approaches to reveal how genotypes of a bacterial parasite, Pasteuria ramosa, change over time, focusing on how infecting P. ramosa genotypes change during the course of epidemics in Daphnia populations in two lakes. We found evidence for genetic change - and, therefore, evolution - of the parasite during outbreaks. In one lake, P. ramosa genotypes were structured by sampling date; in both lakes, genetic distance between groups of P. ramosa isolates increased with time between sampling. Diversity in parasite populations remained constant over epidemics, although one epidemic (which was large) had low genetic diversity while the other epidemic (which was small) had high genetic diversity. Our findings demonstrate that patterns of parasite evolution differ between outbreaks; future studies exploring the feedbacks among epidemic size, host diversity, and parasite genetic diversity would improve our understanding of parasite dynamics and evolution.

Virulence evolution during a naturally occurring parasite outbreak.

Virulence, the degree to which a pathogen harms its host, is an important but poorly understood aspect of host-pathogen interactions. Virulence is not static, instead depending on ecological context and potentially evolving rapidly. For instance, at the start of an epidemic, when susceptible hosts are plentiful, pathogens may evolve increased virulence if this maximizes their intrinsic growth rate. However, if host density declines during an epidemic, theory predicts evolution of reduced virulence. Although well-studied theoretically, there is still little empirical evidence for virulence evolution in epidemics, especially in natural settings with native host and pathogen species. Here, we used a combination of field observations and lab assays in the Daphnia-Pasteuria model system to look for evidence of virulence evolution in nature. We monitored a large, naturally occurring outbreak of Pasteuria ramosa in Daphnia dentifera, where infection prevalence peaked at ~ 40% of the population infected and host density declined precipitously during the outbreak. In controlled infections in the lab, lifespan and reproduction of infected hosts was lower than that of unexposed control hosts and of hosts that were exposed but not infected. We did not detect any significant changes in host resistance or parasite infectivity, nor did we find evidence for shifts in parasite virulence (quantified by host lifespan and number of clutches produced by hosts). However, over the epidemic, the parasite evolved to produce significantly fewer spores in infected hosts. While this finding was unexpected, it might reflect previously quantified tradeoffs: parasites in high mortality (e.g., high predation) environments shift from vegetative growth to spore production sooner in infections, reducing spore yield. Future studies that track evolution of parasite spore yield in more populations, and that link those changes with genetic changes and with predation rates, will yield better insight into the drivers of parasite evolution in the wild. Supplementary Information: The online version contains supplementary material available at 10.1007/s10682-022-10169-6.

Developing an empirical model for spillover and emergence: Orsay virus host range in Caenorhabditis.

A lack of tractable experimental systems in which to test hypotheses about the ecological and evolutionary drivers of disease spillover and emergence has limited our understanding of these processes. Here we introduce a promising system: Caenorhabditis hosts and Orsay virus, a positive-sense single-stranded RNA virus that naturally infects C. elegans. We assayed species across the Caenorhabditis tree and found Orsay virus susceptibility in 21 of 84 wild strains belonging to 14 of 44 species. Confirming patterns documented in other systems, we detected effects of host phylogeny on susceptibility. We then tested whether susceptible strains were capable of transmitting Orsay virus by transplanting exposed hosts and determining whether they transmitted infection to conspecifics during serial passage. We found no evidence of transmission in 10 strains (virus undetectable after passaging in all replicates), evidence of low-level transmission in 5 strains (virus lost between passage 1 and 5 in at least one replicate) and evidence of sustained transmission in 6 strains (including all three experimental C. elegans strains) in at least one replicate. Transmission was strongly associated with viral amplification in exposed populations. Variation in Orsay virus susceptibility and transmission among Caenorhabditis strains suggests that the system could be powerful for studying spillover and emergence.

Density, parasitism, and sexual reproduction are strongly correlated in lake Daphnia populations.

Many organisms can reproduce both asexually and sexually. For cyclical parthenogens, periods of asexual reproduction are punctuated by bouts of sexual reproduction, and the shift from asexual to sexual reproduction has large impacts on fitness and population dynamics. We studied populations of Daphnia dentifera to determine the amount of investment in sexual reproduction as well as the factors associated with variation in investment in sex. To do so, we tracked host density, infections by nine different parasites, and sexual reproduction in 15 lake populations of D. dentifera for 3 years. Sexual reproduction was seasonal, with male and ephippial female production beginning as early as late September and generally increasing through November. However, there was substantial variation in the prevalence of sexual individuals across populations, with some populations remaining entirely asexual throughout the study period and others shifting almost entirely to sexual females and males. We found strong relationships between density, prevalence of infection, parasite species richness, and sexual reproduction in these populations. However, strong collinearity between density, parasitism, and sexual reproduction means that further work will be required to disentangle the causal mechanisms underlying these relationships.

Genotypic variation in an ecologically important parasite is associated with host species, lake and spore size.

Genetic variation in parasites has important consequences for host­parasite interactions. Prior studies of the ecologically important parasite Metschnikowia bicuspidata have suggested low genetic variation in the species. Here, we collected M. bicuspidata from two host species (Daphnia dentifera and Ceriodaphnia dubia) and two regions (Michigan and Indiana, USA). Within a lake, outbreaks tended to occur in one host species but not the other. Using microsatellite markers, we identified six parasite genotypes grouped within three distinct clades, one of which was rare. Of the two main clades, one was generally associated with D. dentifera, with lakes in both regions containing a single genotype. The other M. bicuspidata clade was mainly associated with C. dubia, with a different genotype dominating in each region. Despite these associations, both D. dentifera- and C. dubia-associated genotypes were found infecting both hosts in lakes. However, in lab experiments, the D. dentifera-associated genotype infected both D. dentifera and C. dubia, but the C. dubia-associated genotype, which had spores that were approximately 30% smaller, did not infect D. dentifera. We hypothesize that variation in spore size might help explain patterns of cross-species transmission. Future studies exploring the causes and consequences of variation in spore size may help explain patterns of infection and the maintenance of genotypic diversity in this ecologically important system.

What the reproductive number R0 can and cannot tell us about COVID-19 dynamics.

The reproductive number R (or R0, the initial reproductive number in an immune-naïve population) has long been successfully used to predict the likelihood of pathogen invasion, to gauge the potential severity of an epidemic, and to set policy around interventions. However, often ignored complexities have generated confusion around use of the metric. This is particularly apparent with the emergent pandemic virus SARS-CoV-2, the causative agent of COVID-19. We address some misconceptions about the predictive ability of the reproductive number, focusing on how it changes over time, varies over space, and relates to epidemic size by referencing the mathematical definition of R and examples from the current pandemic. We hope that a better appreciation of the uses, nuances, and limitations of R and R0 facilitates a better understanding of epidemic spread, epidemic severity, and the effects of interventions in the context of SARS-CoV-2.

Shedding light on environmentally transmitted parasites: lighter conditions within lakes restrict epidemic size.

Parasite fitness depends on a successful journey from one host to another. For parasites that are transmitted environmentally, abiotic conditions might modulate the success of this journey. Here we evaluate how light, a key abiotic factor, influences spatiotemporal patterns of zooplankton disease where light varies seasonally, across lakes, and with depth in a lake. In an in situ experiment using those three sources of variation, we tested sensitivity of spores of two parasites to ambient light. Infectivity of both parasites was lower when exposed to ambient light in comparison to parasites exposed to otherwise similar conditions in the dark. The more sensitive parasite (the fungus, Metschnikowia) was damaged even under lower ambient light during late fall (November). With this differential sensitivity established, we evaluated links between light environment and natural outbreaks in lakes. Consistent with the incubations, epidemics of the less sensitive parasite (the bacterium, Pasteuria) started earlier in the fall (under higher ambient light), and both parasites had smaller outbreaks in more transparent lakes. Overall, light environment may impact the timing and size of disease outbreaks. Outbreaks could thus become exacerbated by human activities that darken waters, including lake browning associated with climate change and eutrophication.

Human drivers of ecological and evolutionary dynamics in emerging and disappearing infectious disease systems.

Humans have contributed to the increased frequency and severity of emerging infectious diseases, which pose a significant threat to wild and domestic species, as well as human health. This review examines major pathways by which humans influence parasitism by altering (co)evolutionary interactions between hosts and parasites on ecological timescales. There is still much to learn about these interactions, but a few well-studied cases show that humans influence disease emergence every step of the way. Human actions significantly increase dispersal of host, parasite and vector species, enabling greater frequency of infection in naive host populations and host switches. Very dense host populations resulting from urbanization and agriculture can drive the evolution of more virulent parasites and, in some cases, more resistant host populations. Human activities that reduce host genetic diversity or impose abiotic stress can impair the ability of hosts to adapt to disease threats. Further, evolutionary responses of hosts and parasites can thwart disease management and biocontrol efforts. Finally, in rare cases, humans influence evolution by eradicating an infectious disease. If we hope to fully understand the factors driving disease emergence and potentially control these epidemics we must consider the widespread influence of humans on host and parasite evolutionary trajectories.This article is part of the themed issue 'Human influences on evolution, and the ecological and societal consequences'.

Population Density, Not Host Competence, Drives Patterns of Disease in an Invaded Community.

Generalist parasites can strongly influence interactions between native and invasive species. Host competence can be used to predict how an invasive species will affect community disease dynamics; the addition of a highly competent, invasive host is predicted to increase disease. However, densities of invasive and native species can also influence the impacts of invasive species on community disease dynamics. We examined whether information on host competence alone could be used to accurately predict the effects of an invasive host on disease in native hosts. We first characterized the relative competence of an invasive species and a native host species to a native parasite. Next, we manipulated species composition in mesocosms and found that host competence results did not accurately predict community dynamics. While the invasive host was more competent than the native, the presence of the native (lower competence) host increased disease in the invasive (higher competence) host. To identify potential mechanisms driving these patterns, we analyzed a two-host, one-parasite model parameterized for our system. Our results demonstrate that patterns of disease were primarily driven by relative population densities, mediated by asymmetry in intra- and interspecific competition. Thus, information on host competence alone may not accurately predict how an invasive species will influence disease in native species.

Volatile and semivolatile compounds in gray catbird uropygial secretions vary with age and between breeding and wintering grounds.

The uropygial secretions of some bird species contain volatile and semivolatile compounds that are hypothesized to serve as chemical signals. The abundance of secretion components varies with age and season, although these effects have not been investigated in many species. We used solid-phase microextraction headspace sampling and solvent extraction coupled with gas chromatography-mass spectrometry to detect and identify volatile and semivolatile chemical compounds in uropygial secretions of gray catbirds (Dumetella carolinensis). We identified linear and branched saturated carboxylic acids from acetic (C2) through hexacosanoic (C26); linear alcohols from decanol (C10) through docosanol (C22); one aromatic aldehyde; one monounsaturated carboxylic acid; two methyl ketones; and a C28 ester. We tested for the effect of age on signal strength and found that juvenile birds produced greater amounts of volatile C4 through C7 acids and semivolatile C20 through C26 acids, although the variation among individuals was large. Adult birds displayed small concentrations and minimal individual variation among volatile compounds, but produced significantly higher levels of long-chain linear alcohols than juvenile birds. We tested for the effects of season/location by sampling adult catbirds at their Ohio breeding grounds and at their Florida wintering grounds and found that the heaviest carboxylic acids are significantly more abundant in secretions from birds sampled during winter at the Florida site, whereas methyl ketones are more abundant in birds sampled during summer on the Ohio breeding grounds. We observed no effect of sex on semivolatile compounds, but we found a significant effect of sex on levels of carboxylic acids (C4 through C7) for juvenile birds only.