Evolutionary ecology of dispersal in biodiverse spatially structured systems: what is old and what is new?

Dispersal is a well-recognized driver of ecological and evolutionary dynamics, and simultaneously an evolving trait. Dispersal evolution has traditionally been studied in single-species metapopulations so that it remains unclear how dispersal evolves in metacommunities and metafoodwebs, which are characterized by a multitude of species interactions. Since most natural systems are both species-rich and spatially structured, this knowledge gap should be bridged. Here, we discuss whether knowledge from dispersal evolutionary ecology established in single-species systems holds in metacommunities and metafoodwebs and we highlight generally valid and fundamental principles. Most biotic interactions form the backdrop to the ecological theatre for the evolutionary dispersal play because interactions mediate patterns of fitness expectations across space and time. While this allows for a simple transposition of certain known principles to a multispecies context, other drivers may require more complex transpositions, or might not be transferred. We discuss an important quantitative modulator of dispersal evolution-increased trait dimensionality of biodiverse meta-systems-and an additional driver: co-dispersal. We speculate that scale and selection pressure mismatches owing to co-dispersal, together with increased trait dimensionality, may lead to a slower and more 'diffuse' evolution in biodiverse meta-systems. Open questions and potential consequences in both ecological and evolutionary terms call for more investigation. This article is part of the theme issue 'Diversity-dependence of dispersal: interspecific interactions determine spatial dynamics'.

Coinfection accelerates transmission to new hosts despite no effects on virulence and parasite growth.

One of the fundamental aims of ecological, epidemiological and evolutionary studies of host-parasite interactions is to unravel which factors affect parasite virulence. Theory predicts that virulence and transmission are correlated by a trade-off, as too much virulence is expected to hamper transmission owing to excessive host damage. Coinfections may affect each of these traits and/or their correlation. Here, we used inbred lines of the spider mite Tetranychus urticae to test how coinfection with T. evansi impacted virulence-transmission relationships at different conspecific densities. The presence of T. evansi on a shared host did not change the relationship between virulence (leaf damage) and the number of transmitting stages (i.e. adult daughters). The relationship between these traits was hump-shaped across densities, both in single and coinfections, which corresponds to a trade-off. Moreover, transmission to adjacent hosts increased in coinfection, but only at low T. urticae densities. Finally, we tested whether virulence and the number of daughters were correlated with measures of transmission to adjacent hosts, in single and coinfections at different conspecific densities. Traits were mostly independent, meaning that interspecific competitors may increase transmission without affecting virulence. Thus, coinfections may impact epidemiology and parasite trait evolution, but not necessarily the virulence-transmission trade-off.This article is part of the theme issue 'Diversity-dependence of dispersal: interspecific interactions determine spatial dynamics'.

Species interactions affect dispersal: a meta-analysis.

Context-dependent dispersal allows organisms to seek and settle in habitats improving their fitness. Despite the importance of species interactions in determining fitness, a quantitative synthesis of how they affect dispersal is lacking. We present a meta-analysis asking (i) whether the interaction experienced and/or perceived by a focal species (detrimental interaction with predators, competitors, parasites or beneficial interaction with resources, hosts, mutualists) affects its dispersal; and (ii) how the species' ecological and biological background affects the direction and strength of this interaction-dependent dispersal. After a systematic search focusing on actively dispersing species, we extracted 397 effect sizes from 118 empirical studies encompassing 221 species pairs; arthropods were best represented, followed by vertebrates, protists and others. Detrimental species interactions increased the focal species' dispersal (adjusted effect: 0.33 [0.06, 0.60]), while beneficial interactions decreased it (-0.55 [-0.92, -0.17]). The effect depended on the dispersal phase, with detrimental interactors having opposite impacts on emigration and transience. Interaction-dependent dispersal was negatively related to species' interaction strength, and depended on the global community composition, with cues of presence having stronger effects than the presence of the interactor and the ecological complexity of the community. Our work demonstrates the importance of interspecific interactions on dispersal plasticity, with consequences for metacommunity dynamics.This article is part of the theme issue 'Diversity-dependence of dispersal: interspecific interactions determine spatial dynamics'.

Dispersal evolution and eco-evolutionary dynamics in antagonistic species interactions.

Dispersal evolution modifies diverse spatial processes, such as range expansions or biological invasions of single species, but we are currently lacking a realistic vision for metacommunities. Focusing on antagonistic species interactions, we review existing theory of dispersal evolution between natural enemies, and explain how this might be relevant for classic themes in host-parasite evolutionary ecology, namely virulence evolution or local adaptation. Specifically, we highlight the importance of considering the simultaneous (co)evolution of dispersal and interaction traits. Linking such multi-trait evolution with reciprocal demographic and epidemiological feedbacks might change basic predictions about coevolutionary processes and spatial dynamics of interacting species. Future challenges concern the integration of system-specific disease ecology or spatial modifiers, such as spatial network structure or environmental heterogeneity.

Intraspecific variation for host immune activation by the spider mite Tetranychus evansi.

Many parasites can interfere with their host's defences to maximize their fitness. Here, we investigated if there is heritable variation in the spider mite Tetranychus evansi for traits associated with how they interact with their host plant. We also determined if this variation correlates with mite fecundity. Tetranychus evansi can interfere with jasmonate (JA) defences which are the main determinant of anti-herbivore immunity in plants. We investigated (i) variation in fecundity in the presence and absence of JA defences, making use of a wild-type tomato cultivar and a JA-deficient mutant (defenseless-1), and (ii) variation in the induction of JA defences, in four T. evansi field populations and 59 inbred lines created from an outbred population originating from controlled crosses of the four field populations. We observed a strong positive genetic correlation between fecundity in the presence (on wild-type) and the absence of JA defences (on defenseless-1). However, fecundity did not correlate with the magnitude of induced JA defences in wild-type plants. Our results suggest that the performance of the specialist T. evansi is not related to their ability to manipulate plant defences, either because all lines can adequately reduce levels of defences, or because they are resistant to them.

Limited host availability disrupts the genetic correlation between virulence and transmission.

Virulence is expected to be linked to parasite fitness via transmission. However, it is not clear whether this relationship is genetically determined, nor if it differs when transmission occurs continuously during, or only at the end of, the infection period. Here, we used inbred lines of the macroparasitic spider mite Tetranychus urticae to disentangle genetic vs. nongenetic correlations among traits, while varying parasite density and opportunities for transmission. A positive genetic correlation between virulence and the number of transmitting stages produced was found under continuous transmission. However, if transmission occurred only at the end of the infection period, this genetic correlation disappeared. Instead, we observed a negative relationship between virulence and the number of transmitting stages, driven by density dependence. Thus, within-host density dependence caused by reduced opportunities for transmission may hamper selection for higher virulence, providing a novel explanation as to why limited host availability leads to lower virulence.

Consequences of population structure for sex allocation and sexual conflict.

Both sex allocation and sexual conflict can be modulated by spatial structure. However, how the interplay between the type of dispersal and the scale of competition simultaneously affects these traits in sub-divided populations is rarely considered. We investigated sex allocation and sexual conflict evolution in meta-populations of the spider mite Tetranychus urticae evolving under budding (pairing females from the same patch) or random (pairing females from different patches) dispersal and either local (fixed sampling from each subpopulation) or global (sampling as a function of subpopulation productivity) competition. Females evolving under budding dispersal produced less female-biased offspring sex ratios than those from the random dispersal selection regimes, contradicting theoretical predictions. In contrast, the scale of competition did not strongly affect sex allocation. Offspring sex ratio and female fecundity were unaffected by the number of mates, but female fecundity was highest when their mates evolved under budding dispersal, suggesting these males inflict less harm than those evolving under random dispersal. This work highlights that population structure can impact the evolution of sex allocation and sexual conflict. Moreover, selection on either trait may reciprocally affect the evolution of the other, for example via effects on fecundity.

A New Prevalent Densovirus Discovered in Acari. Insight from Metagenomics in Viral Communities Associated with Two-Spotted Mite (Tetranychus urticae) Populations.

Viral metagenomics and high throughput sequence mining have revealed unexpected diversity, and the potential presence, of parvoviruses in animals from all phyla. Among arthropods, this diversity highlights the poor knowledge that we have regarding the evolutionary history of densoviruses. The aim of this study was to explore densovirus diversity in a small arthropod pest belonging to Acari, the two-spotted spider mite Tetranychus urticae, while using viral metagenomics based on virus-enrichment. Here, we present the viromes obtained from T. urticae laboratory populations made of contigs that are attributed to nine new potential viral species, including the complete sequence of a novel densovirus. The genome of this densovirus has an ambisens genomic organization and an unusually compact size with particularly small non-structural proteins and a predicted major capsid protein that lacks the typical PLA2 motif that is common to all ambidensoviruses described so far. In addition, we showed that this new densovirus had a wide prevalence across populations of mite species tested and a genomic diversity that likely correlates with the host phylogeny. In particular, we observed a low densovirus genomic diversity between the laboratory and natural populations, which suggests that virus within-species evolution is probably slower than initially thought. Lastly, we showed that this novel densovirus can be inoculated to the host plant following feeding by infected mites, and circulate through the plant vascular system. These findings offer new insights into densovirus prevalence, evolution, and ecology.

Ecology and evolution of facilitation among symbionts.

Facilitation occurs when one species positively impacts the fitness of another, and has predominantly been studied in free-living species like plants. Facilitation can also occur among symbiont (mutualistic or parasitic) species or strains, but equivalent studies are scarce. To advance an integrated view of the effect of facilitation on symbiont ecology and evolution, we review empirical evidence and their underlying mechanisms, explore the factors favouring its emergence, and discuss its consequences for virulence and transmission. We argue that the facilitation concept can improve understanding of the evolutionary forces shaping symbiont communities and their effects on hosts.

Integrating Competition for Food, Hosts, or Mates via Experimental Evolution.

Competitive interactions shape the evolution of organisms. However, often it is not clear whether competition is the driving force behind the patterns observed. The recent use of experimental evolution in competitive environments can help establish such causality. Unfortunately, this literature is scattered, as competition for food, mates, and hosts are subject areas that belong to different research fields. Here, we group these bodies of literature, extract common processes and patterns concerning the role of competition in shaping evolutionary trajectories, and suggest perspectives stemming from an integrative view of competition across these research fields. This review reinstates the power of experimental evolution in addressing the evolutionary consequences of competition, but highlights potential pitfalls in the design of such experiments.

Dispersal, environmental forcing, and parasites combine to affect metapopulation synehrony and stability.

Dispersal can have positive and negative effects on metapopulation stability and persistence. One prediction is that high levels of dispersal synchronize density fluctuations between subpopulations. However, little is still known about how biotic and abiotic factors combine to modify the effects of dispersal rate on synchrony and metapopulation dynamics. In a fully factorial experimental design, we investigated the combined effects of (1) dispersal, (2) parasite infection, and (3) synchrony in temperature fluctuations on subpopulation synchrony, metapopulation instability, and minimum population size, in laboratory metapopulations of the ciliate Paramecium caudatum. Metapopulations, comprising two subpopulations linked by high or low levels of dispersal, were exposed to daily fluctuations in temperature between permissive (23 degrees C) and restrictive (5 degrees C) conditions. Infected metapopulations started the experiment with one subpopulation uninfected, while the other was infected at a prevalence of 5% with the bacterial parasite Holospora undulata. The temperature synchrony treatment involved subpopulations within a metapopulation following the same (synchronous temperatures) or different (asynchronous temperatures) temporal sequences. Population size was tracked over the 56-day experiment. We found that subpopulation density fluctuations were synchronized by high dispersal in infected metapopulations, and by synchronous temperatures in all metapopulations. Subpopulation synchrony was positively correlated with metapopulation instability and minimum metapopulation size, highlighting the multiple consequences of our treatments for metapopulation dynamics. Our results illustrate how parasites can generate dispersal-driven synchrony in non-cycling, declining populations. This "biotic forcing" via a natural enemy added to the temperature-dependent environmental forcing. We therefore conclude that predictions of metapopulation persistence in natural populations require simultaneous investigation of multiple ecological and epidemiological factors.

Density- and trait-mediated effects of a parasite and a predator in a tri-trophic food web.

Despite growing interest in ecological consequences of parasitism in food webs, relatively little is known about effects of parasites on long-term population dynamics of non-host species or about whether such effects are density or trait mediated. We studied a tri-trophic food chain comprised of (i) a bacterial basal resource (Serratia fonticola), (ii) an intermediate consumer (Paramecium caudatum), (iii) a top predator (Didinium nasutum) and (iv) a parasite of the intermediate consumer (Holospora undulata). A fully factorial experimental manipulation of predator and parasite presence/absence was combined with analyses of population dynamics, modelling and analyses of host (Paramecium) morphology and behaviour. Predation and parasitism each reduced the abundance of the intermediate consumer (Paramecium), and parasitism indirectly reduced the abundance of the basal resource (Serratia). However, in combination, predation and parasitism had non-additive effects on the abundance of the intermediate consumer, as well as on that of the basal resource. In both cases, the negative effect of parasitism seemed to be effaced by predation. Infection of the intermediate consumer reduced predator abundance. Modelling and additional experimentation revealed that this was most likely due to parasite reduction of intermediate host abundance (a density-mediated effect), as opposed to changes in predator functional or numerical response. Parasitism altered morphological and behavioural traits, by reducing host cell length and increasing the swimming speed of cells with moderate parasite loads. Additional tests showed no significant difference in Didinium feeding rate on infected and uninfected hosts, suggesting that the combination of these modifications does not affect host vulnerability to predation. However, estimated rates of encounter with Serratia based on these modifications were higher for infected Paramecium than for uninfected Paramecium. A mixture of density-mediated and trait-mediated indirect effects of parasitism on non-host species creates rich and complex possibilities for effects of parasites in food webs that should be included in assessments of possible impacts of parasite eradication or introduction.

The consequences of co-infections for parasite transmission in the mosquito Aedes aegypti.

Co-infections may modify parasite transmission opportunities directly as a consequence of interactions in the within-host environment, but also indirectly through changes in host life history. Furthermore, host and parasite traits are sensitive to the abiotic environment with variable consequences for parasite transmission in co-infections. We investigate how co-infection of the mosquito Aedes aegypti with two microsporidian parasites (Vavraia culicis and Edhazardia aedis) at two levels of larval food availability affects parasite transmission directly, and indirectly through effects on host traits. In a laboratory infection experiment, we compared how co-infection, at low and high larval food availability, affected the probability of infection, within-host growth and the transmission potential of each parasite, compared to single infections. Horizontal transmission was deemed possible for both parasites when infected hosts died harbouring horizontally transmitting spores. Vertical transmission was judged possible for E. aedis when infected females emerged as adults. We also compared the total input number of spores used to seed infections with output number, in single and co-infections for each parasite. The effects of co-infection on parasite fitness were complex, especially for V. culicis. In low larval food conditions, co-infection increased the chances of mosquitoes dying as larvae or pupae, thus increasing opportunities for V. culicis' horizontal transmission. However, co-infection reduced larval longevity and hence time available for V. culicis spore production. Overall, there was a negative net effect of co-infection on V. culicis, whereby the number of spores produced was less than the number used to seed infection. Co-infections also negatively affected horizontal transmission of the more virulent parasite, E. aedis, through reduced longevity of pre-adult hosts. However, its potential transmission suffered less relative to V. culicis. Our results show that co-infection can negatively affect parasite transmission opportunities, both directly as well as indirectly via effects on host life history. We also find that transmission is contingent on the combined effect of the abiotic environment.

Stochastic environmental fluctuations drive epidemiology in experimental host-parasite metapopulations.

Environmental fluctuations are important for parasite spread and persistence. However, the effects of the spatial and temporal structure of environmental fluctuations on host-parasite dynamics are not well understood. Temporal fluctuations can be random but positively autocorrelated, such that the environment is similar to the recent past (red noise), or random and uncorrelated with the past (white noise). We imposed red or white temporal temperature fluctuations on experimental metapopulations of Paramecium caudatum, experiencing an epidemic of the bacterial parasite Holospora undulata. Metapopulations (two subpopulations linked by migration) experienced fluctuations between stressful (5 °C) and permissive (23 °C) conditions following red or white temporal sequences. Spatial variation in temperature fluctuations was implemented by exposing subpopulations to the same (synchronous temperatures) or different (asynchronous temperatures) temporal sequences. Red noise, compared with white noise, enhanced parasite persistence. Despite this, red noise coupled with asynchronous temperatures allowed infected host populations to maintain sizes equivalent to uninfected populations. It is likely that this occurs because subpopulations in permissive conditions rescue declining subpopulations in stressful conditions. We show how patterns of temporal and spatial environmental fluctuations can impact parasite spread and host population abundance. We conclude that accurate prediction of parasite epidemics may require realistic models of environmental noise.

Proteome of Aedes aegypti in response to infection and coinfection with microsporidian parasites.

Hosts are frequently infected with more than one parasite or pathogen at any one time, but little is known as to how they respond to multiple immune challenges compared to those involving single infections. We investigated the proteome of Aedes aegypti larvae following infection with either Edhazardia aedis or Vavraia culicis, and coinfections involving both. They are both obligate intracellular parasites belonging to the phylum microsporidia and infect natural populations of Ae. aegypti. The results found some proteins only showing modified abundance in response to infections involving E. aedis, while others were only differentially abundant when infections involved V. culicis. Some proteins only responded with modified abundance to the coinfection condition, while others were differentially abundant in response to all three types of infection. As time since infection increased, the response to each of the single parasite infections diverged, while the response to the E. aedis and coinfection treatments converged. Some of the proteins differentially abundant in response to infection were identified. They included two vacuolar ATPases, proteins known to have a role in determining the infection success of intracellular parasites. This result suggests microsporidia could influence the infection success of other intracellular pathogens infecting vector species of mosquito, including viruses, Plasmodium and Wolbachia.

Genetic influence on disease spread following arrival of infected carriers.

Epidemiology in host meta-populations depends on parasite ability to disperse between, establish and persist in distinct sub-populations of hosts. We studied the genetic factors determining the short-term establishment, and long-term maintenance, of pathogens introduced by infected hosts (i.e. carriers) into recipient populations. We used experimental populations of the freshwater ciliate Paramecium caudatum and its bacterial parasite Holospora undulata. Parasite short-term spread (approximately one horizontal transmission cycle) was affected mainly by carrier genotype, and its interactions with parasite and recipient genotypes. By contrast, parasite longer term spread (2-3 horizontal transmission cycles) was mostly determined by parasite isolate. Importantly, measures of parasite short-term success (reproductive number, R) were not good predictors for longer term prevalence, probably because of the specific interactions between host and parasite genotypes. Analogous to variation in vectorial capacity and super-spreader occurrence, two crucial components of epidemiology, we show that carrier genotype can also affect disease spread within meta-populations.

Reverse evolution: selection against costly resistance in disease-free microcosm populations of Paramecium caudatum.

Evolutionary costs of parasite resistance arise if genes conferring resistance reduce fitness in the absence of parasites. Thus, parasite-mediated selection may lead to increased resistance and a correlated decrease in fitness, whereas relaxed parasite-mediated selection may lead to reverse evolution of increased fitness and a correlated decrease in resistance. We tested this idea in experimental populations of the protozoan Paramecium caudatum and the parasitic bacterium Holospora undulata. After eight years, resistance to infection and asexual reproduction were compared among paramecia from (1) "infected" populations, (2) uninfected "naive" populations, and (3) previously infected, parasite-free "recovered" populations. Paramecia from "infected" populations were more resistant (+12%), but had lower reproduction (-15%) than "naive" paramecia, indicating an evolutionary trade-off between resistance and fitness. Recovered populations showed similar reproduction to naive populations; however, resistance of recently (<3 years) recovered populations was similar to paramecia from infected populations, whereas longer (>3 years) recovered populations were as susceptible as naive populations. This suggests a weak, convex trade-off between resistance and fitness, allowing recovery of fitness, without complete loss of resistance, favoring the maintenance of a generalist strategy of intermediate fitness and resistance. Our results indicate that (co)evolution with parasites can leave a genetic signature in disease-free populations.

Adaptation of Paramecium caudatum to variable conditions of temperature stress.

The environment is rarely constant and organisms are exposed to spatial and temporal variation that will impact life-histories. It is important to understand how such variation affects the adaptation of organisms to their local environment. We compare the adaptation of populations of the ciliate Paramecium caudatum exposed to constant (23 °C or 35 °C) and temporally variable temperature environments (random daily fluctuations between 23 °C or 35 °C). Consistent with theory, our experiment shows the evolution of specialists when evolution proceeds in constant environments and generalists when the environment is temporally variable. In addition, we demonstrate costs for specialists of being locally adapted through reduced fitness in novel environments. Conversely, we do not find any costs for generalists, as all populations from variable environments had equal or superior performance to specialists in their own environment. The lack of a cost for generalists is emphasised by the presence of a super generalist that has the highest performance at both assay temperatures.

Temporal variation in temperature determines disease spread and maintenance in Paramecium microcosm populations.

The environment is rarely constant and organisms are exposed to temporal and spatial variations that impact their life histories and inter-species interactions. It is important to understand how such variations affect epidemiological dynamics in host-parasite systems. We explored effects of temporal variation in temperature on experimental microcosm populations of the ciliate Paramecium caudatum and its bacterial parasite Holospora undulata. Infected and uninfected populations of two P. caudatum genotypes were created and four constant temperature treatments (26°C, 28°C, 30°C and 32°C) compared with four variable treatments with the same mean temperatures. Variable temperature treatments were achieved by alternating populations between permissive (23°C) and restrictive (35°C) conditions daily over 30 days. Variable conditions and high temperatures caused greater declines in Paramecium populations, greater fluctuations in population size and higher incidence of extinction. The additional effect of parasite infection was additive and enhanced the negative effects of the variable environment and higher temperatures by up to 50 per cent. The variable environment and high temperatures also caused a decrease in parasite prevalence (up to 40%) and an increase in extinction (absence of detection) (up to 30%). The host genotypes responded similarly to the different environmental stresses and their effect on parasite traits were generally in the same direction. This work provides, to our knowledge, the first experimental demonstration that epidemiological dynamics are influenced by environmental variation. We also emphasize the need to consider environmental variance, as well as means, when trying to understand, or predict population dynamics or range.

Parasitic infection reduces dispersal of ciliate host.

Parasitic infection can modify host mobility and consequently their dispersal capacity. We experimentally investigated this idea using the ciliate Paramecium caudatum and its bacterial parasite Holospora undulata. We compared the short-distance dispersal of infected and uninfected populations in interconnected microcosms. Infection reduced the proportion of hosts dispersing, with levels differing among host clones. Host populations with higher densities showed lower dispersal, possibly owing to social aggregation behaviour. Parasite isolates that depleted host populations most had the lowest impact on host dispersal. Parasite-induced modification of dispersal may have consequences for the spatial distribution of disease, host and parasite genetic population structure, and coevolution.