Interference competition and species coexistence

Interference competition is ubiquitous in nature. Yet its effects on resource exploitation remain largely unexplored for species that compete for dynamic resources. Here, I present a model of exploitative and interference competition with explicit resource dynamics. The model incorporates both biotic and abiotic resources. It considers interference competition both in the classical sense (i.e. each species suffers a net reduction in per capita growth rate via interference from, and interference on, the other species) and in the broad sense (i.e. each species suffers a net reduction in per capita growth rate via interference from, but can experience an increase in growth rate via interference on, the other species). Coexistence cannot occur under classical interference competition even when the species inferior at resource exploitation is superior at interference. Such a trade-off can, however, change the mechanism of competitive exclusion from dominance by the superior resource exploiter to a priority effect. Now the inferior resource exploiter can exclude the superior resource exploiter provided it has a higher initial abundance. By contrast, when interference is beneficial to the interacting species, coexistence is possible via a trade-off between exploitation and interference. These results hold regardless of whether the resource is biotic or abiotic, indicating that the outcome of exploitative and interference competition does not depend on the exact nature of resource dynamics. The model makes two key predictions. First, species that engage in costly interference mechanisms (e.g. territoriality, overgrowth or undercutting, allelopathy and other forms of chemical competition) should not be able to coexist unless they also engage in beneficial interference mechanisms (e.g. predation or parasitism). Second, exotic invasive species that displace native biota should be superior resource exploiters that have strong interference effects on native species with little or negative cost. The first prediction provides a potential explanation for patterns observed in several natural systems, including plants, aquatic invertebrates and insects. The second prediction is supported by data on invasive plants and vertebrates.     

Coevolution of parasite virulence and host life history

Most models about the evolutionary interactions between a parasite's virulence and its host's life history neglect two potentially important aspects: epidemiological and coevolutionary feedback. We emphasize their importance by presenting models that describe the coevolution of a semelparous host's age at reproduction and a parasite's virulence in different environmental conditions. In particular, we first show that an epidemiological feedback will lead to a nonmonotonic response of the host's age at reproduction as virulence increases. We then show that the coevolutionary pressure on virulence can lead to complex associations between the host's life history and the parasite's virulence, which would not be expected with more traditional models of host or parasite evolution. Thus, for example, a high mortality rate of the host favours avirulent parasites and late reproduction of the host when the environmental conditions allow the host to grow rapidly, but early reproduction and high virulence when growth is slow.     

Host density and the evolution of parasite virulence

Social and cultural habits of human populations affect the biological evolution of the agents of infectious diseases. Measles and similar diseases have evolved in the Old World and cannot have existed in their present form before the rise of the great river valley civilizations. It is suggested that increased virulence of measles in white and indigenous communities in America 1500-1800 may be due to a rare strain of the virus, which was selected during transfer from Europe. The release of viruses for biological pest control has provided new material for the study of the co-evolution of host-parasite systems, which has upset the dogma "evolution tends to avirulence". It is pointed out that this issue is closely related to the group selection debate among ethologists, i.e. to the problem: how can group selection overcome individual selection? A model is proposed in which differential growth of two strains of a parasite within the host and their transmission to new hosts is considered. It is supposed that transmission stages excreted by infectious hosts enter a common pool where they are mixed before infecting new hosts. Under these conditions, selection of the slower strain is possible only if the mean size of parasite inoculum is very small, i.e. if the density of transmission stages in the environment is low. The impact of this result on host pathology depends on the relation between virulence and transmission efficiency of the parasite.     

Within-host parasite cooperation and the evolution of virulence

Infections by multiple genotypes are common in nature and are known to select for higher levels of virulence for some parasites. When parasites produce public goods (PGs) within the host, such co-infections have been predicted to select for lower levels of virulence. However, this prediction is based on simplifying assumptions regarding epidemiological feedbacks on the multiplicity of infections (MOI). Here, we analyse the case of parasites producing a PG (for example, siderophore-producing bacteria) using a nested model that ties together within-host and epidemiological processes. We find that the prediction that co-infection should select for less virulent strains for PG-producing parasites is only valid if both parasite transmission and virulence are linear functions of parasite density. If there is a trade-off relationship such that virulence increases more rapidly than transmission, or if virulence also depends on the total amount of PGs produced, then more complex relationships between virulence and the MOI are predicted. Our results reveal that explicitly taking into account the distribution of parasite strains among hosts could help better understand the selective pressures faced by parasites at the population level.     

Host age modulates within-host parasite competition

In many host populations, one of the most striking differences among hosts is their age. While parasite prevalence differences in relation to host age are well known, little is known on how host age impacts ecological and evolutionary dynamics of diseases. Using two clones of the water flea Daphnia magna and two clones of its bacterial parasite Pasteuria ramosa, we examined how host age at exposure influences within-host parasite competition and virulence. We found that multiply-exposed hosts were more susceptible to infection and suffered higher mortality than singly-exposed hosts. Hosts oldest at exposure were least often infected and vice versa. Furthermore, we found that in young multiply-exposed hosts competition was weak, allowing coexistence and transmission of both parasite clones, whereas in older multiply-exposed hosts competitive exclusion was observed. Thus, age-dependent parasite exposure and host demography (age structure) could together play an important role in mediating parasite evolution. At the individual level, our results demonstrate a previously unnoticed interaction of the host''s immune system with host age, suggesting that the specificity of immune function changes as hosts mature. Therefore, evolutionary models of parasite virulence might benefit from incorporating age-dependent epidemiological parameters.     

Host resistance and parasite virulence in greenfinch coccidiosis

The question why different host individuals within a population differ with respect to infection resistance is of fundamental importance for understanding the mechanisms of parasite-mediated selection. We addressed this question by infecting wild-caught captive male greenfinches with intestinal coccidian parasites originating either from single or multiple hosts. Birds with naturally low pre-experimental infection retained their low infection status also after reinfection with multiple strains, indicating that natural infection intensities confer information about the phenotypic ability of individuals to resist novel strains. Exposure to novel strains did not result in protective immunity against the subsequent infection with the same strains. Infection with multiple strains resulted in greater virulence than single-strain infection, indicating that parasites originating from different host individuals are genetically diverse. Our experiment thus demonstrates the validity of important but rarely tested assumptions of many models of parasite-mediated selection in a wild bird species and its common parasite.     

Coevolution between parasite virulence and host life-history traits

Epidemiological models generally explore the evolution of parasite life-history traits, namely, virulence and transmission, against a background of constant host life-history traits. However, life-history models have predicted the evolution of host traits in response to parasitism. The coevolution of host and parasite life-history traits remains largely unexplored. We present an epidemiological model, based on resource allocation theory, that provides an analysis of the coevolution between host reproductive effort and parasite virulence. This model allows for hosts with either a fixed (i.e., genetic) or conditional (i.e., a phenotypically plastic) response to parasitism. It also considers superinfections. We show that parasitism always favors increased allocation to host reproduction, but because of epidemiological feedbacks, the evolutionarily stable host reproductive effort does not always increase with parasite virulence. Superinfection drives the evolution of parasite virulence and acts on the evolution of the host through parasite evolution, generally leading to higher host reproductive effort. Coevolution, as opposed to cases where only one of the antagonists evolves, may generate correlations between host and parasite life-history traits across environmental gradients affecting the fecundity or the survival of the host. Our results provide a theoretical framework against which experimental coevolution outcomes or field observations can be contrasted.     

Interference competition among native and invader amphipods

Aquarium experiments were used to study indications of interference competition, such as substratum choice shifts, swimming activities and mortality of invasive and indigenous gammarids in each other's presence. The more recent invaders Gammarus tigrinus and Dikerogammarus villosus were more likely to prefer stone substratum, whereas the native Gammarus pulex and an earlier invader Gammarus roeseli were found more frequently in the water layer. Sand was the least likely substratum to be chosen by any of the species. G. pulex and G. roeseli did not alter their substratum preference in each other's presence. In the presence of D. villosus, G. pulex shifted towards smaller stones and increased its swimming activities, whereas D. villosus did not change its behaviour in the presence of G. pulex. These shifts may indicate interference competition, with D. villosus being the stronger competitor. The greatest shifts in substratum preference arose when one species had occupied a substratum before the other one was introduced, especially when D. villosus was already present before G. pulex was introduced, possibly indicating pre-emptive competition. Swimming activities of G. pulex increased in the presence of D. villosus, whereas D. villosus spent little time swimming. Mortality was comparable between the different experiments without any indication of predation. The effect of Intra Guild Predation (IGP) may not be reflected adequately by short-time experiments as moults occurred seldom during the experiments. Although no IGP was observed during our experiments, habitat shifts occurred, which may indicate that competitive interactions are apparent before IGP starts. Such shifts may serve to avoid intraguild competition.     

Interference competition in desert subterranean termites

We examined interspecific aggression between two subterranean termite species, Heterotermes aureus (Snyder) (Rhinotermitidae) and Gnathamitermes perplexus (Banks) (Termitidae). In laboratory tests with worker termites, neither species was the inherently superior fighter, but rather the outcome of interspecific encounters depended on the number of conspecifics. We then investigated patterns of resource use by these species during a 13-month period in the Sonoran Desert. Baits consisted of toilet-paper rolls, which have been shown to be a mutually acceptable food source. Analyses of foraging activity demonstrated that the two species did not forage independently of each other. Not only were the two species negatively associated spatially, but extended periods of temporal segregation were observed. G. perplexus took significantly longer to return to sites that it had simultaneously occupied with H. aureus than to sites that G. perplexus had occupied alone. The pattern of co-occurrence of these two species is consistent with the hypothesis that interspecific interference competition affects their spatial and temporal distribution.     

Mechanisms of pathogenesis and the evolution of parasite virulence

When studying how much a parasite harms its host, evolutionary biologists turn to the evolutionary theory of virulence. That theory has been successful in predicting how parasite virulence evolves in response to changes in epidemiological conditions of parasite transmission or to perturbations induced by drug treatments. The evolutionary theory of virulence is, however, nearly silent about the expected differences in virulence between different species of parasite. Why, for example, is anthrax so virulent, whereas closely related bacterial species cause little harm? The evolutionary theory might address such comparisons by analysing differences in tradeoffs between parasite fitness components: transmission as a measure of parasite fecundity, clearance as a measure of parasite lifespan and virulence as another measure that delimits parasite survival within a host. However, even crude quantitative estimates of such tradeoffs remain beyond reach in all but the most controlled of experimental conditions. Here, we argue that the great recent advances in the molecular study of pathogenesis provide a way forward. In light of those mechanistic studies, we analyse the relative sensitivity of tradeoffs between components of parasite fitness. We argue that pathogenic mechanisms that manipulate host immunity or escape from host defences have particularly high sensitivity to parasite fitness and thus dominate as causes of parasite virulence. The high sensitivity of immunomodulation and immune escape arise because those mechanisms affect parasite survival within the host, the most sensitive of fitness components. In our view, relating the sensitivity of pathogenic mechanisms to fitness components will provide a way to build a much richer and more general theory of parasite virulence.     

Detection of interspecific competition in parasite communities

Matrices of correlation coefficients between the abundances or intensities of all pairs of helminth species, across all individual hosts in a sample, are regularly used to detect possible cases of interspecific competition in parasite communities. In these matrices, however, the range of possible values that any correlation coefficient can take is not -1 to 1, contrary to what is generally assumed. The number and magnitude of other correlation coefficients in a matrix will constrain the values that any given correlation can achieve. This property of matrices, and of inter-related natural variables, is explained and illustrated with 2 examples from real helminth communities. As a rule, the presence of many negative correlations in a matrix raises the lower value that any of them can possibly achieve. This has important but previously overlooked implications for the interpretation of correlation coefficients, and the detection of competition in natural parasite communities.     

Strong density-dependent competition and acquired immunity constrain parasite establishment: implications for parasite aggregation

The vast majority of parasites exhibit an aggregated frequency distribution within their host population, such that most hosts have few or no parasites while only a minority of hosts are heavily infected. One exception to this rule is the trophically transmitted parasite Pterygodermatites peromysci of the white-footed mouse (Peromyscus leucopus), which is randomly distributed within its host population. Here, we ask: what are the factors generating the random distribution of parasites in this system when the majority of macroparasites exhibit non-random patterns? We hypothesise that tight density-dependent processes constrain parasite establishment and survival, preventing the build-up of parasites within individual hosts, and preclude aggregation within the host population. We first conducted primary infections in a laboratory experiment using white-footed mice to test for density-dependent parasite establishment and survival of adult worms. Secondary or challenge infection experiments were then conducted to investigate underlying mechanisms, including intra-specific competition and host-mediated restrictions (i.e. acquired immunity). The results of our experimental infections show a dose-dependent constraint on within-host-parasite establishment, such that the proportion of mice infected rose initially with exposure, and then dropped off at the highest dose. Additional evidence of density-dependent competition comes from the decrease in worm length with increasing levels of exposure. In the challenge infection experiment, previous exposure to parasites resulted in a lower prevalence and intensity of infection compared with primary infection of naïve mice; the magnitude of this effect was also density-dependent. Host immune response (IgG levels) increased with the level of exposure, but decreased with the number of worms established. Our results suggest that strong intra-specific competition and acquired host immunity operate in a density-dependent manner to constrain parasite establishment, driving down aggregation and ultimately accounting for the observed random distribution of parasites.     

A meta-analysis of parasite virulence in nestling birds

Parasitism is a common cause of host mortality, but little is known about the ecological factors affecting parasite virulence (the rate of mortality among infected hosts). We reviewed 117 field estimates of parasite-induced nestling mortality in birds, showing that there was significant consistency in mortality among host and parasite taxa. Virulence increased towards the tropics in analyses of both species-specific data and phylogenetic analyses. We found evidence of greater parasite prevalence being associated with reduced virulence. Furthermore, bird species breeding in open nest sites suffered from greater parasite-induced mortality than hole-nesting species. By contrast, parasite specialization and generation time of parasites relative to that of hosts explained little variation in virulence. Likewise, there were little or no significant effects of host genetic variability, host sociality, host migration, host insular distribution or host survival on parasite virulence. These findings suggest that parasite-induced nestling mortality in birds is mainly determined by geographical location and to a smaller extent nest site and prevalence.     

Condition-dependent virulence in a horizontally and vertically transmitted bacterial parasite

Virulence is a key component of parasite fitness. Its expression and selective value may not only depend on the features of the parasite's life cycle, but also on host genotype or environmental conditions. Using the freshwater ciliate Paramecium caudatum and its endonuclear bacterial parasite Holospora undulata , we measured variation in virulence (reduction in host division and survival), parasite load and fidelity of vertical transmission for (i) different stages of infection (associated with different opportunities for vertical and horizontal transmission), (ii) different host clones, and (iii) two food conditions. Later stages of infection dedicated to horizontal transmission were more virulent than earlier stages which rely on vertical transmission only. Besides, investment in horizontal transmission decreased the efficacy of vertical transmission, indicating a tradeoff between the two pathways. This may explain the phenotypic plasticity of transmission mode of this parasite. To some extent, virulence, parasite load and transmission fidelity varied with host clone identity and food treatment (higher virulence at low food). These results suggest that virulence is not a constant property of the parasite, and that a single (and simple) relationship between virulence and transmission does not exist.     

Intraspecific competition for host resources in a parasite

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Genetic and environmental determinants of malaria parasite virulence in mosquitoes

Models of malaria epidemiology and evolution are frequently based on the assumption that vector-parasitic associations are benign. Implicit in this assumption is the supposition that all Plasmodium parasites have an equal and neutral effect on vector survival, and thus that there is no parasite genetic variation for vector virulence. While some data support the assumption of avirulence, there has been no examination of the impact of parasite genetic diversity. We conducted a laboratory study with the rodent malaria parasite, Plasmodium chabaudi and the vector, Anopheles stephensi, to determine whether mosquito mortality varied with parasite genotype (CR and ER clones), infection diversity (single versus mixed genotype) and nutrient availability. Vector mortality varied significantly between parasite genotypes, but the rank order of virulence depended on environmental conditions. In standard conditions, mixed genotype infections were the most virulent but when glucose water was limited, mortality was highest in mosquitoes infected with CR. These genotype-by-environment interactions were repeatable across two experiments and could not be explained by variation in anaemia, gametocytaemia, blood meal size, mosquito body size, infection rate or oocyst burden. Variation in the genetic and environmental determinants of virulence may explain conflicting accounts of Plasmodium pathogenicity to mosquitoes in the malaria literature.     

红火蚁与热带火蚁间的干扰竞争

【目的】为了探讨入侵火蚁在我国成功定殖及其之间的竞争机制。【方法】运用行为学方法研究红火蚁Solenopsis invicta(Buren)和热带火蚁Solenopsis geminata(Fabricius)在个体水平和群体水平上的攻击性、攻击手段及合作能力。【结果】一对一攻击试验中,红火蚁和热带火蚁之间攻击级别多集中在3级,两种入侵蚂蚁间以相互威胁为主;红火蚁大型工蚁与热带火蚁兵、工蚁间最为好斗,其攻击级别达到4级的比例最高,分别为33.04%、37.92%。热带火蚁兵蚁与各型红火蚁间攻击强度差异不显著;热带火蚁工蚁与红火蚁小型工蚁之间的攻击性最强,其攻击性(3.49)显著高于热带火蚁工蚁与红火蚁大、中型工蚁的攻击性(3.32和2.97)。在攻击手段上,3级打斗时各型红火蚁更倾向以物理攻击主动威胁热带火蚁,而热带火蚁兵、工蚁会采取多种方式主动攻击红火蚁,双方皆以躲避应对为主;4级打斗时两种火蚁主要以混合攻击为主动或应对手段。群体攻击试验显示,红火蚁群体间攻击强度和合作性会随着群体数量的增加而显著增加,热带火蚁合作性较差,其群体对抗红火蚁的优势仅仅是由于个体数量的增加。【结论】红火蚁比热带火蚁具有更强的竞争优势。研究结果为入侵蚂蚁间不对称竞争机制和长期群落替代的内在原因提供理论基础。     

Interference competition between alien invasive gammaridean species

The relative abundances of gammaridean species in the river Rhine have profoundly changed since the invasion of Dikerogammarus villosus in 1994/1995. This study tested whether these changes in gammaridean dominance could have been determined by interspecific competition and unequal mortality, for example by intraguild predation (IGP). Single and two species tests have been carried out in aquariums provided with all substrata present in the main channel of the Rhine. Changes in substratum choice, increased swimming activity and increased mortality of a species were used as indicators of interspecific competition during interaction between gammaridean species. Interspecific competition and mortality between the most abundant invasive gammaridean species in the Rhine, viz. Gammarus tigrinus, Echinogammarus ischnus and Dikerogammarus villosus were tested. In single-species experiments, G. tigrinus and D. villosus showed similar preferences for a stony substratum, whereas E. ischnus mostly occupied the water column. The two-species aquarium experiments indicated direct interference competition for substratum and unequal mortality between G. tigrinus and D. villosus, with D. villosus being the stronger competitor. Competitive stress was influenced by population density, was size-dependent and varied between the different types of substratum due to substratum choice. G. tigrinus did not show any behaviour indicative of interference competition in the presence of E. ischnus, and neither did E. ischnus or D. villosus in the presence of any of the other gammarideans. Swimming in the water layer may already enable E. ischnus to minimise its encounters with the stone-dwelling D. villosus and G. tigrinus. To maximise the encounters between E. ischnus and D. villosus, a fish (Lepomis gibbosus) was added to occupy the water layer during the aquarium experiments. E. ischnus showed a higher mortality in the presence of both D. villosus and fish, probably due to increased stress, as shelter opportunities to escape the predators had been minimised. The study shows that interference competition between gammaridean species can explain the replacement of the North American invader G. tigrinus by D. villosus in the river Rhine. E. ischnus and D. villosus both Ponto-Caspian invaders did not show interference competition in our experiments and co-exist in the Rhine.     

Metabolic changes in glucose transporter-deficient Leishmania mexicana and parasite virulence

Leishmania mexicana are parasitic protozoa that express a variety of glycoconjugates that play important roles in their biology as well as the storage carbohydrate beta-mannan, which is an essential virulence factor for survival of intracellular amastigote forms in the mammalian host. Glucose transporter null mutants, which are viable as insect form promastigotes but not as amastigotes, do not take up glucose and other hexoses but are still able to synthesize these glycoconjugates and beta-mannan, although at reduced levels. Synthesis of these carbohydrate-containing macromolecules could be accounted for by incorporation of non-carbohydrate precursors into carbohydrates by gluconeogenesis. However, the significantly reduced level of the virulence factor beta-mannan in the glucose transporter null mutants compared with wild-type parasites may contribute to the non-viability of these null mutants in the disease-causing amastigote stage of the life cycle.