Population dynamic consequences of parasitised-larval competition in stage-structured host–parasitoid systems

Parasitism can influence many aspects of the host's behaviour and physiology, which in turn can have a profound impact on their population and evolutionary ecology. In many host–parasite interactions there is often a time lag between infection and the death of the host, yet little is known, experimentally or theoretically, about the effects that intra-class competition between parasitised and unparasitised hosts have on the host–parasite population dynamics.
In this article we address this gap in our understanding using a stage-structured mathematical model for a host–parasitoid interaction, which has been parameterised for the Plodia–Venturia experimental system.
In the case where parasitised larvae do not compete and do not cannibalise unparasitised larvae, our model predicts a wide range of host–parasitoid dynamics, ranging from host–parasitoid generation cycles, to host generation cycles with parasitoid half-generation cycles, to host–parasitoid equilibria, to host generation cycles with parasitoid extinction.
However, when parasitised larvae can compete with their unparasitised larvae counterparts, the host–parasitoid population dynamics can dramatically change. In particular, we show that high levels of competition exerted by unparasitised larvae upon parasitised larvae is more likely to lead to parasitoid extinction.
In addition, we demonstrate that unparasitised host larvae that are sufficiently susceptible to intra-class competition, or parasitised host larvae that are sufficiently strong competitors, can have a stabilising effect on the host–parasitoid population dynamics.
The implications of these theoretical results are discussed in light of our understanding of host–parasitoid interactions and host–parasite systems in general.     

Influence of experimental warming and shading on host–parasitoid synchrony

As the climate warms, many species are showing altered phenology patterns, potentially disrupting synchrony between interacting species. Recent studies have documented disrupted synchrony in plant–herbivore and predator–prey interactions. However, studies investigating climate‐related asynchrony in host–parasitoid interactions and exploring the relative responses of interacting hosts and parasitoids to climate change are lacking. This is an important gap in knowledge given the ubiquity of insect parasitoids and their importance in influencing the abundance and dynamics of their hosts. In the threatened marsh fritillary butterfly Euphydryas aurinia (Lepidoptera: Nymphalidae) and its specialized parasitoid, Cotesia bignellii (Hymenoptera: Braconidae) phenological synchrony (and consequently population fluctuations) are thought to be weather‐dependent. To assess the likely influence of climate and microenvironment change on synchrony between E. aurinia and C. bignellii, we experimentally manipulated the exposure of sensitive‐stage host larvae and parasitoid pupae to temperature (ambient or elevated) and shading (shaded or unshaded) regimes. We also analysed a 20‐year population dynamic dataset from the United Kingdom for E. aurinia to investigate whether population variations could be explained by interannual variations in the thermal and sunshine environment. Development times were affected significantly by the experimental temperature and shading treatments for E. aurinia but not for C. bignellii. However, the contrasting responses were insufficient to significantly affect host availability for parasitoids. In the field, thermal and sunshine conditions did not influence population fluctuations, and population variations across a large (UK‐wide) scale were uncorrelated. Changes to the thermal and sunshine environment of the magnitude investigated in our experiment and within the range experienced by wild E. aurinia populations over the last 20‐years thus seem unlikely to cause breakdown in host–parasitoid synchrony. We suggest that experiments investigating the mechanistic responses of interacting species to environmental change are needed to support the analysis and interpretation of observational data on species' phenology.     

Speciation and the evolution of dispersal along environmental gradients

We analyze the joint evolution of an ecological character and of dispersal distance in asexual and sexual populations inhabiting an environmental gradient. Several interesting phenomena resulting from the evolutionary interplay of these characters are revealed. First, asexual and sexual populations exhibit two analogous evolutionary regimes, in which either speciation in the ecological character occurs in conjunction with evolution of short-range dispersal, or dispersal distance remains high and speciation does not occur. Second, transitions between these two regimes qualitatively differ between asexual and sexual populations, with the former showing speciation with long-range dispersal and the latter showing no speciation with short-range dispersal. Third, a phenotypic gradient following the environmental gradient occurs only in the last case, i.e., for non-speciating sexual populations evolving towards short-range dispersal. Fourth, the transition between the evolutionary regimes of long-range dispersal with no speciation and short-range dispersal with speciation is typically abrupt, mediated by a positive feedback between incipient speciation and the evolution of short-range dispersal. Fifth, even though the model of sexual evolution analyzed here does not permit assortative mating preferences, speciation occurs for a surprisingly wide range of conditions. This illustrates that dispersal evolution is a powerful alternative to preference evolution in enabling spatially distributed sexual populations to respond to frequency-dependent disruptive selection.     

The evolution of conditional dispersal and reproductive isolation along environmental gradients

Dispersal modulates gene flow throughout a population's spatial range. Gene flow affects adaptation at local spatial scales, and consequently impacts the evolution of reproductive isolation. A recent theoretical investigation has demonstrated that local adaptation along an environmental gradient, facilitated by the evolution of limited dispersal, can lead to parapatric speciation even in the absence of assortative mating. This and other studies assumed unconditional dispersal, so individuals start dispersing without regard to local environmental conditions. However, many species disperse conditionally; their propensity to disperse is contingent upon environmental cues, such as the degree of local crowding or the availability of suitable mates. Here, we use an individual-based model in continuous space to investigate by numerical simulation the relationship between the evolution of threshold-based conditional dispersal and parapatric speciation driven by frequency-dependent competition along environmental gradients. We find that, as with unconditional dispersal, parapatric speciation occurs under a broad range of conditions when reproduction is asexual, and under a more restricted range of conditions when reproduction is sexual. In both the asexual and sexual cases, the evolution of conditional dispersal is strongly influenced by the slope of the environmental gradient: shallow environmental gradients result in low dispersal thresholds and high dispersal distances, while steep environmental gradients result in high dispersal thresholds and low dispersal distances. The latter, however, remain higher than under unconditional dispersal, thus undermining isolation by distance, and hindering speciation in sexual populations. Consequently, the speciation of sexual populations under conditional dispersal is triggered by a steeper gradient than under unconditional dispersal. Enhancing the disruptiveness of frequency-dependent selection, more box-shaped competition kernels dramatically lower the speciation-enabling slope of the environmental gradient.     

Host refuges and spatial patterns of parasitism in an endophytic host–parasitoid system

Abstract. 1. Larvae of Tephritis conura Loew (Diptera: Tephritidae) live gregariously in flower heads of Cirsium heterophyllum (L.) Hill (Cardueae). They are attacked by the endoparasitic wasps Eurytoma sp. near tibialis Boheman (Hymenoptera: Eurytomidae) and Pteromalus caudiger (Graham) (Hymenoptera: Pteromalidae).
2. The responses of the parasitoids to different host patch sizes were investigated from the analysis of field samples. At the host population level, overall probabilities of parasitism were independent of host numbers per flower head or showed a tendency to inverse density-dependence for both parasitoid species.
3. Measurements of ovipositor length in Eurytoma and P.caudiger indicated that parts of the flower head constitute a structural refuge from parasitism.
4. The accessibility of hosts in a flower head was found to differ markedly, depending on larval locations and flower head characters. In spite of this high variability, similar average percentages of larvae were accessible to the parasitoids in each patch size class.
5. High variability of oviposition success in laboratory experiments can be explained by random locations of hosts in the flower heads.     

Population abundance of two-patch competitive systems with asymmetric dispersal

Journal of Mathematical Biology - This paper considers two-species competitive systems with two patches, in which one of the species can move between the patches. One patch is a source where each...     

Effects of gender and mating status on self-directed dispersal by the whitefly parasitoid Eretmocerus eremicus

1. The impacts of gender and mating on short‐range (< 10 km) dispersal by the whitefly parasitoid Eretmocerus eremicus Rose and Zolnerowich (Hymenoptera: Aphelinidae) were examined. A fluorescent dust‐marking technique was also tested. 2. In a vertical flight chamber, female flight duration was significantly longer than that of males, and unmated parasitoids flew for longer than mated parasitoids. The mean flight durations were: unmated females 34 min, mated females 10 min, unmated males 7 min, mated males < 1 min. 3. The dispersal behaviour of E. eremicus was investigated in the field using fluorescent dust. Before doing so, it was determined in the laboratory that this dust did not affect flight behaviour, was retained over the length of the experiments, and allowed large samples to be processed quickly and inexpensively. 4. In the field, traps were placed along annuli at 3, 5, 7, and 10 m from release points. Eighty‐seven per cent of the 4153 parasitoids captured were males. Sex ratios were near parity on release. 5. The difference in dispersal characteristics between males and females may be resource based, suggesting that certain requirements were met within the field plots for males that were not met for females. 6. Locally, males dispersed in a manner consistent with a simple diffusion model while females engaged in wind‐directed flight soon after leaving release sites. The fact that the genders exhibited dissimilar dispersal characteristics, supports the claim that insect flight, even by small species, can be self‐directed.     

Effects of dispersal on the stability of a gonorrhea endemic model

Using Liapunov's direct method, effects of dispersal on the linear and nonlinear stability of the endemic equilibrium state of the system governing the spread of gonorrhea are investigated. It is noted that the equilibrium state, which is nonlinearly asymptotically stable in the feasible region of the phase plane in the absence of dispersal, remains so with self-dispersal also (cross-dispersal being absent). However, in the presence of both self- and cross-dispersal, the equilibrium state can still remain nonlinearly asymptotically stable in the entire feasible region provided a certain condition involving self- and cross-dispersal coefficients is satisfied. It is also seen in this case that, for the linearly stable equilibrium state, there exists a subregion of the feasible region where it is nonlinearly asymptotically stable.     

The dispersal success and persistence of populations with asymmetric dispersal

Asymmetric dispersal is a common trait among populations, often attributed to heterogeneity and stochasticity in both environment and demography. The cumulative effects of population dispersal in space and time have been described with some success by Van Kirk and Lewis’s average dispersal success approximation (Bull Math Biol 59(1): 107–137 1997), but this approximation has been demonstrated to perform poorly when applied to asymmetric dispersal. Here we provide a comparison of different characterizations of dispersal success and demonstrate how to capture the effects of asymmetric dispersal. We apply these different methods to a variety of integrodifference equation population models with asymmetric dispersal, and examine the methods’ effectiveness in approximating key ecological traits of the models, such as the critical patch size and the critical speed of climate change for population persistence.     

Effects of dispersal on the stability of a prey-predator system with functional response

Using Liapunov's direct method, effects of dispersal on the linear and nonlinear stability of the equilibrium state for a prey-predator system with functional response are investigated. It is noted that the functional response has a destabilizing effect. It is shown that an otherwise linearly or nonlinearly stable equilibrium state of the system remains so with dispersal as well, even with functional response. It is further established that if the equilibrium state is linearly stable a subregion of the positive quadrant can be found in the phase plane where it is nonlinearly stable with or without dispersal.     

Density-dependent dispersal and relative dispersal affect the stability of predator-prey metacommunities

Although density-dependent dispersal and relative dispersal (the difference in dispersal rates between species) have been documented in natural systems, their effects on the stability of metacommunities are poorly understood. Here we investigate the effects of intra- and interspecific density-dependent dispersal on the regional stability in a predator-prey metacommunity model. We show that, when the dynamics of the populations reach equilibrium, the stability of the metacommunity is not affected by density-dependent dispersal. However, the regional stability, measured as the regional variability or the persistence, can be modified by density-dependent dispersal when local populations fluctuate over time. Moreover these effects depend on the relative dispersal of the predator and the prey. Regional stability is modified through changes in spatial synchrony. Interspecific density-dependent dispersal always desynchronizses local dynamics, whereas intraspecific density-dependent dispersal may either synchronize or desynchronize it depending on dispersal rates. Moreover, intra- and interspecific density-dependent dispersal strengthen the top-down control of the prey by the predator at intermediate dispersal rates. As a consequence the regional stability of the metacommunity is increased at intermediate dispersal rates. Our results show that density-dependent dispersal and relative dispersal of species are keys to understanding the response of ecosystems to fragmentation.     

Competition between relatives and the evolution of dispersal in a parasitoid wasp

Evolutionary theory predicts that levels of dispersal vary in response to the extent of local competition for resources and the relatedness between potential competitors. Here, we test these predictions by making use of a female dispersal dimorphism in the parasitoid wasp Melittobia australica. We show that there are two distinct female morphs, which differ in morphology, pattern of egg production, and dispersal behaviour. As predicted by theory, we found that greater competition for resources resulted in increased production of dispersing females. In contrast, we did not find support for the prediction that high relatedness between competitors increases the production of dispersing females in Melittobia. Finally, we exploit the close links between the evolutionary processes leading to selection for dispersal and for biased sex ratios to examine whether the pattern of dispersal can help distinguish between competing hypotheses for the lack of sex ratio adjustment in Melittobia.     

Density dependence and environmental factors affect population stability of an agricultural pest and its specialist parasitoid

Host–parasitoid dynamics are intrinsically unstable unless the risk of parasitism is sufficiently heterogeneous among hosts. Spatial aggregation of parasitoids can contribute to this heterogeneity, stabilising host–parasitoid population dynamics and thereby reducing pest outbreaks. We examined the spatial distribution of mango gall fly (Procontarinia matteiana, Kiefer and Cecconi), a non-native pest of South African mango orchards, which is controlled by a single parasitoid (Chrysonotomyia pulcherrima, Kerrich). We assessed whether spatial aggregation of parasitoids is associated with proximity to natural vegetation and/or to host density-dependent and host density-independent factors at three spatial scales. We found evidence for higher parasitism rates near natural vegetation at the field scale, and inverse host-density dependent and density-independent parasitoid aggregation at both the leaf scale and field scale. Therefore, we conclude that natural vegetation plays a role in promoting stabilising aggregation of parasitoids, possibly through provision of non-host resources (nectar, pollen), in this system.     

Local adaptation and the geometry of host–parasite coevolution

Metapopulation dynamics can strongly affect the ecological and evolutionary processes involved in host–parasite interactions. Here, I analyse a deterministic host–parasite coevolutionary model and derive analytic approximations for the level of local adaptation as a function of (1) host migration rate, (2) parasite migration rate, (3) parasite specificity and (4) parasite virulence. This analysis confirms the results of previous simulation studies: the difference between host and parasite migration rates may explain the level of local adaptation of both species. I also show that both higher specificity and higher virulence generally lead to higher levels of local adaptation of the species which is already ahead in the coevolutionary arms race. The present analysis also provides a simple geometric interpretation for local adaptation which captures the complexity of the temporal dynamics of host–parasite coevolution.