Among population variation in specialist and generalist seed predation – the importance of host plant distribution, alternative hosts and environmental variation

Pre-dispersal seed predators can have important effects on population dynamics and trait selection in their host plants. However, the factors determining spatial variation in predation intensity are poorly known. We assessed the relative importance of host plant distribution, alternative hosts and environmental factors for among-population variation in predation in a system with three host plants, a specialist and a generalist pre-dispersal seed predator.
Effects of host plant population size were relatively more important in the specialist than in the generalist seed predator. The specialist seed predator Apion opeticum , utilizing only Lathyrus vernus occurred in less than half of the patches, and specialist seed predation was influenced only by host plant population size. The generalist Bruchus atomarius was present in nearly all patches, and generalist predation was influenced by environmental factors and availability of alternative hosts. Predation on alternative hosts was not affected by L. vernus presence.
The results suggest that a wide range of factors influences the strength of plant–seed–predator interactions, and that the relative importance of different factors depend on the degree of specialization. This will result in highly complex selection mosaics and coevolutionary trajectories.     

Optimal foraging predicts the ecology but not the evolution of host specialization in bacteriophages

We explore the ability of optimal foraging theory to explain the observation among marine bacteriophages that host range appears to be negatively correlated with host abundance in the local marine environment. We modified Charnov's classic diet composition model to describe the ecological dynamics of the related generalist and specialist bacteriophages phiX174 and G4, and confirmed that specialist phages are ecologically favored only at high host densities. Our modified model accurately predicted the ecological dynamics of phage populations in laboratory microcosms, but had only limited success predicting evolutionary dynamics. We monitored evolution of attachment rate, the phenotype that governs diet breadth, in phage populations adapting to both low and high host density microcosms. Although generalist phiX174 populations evolved even broader diets at low host density, they did not show a tendency to evolve the predicted specialist foraging strategy at high host density. Similarly, specialist G4 populations were unable to evolve the predicted generalist foraging strategy at low host density. These results demonstrate that optimal foraging models developed to explain the behaviorally determined diets of predators may have only limited success predicting the genetically determined diets of bacteriophage, and that optimal foraging probably plays a smaller role than genetic constraints in the evolution of host specialization in bacteriophages.     

Contrasting genomic patterns and infection strategies of two co‐existing Bacteroidetes podovirus genera

Bacterial viruses (phages) are abundant, ecologically important biological entities. However, our understanding of their impact is limited by model systems that are primarily not well represented in nature, e.g. Enterophages and their hosts. Here, we investigate genomic characteristics and infection strategies among six aquatic Bacteroidetes phages that represent two genera of exceptionally large (～70–75 kb genome) podoviruses, which were isolated from the same seawater sample using Cellulophaga baltica as host. Quantitative host range studies reveal that these genera have contrasting narrow (specialist) and broad (generalist) host ranges, with one‐step growth curves revealing reduced burst sizes for the generalist phages. Genomic comparisons suggest candidate genes in each genus that might explain this host range variation, as well as provide hypotheses about receptors in the hosts. One generalist phage, φ38:1, was more deeply characterized, as its infection strategy switched from lytic on its original host to either inefficient lytic or lysogenic on an alternative host. If lysogenic, this phage was maintained extrachromosomally in the alternative host and could not be induced by mitomycin C. This work provides fundamental knowledge regarding phage‐host ranges and their genomic drivers while also exploring the ‘host environment’ as a driver for switching phage replication mode.     

Spatiotemporal Model of Barley and Cereal Yellow Dwarf Virus Transmission Dynamics with Seasonality and Plant Competition

Many generalist pathogens are influenced by the spatial distributions and relative abundances of susceptible host species. The spatial structure of host populations can influence patterns of infection incidence (or disease outbreaks), and the effects of a generalist pathogen on host community dynamics in a spatially heterogeneous community may differ from predictions derived via simple models. In this paper, we model the transmission of a generalist pathogen within a patch framework that incorporates the movement of vectors between discrete host patches to investigate the effects of local host community composition and vector movement rates on disease dynamics.     

Specialized avian Haemosporida trade reduced host breadth for increased prevalence

Parasite specialization on one or a few host species leads to a reduction in the total number of available host individuals, which may decrease transmission. However, specialists are thought to be able to compensate by increased prevalence in the host population and increased success in each individual host. Here, we use variation in host breadth among a community of avian Haemosporida to investigate consequences of generalist and specialist strategies on prevalence across hosts. We show that specialist parasites are more prevalent than generalist parasites in host populations that are shared between them. Moreover, the total number of infections of generalist and specialist parasites within the study area did not vary significantly with host breadth. This suggests that specialists can infect a similar number of host individuals as generalists, thus compensating for a reduction in host availability by achieving higher prevalence in a single host species. Specialist parasites also tended to infect older hosts, whereas infections by generalists were biased towards younger hosts. We suggest that this reflects different abilities of generalists and specialists to persist in hosts following infection. Higher abundance and increased persistence in hosts suggest that specialists are more effective parasites than generalists, supporting the existence of a trade‐off between host breadth and average host use among these parasites.     

Specificity and host predictability: a comparative analysis among monogenean parasites of fish

1. This article compares generalist (parasite species found on two or more host species) and specialist (found on only one host species) monogenean parasite species of fish. The reduction of the host range – that is an increase in host specificity – may correspond with a better adaptation of the parasite to a more predictable host environment. A more predictable environment may allow the parasite species to develop specific adaptations.
2. We assume that the more predictable host environment can be evaluated by host body size, since numerous life-traits, such as longevity, are positively correlated with size.
3. We found that specialist parasites parasitize larger hosts species than generalist parasites. We also found a good relationship between host body size and parasite body size for specialist parasite species.
4. An adaptation to the mechanical problems encountered in the host's gill chamber may lead to an increase in parasite body size. The infection of a larger part of the host population in order to decrease the chances of local extinction due to fluctuations of host abundance may be another adaptive mechanism.
5. We found a negative correlation between parasite body size and prevalence for generalist parasite species. This relationship disappeared when using the comparative method controlling for phylogeny, which proved that it was a phylogenetic effect.     

Changes in phytophagous insect host ranges following the invasion of their community: Long‐term data for fruit flies

The invasion of an established community by new species can trigger changes in community structure. Invasions often occur in phytophagous insect communities, the dynamics of which are driven by the structure of the host assemblage and the presence of competitors. In this study, we investigated how a community established through successive invasions changed over time, taking the last invasion as the reference. The community included four generalist and four specialist species of Tephritidae fruit flies. We analyzed a long‐term database recording observed numbers of flies per fruit for each species on 36 host plants, over 18 years, from 1991 to 2009. Community structure before the last invasion by Bactrocera zonata in 2000 was described in relation to host plant phylogeny and resource availability. Changes in the host range of each species after the arrival of B. zonata were then documented by calculating diversity indices. The flies in the community occupied three types of niches defined on the basis of plant phylogeny (generalists, Solanaceae specialist, and Cucurbitaceae specialists). After the arrival of B. zonata, no change in the host range of specialist species was observed. However, the host ranges of two generalist species, Ceratitis quilicii and Ceratitis capitata, tended to shrink, as shown by the decreases in species richness and host plant α‐diversity. Our study shows increased host specialization by generalist phytophagous insects in the field following the arrival of an invasive species sharing part of their resources. These findings could be used to improve predictions of new interactions between invaders and recipient communities.     

Coexistence of Habitat Specialists and Generalists in Metapopulation Models of Multiple-Habitat Landscapes

In coarse-grained environments specialists are generally predicted to dominate. Empirically, however, coexistence with generalists is often observed. We present a simple, but previously unrecognized, mechanism for coexistence of a habitat generalist and a number of habitat specialist species. In our model all species have a metapopulation structure in a landscape consisting of patches of different habitat types, governed by local extinction and colonization. Each specialist is limited to its specific type of habitat. The generalist can use more types of habitat, has a lower local competitive ability but can exploit patches left open by the specialists. Our modeling shows that coexistence is easily possible. The mechanism amounts to a colonization/competition trade-off at the landscape level, where the colonization advantage of the inferior competitor does not arise from a higher colonization rate but from its ability to use more types of habitat. Habitat availability has to be intermediate: when there are few patches of each habitat, only the generalist is able to maintain itself and when there are many patches, high propagule pressure of the specialists excludes the generalist. Habitat selection or temporal variations in relative habitat quality are not necessary for coexistence. Increased niche-width, colonization rate or local competitive ability of the generalist enhances its performance compared to the specialists. Various types of habitat degradation favour generalism. When able to use a broad range of habitats, generalists can generate so much propagule pressure that only a low level of local competitive ability is needed to globally exclude the specialists. Hence, in a reversal of the original problem, the question is why there are so many specialist metapopulations?     

Can natural enemies enforce geographical range limits?

We develop a simple mathematical model to investigate the question as to whether a specialised consumer can be responsible for creating a range limit in the population of its dynamic resource. The model is most attuned for parasitoid-host relationships, but the central results should apply to a broad range of systems. Specifically, at the beginning of each simulation host and parasitoid populations are distributed at random along a string of patches. In each discrete generation and for each patch, host and parasitoid populations grow and interact, and then a constant fraction of those remaining disperses one or more patch distances in either direction according to a geometric distribution. We iterate the model 200 generations, and in any generation for any patch, either host and/or parasitoid can go locally extinct if its population falls below a threshold density. We find that a specialised parasitoid can enforce a limit, and it is even more likely to fragment its host population. The two most important conditions for parasitoid-enforced range limits are: 1) the theoretical host equilibrium density in the presence of the parasitoid be very small at sites eliminated from the host's range, and 2) the parasitoid disperses at high rates. We close by discussing our findings for specialist and generalist natural enemies, and the relevance of our study to the wealth of investigations on the causes of geographical range limits.     

Predator diet breadth influences the relative importance of bottom-up and top-down control of prey biomass and diversity

We investigated the effects of predator diet breadth on the relative importance of bottom-up and top-down control of prey assemblages, using microbial food webs containing bacteria, bacterivorous protists and rotifers, and two different top predators. The experiment used a factorial design that independently manipulated productivity and the presence or absence of two top predators with different diet breadths. Predators included a "specialist" predatory ciliate Euplotes aediculatus, which was restricted to feeding on small prey, and a "generalist" predatory ciliate Stentor coeruleus, which could feed on the entire range of prey sizes. Both total prey biomass and prey diversity increased with productivity in the predator-free control and specialist predator treatments, a pattern consistent with bottom-up control, but both remained unchanged by productivity in the generalist predator treatment, a pattern consistent with top-down control. Linear food chain models adequately described responses in the generalist predator treatment, whereas food web models incorporating edible and inedible prey (which can coexist in the absence of predators) adequately described responses in the specialist predator treatment. These results suggest that predator diet breadth can play an important role in modulating the relative strength of bottom-up and top-down forces in ecological communities.     

Facilitation through altered resource availability in a mixed‐species rodent malaria infection

A major challenge in disease ecology is to understand how co‐infecting parasite species interact. We manipulate in vivo resources and immunity to explain interactions between two rodent malaria parasites, Plasmodium chabaudi and P. yoelii. These species have analogous resource‐use strategies to the human parasites Plasmodium falciparum and P. vivax: P. chabaudi and P. falciparum infect red blood cells (RBC) of all ages (RBC generalist); P. yoelii and P. vivax preferentially infect young RBCs (RBC specialist). We find that: (1) recent infection with the RBC generalist facilitates the RBC specialist (P. yoelii density is enhanced ~10 fold). This occurs because the RBC generalist increases availability of the RBC specialist's preferred resource; (2) co‐infections with the RBC generalist and RBC specialist are highly virulent; (3) and the presence of an RBC generalist in a host population can increase the prevalence of an RBC specialist. Thus, we show that resources shape how parasite species interact and have epidemiological consequences.     

Responses of a generalist and a specialist parasitoid (Hymenoptera: Eucoilidae) to Drosophilid larval kairomones

Foraging parasitoids are thought to need more specific information than generalists on the presence, identity, availability, and suitability of their insect host species. In the present paper, we compare responses to host kairomones by two phylogenetically related parasitoid species that attack Drosophilidae and that differ in the width of their host range. As predicted, the behavioral response of the parasitoids to host kairomones reflected their difference in host range. The response of the specialist parasitoid Leptopilina boulardiwas restricted to contact kairomones from its natural hosts and one closely related species. In contrast, the generalist parasitoid Leptopilina heterotomaresponded to contact kairomones of a variety of Drosophilidae species.     

Decision making by generalist and specialist aphids with the same genotype

One idea to explain the high incidence of specialisation in phytophagous insects is that their nervous systems are simple and unable to efficiently recognise multiple host plants. Here this 'neural limitations' hypothesis is tested using a generalist (the summer winged virginopara) and specialist (the autumn gynopara) morph of a single clone of the black bean aphid, Aphis fabae, that are almost identical morphologically and have the same genotype. Electrical monitoring of stylet behaviour and non-invasive behavioural observations are used to compare initial plant recognition, first reproduction, 'first registered phloem contact' and 'phloem acceptance' of the generalist and specialist on their specific host plants (generalist--herbaceous hosts, Beta vulgaris, Papaver dubium, Rumex obtusifolius, Vicia faba; specialist--woody host, Euonymus europaeus) and on the same host (E. europaeus). Additional analyses of behaviour over the first few minutes of plant contact are carried out for three mutual non-host plants: Euonymus alatus, Prunus padus and Brassica pekinensis. Few examples are found where the host-selection behaviour of the specialist on its host plant is more efficient than the generalist across its hosts and there is little difference in the behaviour of the different forms on the same host. Indeed there are several instances where the generalist is behaviourally more efficient than the specialist. These include absolute time to first reproduction by the generalist on various herbaceous hosts and the same host, E. europaeus, absolute time to first registered phloem contact by the generalist on P. dubium, and incidence of phloem acceptance by the generalist on several of its herbaceous hosts. Rejection of non-hosts is carried out more efficiently by the specialist gynopara on P. padus and B. pekinensis but not on E. alatus. For generalist and specialist morphs of the same A. fabae genotype, therefore, broad host range does not appear to be associated with a reduced ability to make plant-use decisions.     

Use of novel pollen species by specialist and generalist solitary bees (Hymenoptera: Megachilidae)

If trade-offs between flexibility to use a range of host species and efficiency on a limited set underlie the evolution of diet breadth, one resulting prediction is that specialists ought to be more restricted than generalists in their ability to use novel resource species. I used foraging tests and feeding trials to compare the ability of a generalist and a specialist solitary mason bee species to collect and develop on two pollen species that are not normally used in natural populations (novel pollens). Osmia lignaria (Hymenoptera: Megachilidae) is a generalist pollen feeder; O. californica, is more specialized. Adults of the specialist were more limited in use of novel hosts, but only in some contexts. Both bee species refused to collect one novel pollen. The specialist accepted a second novel pollen only when it was presented along with its normal pollen, whereas the generalist collected novel pollen whether presented alone or with normal pollen. Surprisingly, larvae of the specialist were more flexible than were generalists. The specialist grew well on mixtures of normal and novel pollen species, in some cases better than on its normal host alone. Larvae of the generalist grew more poorly on all diets containing novel pollens than on their normal host. Data on these two species of bees suggest that specialization by itself need not reduce flexibility on novel hosts. The findings also provide information about mechanisms of specialization in bees. Similar to some folivores, specific cues of the pollen host and the bee's interpretation of these contribute, along with foraging economics, to pollen choice by adults. The ability of the larvae to cope with specific components of one pollen species need not interfere with its ability to use others.     

Dynamics of a intraguild predation model with generalist or specialist predator

Intraguild predation (IGP) is a combination of competition and predation which is the most basic system in food webs that contains three species where two species that are involved in a predator/prey relationship are also competing for a shared resource or prey. We formulate two intraguild predation (IGP: resource, IG prey and IG predator) models: one has generalist predator while the other one has specialist predator. Both models have Holling-Type I functional response between resource-IG prey and resource-IG predator; Holling-Type III functional response between IG prey and IG predator. We provide sufficient conditions of the persistence and extinction of all possible scenarios for these two models, which give us a complete picture on their global dynamics. In addition, we show that both IGP models can have multiple interior equilibria under certain parameters range. These analytical results indicate that IGP model with generalist predator has “top down” regulation by comparing to IGP model with specialist predator. Our analysis and numerical simulations suggest that: (1) Both IGP models can have multiple attractors with complicated dynamical patterns; (2) Only IGP model with specialist predator can have both boundary attractor and interior attractor, i.e., whether the system has the extinction of one species or the coexistence of three species depending on initial conditions; (3) IGP model with generalist predator is prone to have coexistence of three species.     

Host availability and the evolution of parasite life-history strategies

Parasites exploit an inherently patchy resource, their hosts, which are discrete entities that may only be available for infection within a relatively short time window. However, there has been little consideration of how heterogeneities in host availability may affect the phenotypic or genotypic composition of parasite populations or how parasites may evolve to cope with them. Here we conduct a selection experiment involving an entomopathogenic nematode (Steinernema feltiae) and show for the first time that the infection rate of a parasite can evolve rapidly to maximize the chances of infecting within an environment characterized by the rate of host availability. Furthermore, we show that the parasite's infection rate trades off with other fitness traits, such as fecundity and survival. Crucially, the outcome of competition between strains with different infection strategies depends on the rate of host availability; frequently available hosts favor "fast" infecting nematodes, whereas infrequently available hosts favor "slow" infecting nematodes. A simple evolutionarily stable strategy (ESS) analysis based on classic epidemiological models fails to capture this behavior, predicting instead that the fastest infecting phenotype should always dominate. However, a novel model incorporating more realistic, discrete bouts of host availability shows that strain coexistence is highly likely. Our results demonstrate that heterogeneities in host availability play a key role in the evolution of parasite life-history traits and in the maintenance of phenotypic variability. Parasite life-history strategies are likely to evolve rapidly in response to changes in host availability induced by disease management programs or by natural dynamics in host abundance. Incorporating parasite evolution in response to host availability would therefore enhance the predictive ability of current epidemiological models of infectious disease.     

Competitive interactions and persistence of two nematode species that parasitize Drosophila recens

Drosophila recens is parasitized in the wild by two nematodes, Howardula aoronymphium , a host generalist, and Parasitylenchus nearcticus , a host specialist known only from D .  recens . In order to understand how these two parasite species coexist, we compared their ability to infect and grow in D .  recens , their effects on host fecundity and survival, and whether one parasite species was competitively superior in double infections. The specialist nematode P. nearcticus had greater rates of infection and reproduction than the generalist H. aoronymphium , and completely sterilized females in single and mixed infections. The specialist was competitively superior in mixed infections, as generalist motherworms were significantly smaller than in single infections. These results suggest that P. nearcticus might competitively exclude H. aoronymphium if D. recens were the only host available. It is likely that H. aoronymphium persists in D. recens by transmission from other, more suitable host species.     

Transmission rates and adaptive evolution of pathogens in sympatric heterogeneous plant populations

Diversification in agricultural cropping patterns is widely practised to delay the build-up of virulent races that can overcome host resistance in pathogen populations. This can lead to balanced polymorphism, but the long-term consequences of this strategy for the evolution of crop pathogen populations are still unclear. The widespread occurrence of sibling species and reproductively isolated sub-species among fungal and oomycete plant pathogens suggests that evolutionary divergence is common. This paper develops a mathematical model of host-pathogen interactions using a simple framework of two hosts to analyse the influences of sympatric host heterogeneity on the long-term evolutionary behaviour of plant pathogens. Using adaptive dynamics, which assumes that sequential mutations induce small changes in pathogen fitness, we show that evolutionary outcomes strongly depend on the shape of the trade-off curve between pathogen transmission on sympatric hosts. In particular, we determine the conditions under which the evolutionary branching of a monomorphic into a dimorphic population occurs, as well as the conditions that lead to the evolution of specialist (single host range) or generalist (multiple host range) pathogen populations.     

Temporal variation and the evolution of a parasitoid foraging cue

This work details theory in which selection favors generalists in a more variable environment. Specifically, in a two-host-one-parasitoid model, temporal variation in host abundances alters the optimal searching strategy and leads to the evolution of more generalist parasitoid strategies. Consistent with empirical observations, parasitoids learn host/plant odors, and use them as a cue to search for oviposition sites. The amount of unsuccessful search time required before a parasitoid alters its searching cues (the "giving-up time") is modeled in order to understand the evolutionarily optimal giving-up times under a variety of conditions. When host abundances vary across time, a generalist parasitoid strategy evolves with short giving-up times as it is likely that the host initially favored by a parasitoid will now have a low abundance. In contrast, when populations reach stable dynamics across time, giving-up times typically evolve to longer times, i.e. parasitoids remain specialized longer. The effect of temporal fluctuations is consistent across variation caused by endogenous population interactions and, to some degree, by environmental stochasticity. The conclusions are robust in that there is a strong degree of concordance between the results of a stochastic, individual-based model and a deterministic, numerical model. As an extension, spatial variation in hosts that leads to unequal tradeoffs between generalist parasitoids and specialist parasitoids may also result in the evolution of reduced giving-up times.