Competition promotes the evolution of host generalists in obligate parasites

Ecological theory traditionally predicts that interspecific competition selects for an increase in ecological specialization. Specialization, in turn, is often thought to be an evolutionary ‘dead end,’ with specialist lineages unlikely to evolve into generalist lineages. In host–parasite systems, this specialization can take the form of host specificity, with more specialized parasites using fewer hosts. We tested the hypothesis that specialists are evolutionarily more derived, and whether competition favours specialization, using the ectoparasitic feather lice of doves. Phylogenetic analyses revealed that complete host specificity is actually the ancestral condition, with generalists repeatedly evolving from specialist ancestors. These multiple origins of generalists are correlated with the presence of potentially competing species of the same genus. A competition experiment with captive doves and lice confirmed that congeneric species of lice do, in fact, have the potential to compete in ecological time. Taken together, these results suggest that interspecific competition can favour the evolution of host generalists, not specialists, over macroevolutionary time.     

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.     

Testing the trend towards specialization in herbivore-host plant associations using a molecular phylogeny of Tomoplagia (Diptera: Tephritidae)

Herbivorous insects are abundant and diverse and insect-host plant associations tend to be specialized and evolutionarily conserved. Some authors suggested that generalist insect lineages tend to become specialists, with host specialization leading to an evolutionary dead-end for the parasite species. In this paper, we have examined this tendency using a phylogenetic tree of Tomoplagia (Diptera: Tephritidae), a parasite of asteracean plants. We have tested the trend towards specialization in different hierarchical degrees of host specialization. The topology of the tree, the inference of ancestral hosts, and the lack of directional evolution indicated that specialization does not correspond to a phylogenetic dead-end. Although most Tomoplagia species are restricted to a single host genus, specialization does not seem to limit further host range evolution. This work emphasizes the advantages of the use of different levels of specialization and the inclusion of occasional hosts to establish a more detailed scenario for the evolution of this kind of ecological association.     

Resource heterogeneity, diet shifts and intra-cohort competition: effects on size divergence in YOY fish

The pollination syndrome hypothesis has provided a major conceptual framework for how plants and pollinators interact. However, the assumption of specialization in pollination systems and the reliability of floral traits in predicting the main pollinators have been questioned recently. In addition, the relationship between ecological and evolutionary specialization in pollination interactions is still poorly understood. We used data of 62 plant species from three communities across southern Norway to test: (1) the relationships between floral traits and the identity of pollinators, (2) the association between floral traits (evolutionary specialization) and ecological generalization, and (3) the consistency of both relationships across communities. Floral traits significantly affected the identity of pollinators in the three communities in a way consistent with the predictions derived from the pollination syndrome concept. However, hover flies and butterflies visited flowers with different shapes in different communities, which we mainly attribute to among-community variation in pollinator assemblages. Interestingly, ecological generalization depended more on the community-context (i.e. the plant and pollinator assemblages in the communities) than on specific floral traits. While open yellow and white flowers were the most generalist in two communities, they were the most specialist in the alpine community. Our results warn against the use of single measures of ecological generalization to question the pollination syndrome concept, and highlight the importance of community comparisons to assess the pollination syndromes, and to understand the relationships between ecological and evolutionary specialization in plant-pollinator interactions.     

Delicious poison: genetics of Drosophila host plant preference

Insects use chemical cues to identify host plants, which suggests that chemosensory perception could be a target of natural selection during host specialization. Five papers using data from the 12 recently sequenced Drosophila genomes examined chemosensory gene function and evolution across specialist and generalist species. A functional study identifies odorant binding proteins that mediate loss of toxin avoidance in a specialist, and targeted genomic studies indicate specialists and island endemics lose chemosensory genes more rapidly than generalist and mainland relatives. Together, these studies suggest a mode of chemoreceptor evolution dominated by birth/death dynamics, coupled with a low level of potential positive selection.     

Nested diets: a novel pattern of individual-level resource use

Many generalist populations may actually be composed of relatively specialist individuals. This 'individual specialization' may have important ecological and evolutionary implications. Although this phenomenon has been documented in more than one hundred taxa, it is still unclear how individuals within a population actually partition resources. Here we applied several methods based on network theory to investigate the intrapopulation patterns of resource use in the gracile mouse opossum Gracilinanus microtarsus . We found evidence of significant individual specialization in this species and that the diets of specialists are nested within the diets of generalists. This novel pattern is consistent with a recently proposed model of optimal foraging and implies strong asymmetry in the interactions among individuals of a population.     

Variation in the degree of specialization can maintain local diversity in model communities

We hypothesize that the continuum between generalist and specialist adaptations is an important general trade-off axis in the maintenance of local diversity, and we explore this idea with a simple model in which there are patch types to which species arrive as propagules and compete. Each patch type is defined by a competitive ranking of all species. A highly specialist species is the top competitor in one patch type but has a relatively low average ranking across different patch types, while a generalist species has a high average rank across patch types but is not the top competitor in any patch type. We use random dispersal and vary the fecundity of all species together to vary total propagule density and therefore recruitment limitation and density-dependent mortality. When fecundity is very high, each patch becomes occupied by its specialist species and generalists go extinct, so the number of species at equilibrium is equal to the number of patch types. If fecundity is very low, generalists dominate and specialists go extinct. There is a range of fecundity levels in which specialists, generalists, and intermediates coexist, and the number of species is substantially greater than the number of patch types. While coexistence of specialists and generalists has been considered a problem in evolutionary ecology, our results suggest to the contrary that this trade-off contributes to the maintenance of local diversity.     

Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish

Patterns and likely processes connected with evolution of host specificity in congeneric monogeneans parasitizing fish species of the Cyprinidae were investigated. A total of 51 Dactylogyrus species was included. We investigated (1) the link between host specificity and parasite phylogeny; (2) the morphometric correlates of host specificity, parasite body size, and variables of attachment organs important for host specificity; (3) the evolution of morphological adaptation, that is, attachment organ; (4) the determinants of host specificity following the hypothesis of specialization on more predictable resources considering maximal body size, maximal longevity, and abundance as measures of host predictability; and (5) the potential link between host specificity and parasite diversification. Host specificity, expressed as an index of host specificity including phylogenetic and taxonomic relatedness of hosts, was partially associated with parasite phylogeny, but no significant contribution of host phylogeny was found. The mapping of host specificity into the phylogenetic tree suggests that being specialist is not a derived condition for Dactylogyrus species. The different morphometric traits of the attachment apparatus seem to be selected in connection with specialization of specialist parasites and other traits favored as adaptations in generalist parasites. Parasites widespread on several host species reach higher abundance within hosts, which supports the hypothesis of ecological specialization. When separating specialists and generalists, we confirmed the hypothesis of specialization on a predictable resource; that is, specialists with larger anchors tend to live on fish species with larger body size and greater longevity, which could be also interpreted as a mechanism for optimizing morphological adaptation. We demonstrated that ecology of host species could also be recognized as an important determinant of host specificity. The mapping of morphological characters of the attachment organ onto the parasite phylogenetic tree reveals that morphological evolution of the attachment organ is connected with host specificity in the context of fish relatedness, especially at the level of host subfamilies. Finally, we did not find that host specificity leads to parasite diversification in congeneric monogeneans.     

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.     

Origins and ecological consequences of pollen specialization among desert bees

An understanding of the evolutionary origins of insect foraging specialization is often hindered by a poor biogeographical and palaeoecological record. The historical biogeography (20,000 years before present to the present) of the desert-limited plant, creosote bush (Larrea tridentata), is remarkably complete. This history coupled with the distribution pattern of its bee fauna suggests pollen specialization for creosote bush pollen has evolved repeatedly among bees in the Lower Sonoran and Mojave deserts. In these highly xeric, floristically depauperate environments, species of specialist bees surpass generalist bees in diversity, biomass and abundance. The ability of specialist bees to facultatively remain in diapause through resource-poor years and to emerge synchronously with host plant bloom in resource-rich years probably explains their ecological dominance and persistence in these areas. Repeated origins of pollen specialization to one host plant where bloom occurs least predictably is a counter-example to prevailing theories that postulate such traits originate where the plant grows best and blooms most reliably Host-plant synchronization, a paucity of alternative floral hosts, or flowering attributes of creosote bush alone or in concert may account for the diversity of bee specialists that depend on this plant instead of nutritional factors or chemical coevolution between floral rewards and the pollinators they have evolved to attract.     

DYNAMIC TRANSMISSION,HOST QUALITY,AND POPULATION STRUCTURE IN A MULTIHOST PARASITE OF BUMBLEBEES

The evolutionary ecology of multihost parasites is predicted to depend upon patterns of host quality and the dynamics of transmission networks. Depending upon the differences in host quality and transmission asymmetries, as well as the balance between intra‐ and interspecific transmission, the evolution of specialist or generalist strategies is predicted. Using a trypanosome parasite of bumblebees, we ask how host quality and transmission networks relate to parasite population structure across host species, and thus the potential for the evolution of specialist strains adapted to different host species. Host species differed in quality, with parasite growth varying across host species. Highly asymmetric transmission networks, together with differences in host quality, likely explain local population structure of the parasite across host species. However, parasite population structure across years was highly dynamic, with parasite populations varying significantly from one year to the next within individual species at a given site. This suggests that, while host quality and transmission may provide the opportunity for short‐term host specialization by the parasite, repeated bottlenecking of the parasite, in combination with its own reproductive biology, overrides these smaller scale effects, resulting in the evolution of a generalist parasite.     

Resource predictability and specialization in avian malaria parasites

We tested the hypothesis that avian haemosporidian (malaria) parasites specialize on hosts that can be characterized as predictable resources at a site in Amazonian Ecuador. We incorporated host phylogenetic relationship and relative abundance in assessing parasite specialization, and we examined associations between parasite specialization and three host characteristics – abundance, mass and longevity – using quantile regression, phylogenetic logistic regression and t‐tests. Hosts of specialist malaria parasite lineages were on average more abundant than hosts of generalist parasite lineages, but the relationship between host abundance and parasite specialization was not consistent across analyses. We also found support for a positive association between parasite specialization and host longevity, but this also was not consistent across analyses. Nonetheless, our findings suggest that the predictability of a host resource may play a role in the evolution of specialization. However, we also discuss two alternative explanations to the resource predictability hypothesis for specialization: (i) that interspecific interactions among the parasites themselves might constrain some parasites to a specialist strategy, and (ii) that frequent encounters with multiple host species, mediated by blood‐sucking insects, might promote generalization within this system.     

The evolution and coexistence of generalist and specialist herbivores under between-plant competition

Consumer-resource models have been used extensively to study the evolution and coexistence of generalist and specialist consumers. However, current consumer-resource models do not take into account competition between resources or only incorporate intraspecific competition phenomenologically with, for example, a logistic growth function. Here, we mechanistically incorporate competition in an existing two-resource model, by introducing nutrient-limited resource growth and setting the total amount of nutrients (free or contained in consumers and resources) to a fixed value. In addition to the three combinations of generalists and specialists found in previous models, we find four other evolutionary outcomes, depending on the strength of the consumer trade-off: coexistence of one specialist and a generalist and three types of evolutionary cycling. Furthermore, which outcomes are most likely depends strongly on the combination of intrinsic growth rate of resources and the total amount of nutrients in the system. Our results suggest that the realistic assumption of nutrient competition may shed new light on the evolution of the multitude of strategies in real systems.     

Evolution of resource specialisation in competitive metacommunities

Spatial environmental heterogeneity coupled with dispersal can promote ecological persistence of diverse metacommunities. Does this premise hold when metacommunities evolve? Using a two‐resource competition model, we studied the evolution of resource‐uptake specialisation as a function of resource type (substitutable to essential) and shape of the trade‐off between resource uptake affinities (generalist‐ to specialist‐favouring). In spatially homogeneous environments, evolutionarily stable coexistence of consumers is only possible for sufficiently substitutable resources and specialist‐favouring trade‐offs. Remarkably, these same conditions yield comparatively low diversity in heterogeneous environments, because they promote sympatric evolution of two opposite resource specialists that, together, monopolise the two resources everywhere. Consumer diversity is instead maximised for intermediate trade‐offs and clearly substitutable or clearly essential resources, where evolved metacommunities are characterised by contrasting selection regimes. Taken together, our results present new insights into resource‐competition‐mediated evolutionarily stable diversity in homogeneous and heterogeneous environments, which should be applicable to a wide range of systems.     

IS SPECIALIZATION A DEAD END? THE PHYLOGENY OF HOST USE IN DENDROCTONUS BARK BEETLES (SCOLYTIDAE)

Ecological explanations for the prevalence of resource specialists are abundant, whereas phylogenetic evidence on their origins is scarce. In this paper, we provide a molecular phylogenetic study of the 19 specialist or generalist species in the bark beetle genus Dendroctonus, which collectively attack species in four different genera in the conifer family Pinaceae. Given substantial variation in diet breadth, we asked two general questions concerning the evolution of resource use in this group. How conservative is the evolution of host use in these insects? Does specialization tend to be derived (i.e., a “dead end”)? To answer these questions, we estimated the phylogeny of Dendroctonus using mitochondrial DNA sequences and mapped transitions in resource use on the resulting phylogeny estimate. The evolution of affiliations with Pinus and Picea hosts in Dendroctonus was conservative among beetle species (PTP test; P < 0.012), but there was no significant correspondence between the phylogeny of these beetles and the phylogeny among their Pinaceae hosts (among genera, P = 0.28; among Pinus species, P = 0.82). Degree of specialization, as measured in the proportion of hosts used, was bimodally distributed with “generalist” species utilizing < 60% of the congeneric hosts within their range and six specialist species utilizing < 40% of the available hosts. Among the generalists, we found a strong correlation between the number of hosts encountered and the number of hosts utilized (R = 0.97, P < 0.0001), whereas there was no significant correlation among the specialists (R = 0.27, P = 0.59). The evolution of specialization in Dendroctonus proved highly labile—specialists arose from generalists at least six separate times (without reversal) all in derived positions, and closer examination of some specialists revealed instances where they appear to have lost particular host species from their diet. However, evidence from the ecological literature also suggests that several Dendroctonus generalists may have increased their range of host genera within the Pinaceae.     

Host specialization in habitat specialists and generalists

Generalists and specialists use different cues to find their habitat and essential resources. While generalists have the advantage of exploiting a wider range of resources, they are predicted to be less efficient in using one particular resource compared to specialists. The level of specialization of parasitoids can be either at the habitat or at the host level; strategies used by either type are expected to differ. We examined interactions between three aphid parasitoid species that are a habitat specialist Aphidius rhopalosiphi, a habitat generalist Aphidius ervi, and a host generalist Praon volucre on three cereal aphids, Sitobion avenae, Metopolophium dirhodum and Rhopalosiphum padi. We compared total parasitism rate across behavioral and physiological variation in a non-choice test. Next, we addressed total parasitism in two phases to examine: (1) the response of parasitoids to different hosts through the behavioral sequence from antennation through oviposition, and (2) the physiological suitability of different hosts for oviposition and larval development. Parasitization typically involved the following behavioral steps: (1) antennal contact, (2) abdominal bending, and (3) ovipositor insertion (acceptance). A. rhopalosiphi had the same number of antennal contacts with the three aphids but showed fewer instances of abdominal bending towards R. padi. Pre-contact host preference was found for A. ervi but it did not correspond to the level of acceptance. The number of antennal contacts by P. volucre corresponded to the parasitization level of the aphid species but more mummies were produced on M. dirhodum than on R. padi. These results suggest that parasitoid species that are habitat specialists react similarly to the different host species present in the same habitat, whereas generalist species exhibit clear preferences during host selection. Preferences were, however, not always related to host suitability.     

Adaptive change in the resource-exploitation traits of a generalist consumer: the evolution and coexistence of generalists and specialists

Mathematical models of consumer-resource systems are used to explore the evolution of traits related to resource acquisition in a generalist consumer species that is capable of exploiting two resources. The analysis focuses on whether evolution of traits determining the capture rates of two resources by a consumer species produce one generalist, two specialists, or all three types, when all types are characterized by a common fitness function. In systems with a stable equilibrium, evolution produces one generalist or two specialists, depending on the second derivative of the trade-off relationship. When there are sustained population fluctuations, the nature of the trade-off between the consumer's capture rates of the two resources still plays a key role in determining the evolutionary outcome. If the trade-off is described by a choice variable between zero and one that is raised to a power n, polymorphic states are possible when n > 1, which implies a positive second derivative of the curve. These states are either dimorphism, with two relatively specialized consumer types, or trimorphism, with a single generalist type and two specialists. Both endogenously driven consumer-resource cycles, and fluctuations driven by an environmental variable affecting resource growth are considered. Trimorphic evolutionary outcomes are relatively common in the case of endogenous cycles. In contrast to a previous study, these trimorphisms can often evolve even when new lineages are constrained to have phenotypes very similar to existing lineages. Exogenous cycles driven by environmental variation in resource growth rates appear to be much less likely to produce a mixture of generalists and specialists than are endogenous consumer-resource cycles.     

Comparison of the ecology and evolution of plants with a generalist bird pollination system between continents and islands worldwide

Thousands of plant species worldwide are dependent on birds for pollination. While the ecology and evolution of interactions between specialist nectarivorous birds and the plants they pollinate is relatively well understood, very little is known on pollination by generalist birds. The flower characters of this pollination syndrome are clearly defined but the geographical distribution patterns, habitat preferences and ecological factors driving the evolution of generalist‐bird‐pollinated plant species have never been analysed. Herein I provide an overview, compare the distribution of character states for plants growing on continents with those occurring on oceanic islands and discuss the environmental factors driving the evolution of both groups. The ecological niches of generalist‐bird‐pollinated plant species differ: on continents these plants mainly occur in habitats with pronounced climatic seasonality whereas on islands generalist‐bird‐pollinated plant species mainly occur in evergreen forests. Further, on continents generalist‐bird‐pollinated plant species are mostly shrubs and other large woody species producing numerous flowers with a self‐incompatible reproductive system, while on islands they are mostly small shrubs producing fewer flowers and are self‐compatible. This difference in character states indicates that diverging ecological factors are likely to have driven the evolution of these groups: on continents, plants that evolved generalist bird pollination escape from pollinator groups that tend to maintain self‐pollination by installing feeding territories in single flowering trees or shrubs, such as social bees or specialist nectarivorous birds. This pattern is more pronounced in the New compared to the Old World. By contrast, on islands, plants evolved generalist bird pollination as an adaptation to birds as a reliable pollinator group, a pattern previously known from plants pollinated by specialist nectarivorous birds in tropical mountain ranges. Additionally, I discuss the evolutionary origins of bird pollination systems in comparison to systems involving specialist nectarivorous birds and reconstruct the bird pollination system of Hawaii, which may represent an intermediate between a specialist and generalist bird pollination system. I also discuss the interesting case of Australia, where it is difficult to distinguish between specialist and generalist bird pollination systems.     

Unifying concepts and mechanisms in the specificity of plant-enemy interactions

Host ranges are commonly quantified to classify herbivores and plant pathogens as either generalists or specialists. Here, we summarize patterns and mechanisms in the interactions of plants with these enemies along different axes of specificity. We highlight the many dimensions within which plant enemies can specify and consider the underlying ecological, evolutionary and molecular mechanisms. Host resistance traits and enemy effectors emerge as central players determining host utilization and thus host range. Finally, we review approaches to studying the causes and consequences of variation in the specificity of plant-enemy interactions. Knowledge of the molecular mechanisms that determine host range is required to understand host shifts, and evolutionary transitions among specialist and generalist strategies, and to predict potential host ranges of pathogens and herbivores.     

Experimental demography and the vital rates of generalist and specialist insect herbivores on native and novel host plants

1. Colonization success of species when confronted with novel environments is of interest in ecological, evolutionary and conservation contexts. Such events may represent the first step for ecological diversification. They also play an important role in adaptive divergence and speciation. 2. A species that is able to do well across a range of environments has a higher plasticity than one whose success is restricted to a single or few environments. The breadth of environments in which a species can succeed is ultimately determined by the full pattern of its vital rates in each environment. 3. Examples of organisms colonizing novel environments are insect herbivores expanding their diets to novel host plants. One expectation for insect herbivores is that species with specialized diets may display less plasticity when faced with novel hosts than generalist species. 4. We examine this hypothesis for two generalist and two specialist neotropical beetles (genus Cephaloleia: Chrysomelidae) currently expanding their diets from native to novel plants of the order Zingiberales. Using an experimental approach, we estimated changes in vital rates, life-history traits and lifetime fitness for each beetle species when feeding on native or novel host plants. 5. We did not find evidence supporting more plasticity for generalists than for specialists. Instead, we found similar patterns of survival and fecundity for all herbivores. Larvae survived worse on novel hosts; adults survived at least as well or better, but reproduced less on the novel host than on natives. 6. Some of the novel host plants represent challenging environments where population growth was negative. However, in four novel plant-herbivore interactions, instantaneous population growth rates were positive. 7. Positive instantaneous population growth rates during initial colonization of novel host plants suggest that both generalist and specialist Cephaloleia beetles may be pre-adapted to feed on some novel hosts. This plasticity in host use is a key factor for successful colonization of novel hosts. Future success or failure in the colonization of these novel hosts will depend on the demographic rates described in this research, natural selection and the evolutionary responses of life-history traits in novel environments.