Pleiotropic costs of niche expansion in the RNA bacteriophage phi 6

Natural and experimental systems have failed to universally demonstrate a trade-off between generalism and specialism. When a trade-off does occur it is difficult to attribute its cause to antagonistic pleiotropy without dissecting the genetic basis of adaptation, and few previous experiments provide these genetic data. Here we investigate the evolution of expanded host range (generalism) in the RNA virus phi6, an experimental model system allowing adaptive mutations to be readily identified. We isolated 10 spontaneous host range mutants on each of three novel Pseudomonas hosts and determined whether these mutations imposed fitness costs on the standard laboratory host. Sequencing revealed that each mutant had one of nine nonsynonymous mutations in the phi6 gene P3, important in host attachment. Seven of these nine mutations were costly on the original host, confirming the existence of antagonistic pleiotropy. In addition to this genetically imposed cost, we identified an epigenetic cost of generalism that occurs when phage transition between host types. Our results confirm the existence in phi6 of two costs of generalism, genetic and environmental, but they also indicate that the cost is not always large. The possibility for cost-free niche expansion implies that varied ecological conditions may favor host shifts in RNA viruses.     

The ‘generalism’ debate: misinterpreting the term in the empirical literature focusing on dietary breadth in insects

We here attempt to show, using three broad insect groups – Lepidoptera (mainly leaf‐chewing larval herbivores and nectar‐sucking adults), parasitic Hymenoptera (mainly endoparasitoids, especially of other insects) and aphids (sap‐sucking plant parasites) – how the terms ‘generalist’, usually equated with levels of phagy (oligo‐ and polyphagy), and ‘specialist’ (monophagy), still in widespread parlance, have often been misrepresented. Probably, the reality of generalism, be that herbivorous, predatory and parasitic, can only be demonstrated by detailed empirical field observations plus the use of high‐resolution molecular (DNA) markers, including sequencing, and thereby determining whether the organism in question is really a homogeneous species population over a wide geographical range, or rather comprises a series of morphologically similar/identical cryptic, host‐adapted specialist populations. In the case of insects, the largest group of terrestrial animals on the planet, even if it can be shown that certain species are indeed polyphagous and feed on a variety of plant hosts (herbivores) or prey species (predators and parasitoids), nevertheless, the range of these food items may be highly selective and restricted, depending on morphological–genetical (biochemical/chemical)–behavioural constraints. In the end, while some animals appear to be generalist, this situation may well be illusory. Our present recognition of the term is at best inappropriate, and at worse, inaccurate, as we demonstrate in the examples given, mostly insects. In the meantime, we suggest that the terms used should be re‐defined as four broad classes of specialism–generalism, although the apparent ‘generalism’ is itself conditional on proof following further empirical analyses.     

Comparisons of yeast florae from natural substrates and larval guts of southwestern Drosophila

Summary The yeast florae in the natural substrates of four desert and three non-desert Drosophila species were compared both qualitatively and quantatively to the yeast present in the guts of Drosophila larvae living in those substrates. The desert species breed in rotting cacti and the other Drosophila were found breeding in necrotic oranges. Larvae of one cactophilic species, D. mojavensis, and larvae of all of the species utilizing oranges (D. melanogaster, D. pseudoobscura, and D. arizonensis) were found to contain non-random samples of the yeasts available in their respective substrates. Larval preference behavior is most likely responsible for these differences. The other cactophilic Drosophila (D. nigrospiracula, D. mettleri, and D. pachea) did not exhibit significant differences when the yeast florae of their larvae and substrates were compared. Selective feeding by larvae appears to be related to the degree of polyphagy in that only larvae of polyphagous species are selective. Trade-off between generalism and specialism at two biological levels is discussed.     

Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity

Biodiversity is fundamental to both eukaryote and prokaryote ecology, yet investigations of diversity often differ markedly between the two disciplines. Host specificity - the association of organisms with only a few (specialism) or many (generalism) host species - is recognized within eukaryote ecology as a key determinant of diversity. In contrast, its implications for microbial diversity have received relatively little attention. Here we explore the relationship between microbial diversity and host specificity using marine sponge-bacteria associations. We used a replicated, hierarchical sampling design and both 16S rDNA- and rpoB-based denaturing gradient gel electrophoresis (DGGE) to examine whether three co-occurring sponges from temperate Australia -Cymbastela concentrica, Callyspongia sp. and Stylinos sp. - contained unique, specialized communities of microbes. Microbial communities varied little within each species of sponge, but variability among species was substantial. Over five seasons, the microbial community in C. concentrica differed significantly from other sponges, which were more similar to seawater. Overall, three types of sponge-associated bacteria were identified via 16S rDNA sequencing of excised DGGE bands: 'specialists'- found on only one host species, 'sponge associates'- found on multiple hosts but not in seawater, and 'generalists' from multiple hosts and seawater. Analogous to other high diversity systems, the degree of specificity of prokaryotes to host eukaryotes could have a potentially significant effect on estimates of marine microbial diversity.     

The evolution of climate tolerance in conifer‐feeding aphids in relation to their host's climatic niche

Climate adaptation has major consequences in the evolution and ecology of all living organisms. Though phytophagous insects are an important component of Earth's biodiversity, there are few studies investigating the evolution of their climatic preferences. This lack of research is probably because their evolutionary ecology is thought to be primarily driven by their interactions with their host plants. Here, we use a robust phylogenetic framework and species‐level distribution data for the conifer‐feeding aphid genus Cinara to investigate the role of climatic adaptation in the diversity and distribution patterns of these host‐specialized insects. Insect climate niches were reconstructed at a macroevolutionary scale, highlighting that climate niche tolerance is evolutionarily labile, with closely related species exhibiting strong climatic disparities. This result may suggest repeated climate niche differentiation during the evolutionary diversification of Cinara. Alternatively, it may merely reflect the use of host plants that occur in disparate climatic zones, and thus, in reality the aphid species' fundamental climate niches may actually be similar but broad. Comparisons of the aphids' current climate niches with those of their hosts show that most Cinara species occupy the full range of the climatic tolerance exhibited by their set of host plants, corroborating the hypothesis that the observed disparity in Cinara species' climate niches can simply mirror that of their hosts. However, 29% of the studied species only occupy a subset of their hosts' climatic zone, suggesting that some aphid species do indeed have their own climatic limitations. Our results suggest that in host‐specialized phytophagous insects, host associations cannot always adequately describe insect niches and abiotic factors must be taken into account.     

Ancestrality and evolution of trait syndromes in finches (Fringillidae)

Species traits have been hypothesized by one of us (Ponge, 2013) to evolve in a correlated manner as species colonize stable, undisturbed habitats, shifting from “ancestral” to “derived” strategies. We predicted that generalism, r‐selection, sexual monomorphism, and migration/gregariousness are the ancestral states (collectively called strategy A) and evolved correlatively toward specialism, K‐selection, sexual dimorphism, and residence/territoriality as habitat stabilized (collectively called B strategy). We analyzed the correlated evolution of four syndromes, summarizing the covariation between 53 traits, respectively, involved in ecological specialization, r‐K gradient, sexual selection, and dispersal/social behaviors in 81 species representative of Fringillidae, a bird family with available natural history information and that shows variability for all these traits. The ancestrality of strategy A was supported for three of the four syndromes, the ancestrality of generalism having a weaker support, except for the core group Carduelinae (69 species). It appeared that two different B‐strategies evolved from the ancestral state A, both associated with highly predictable environments: one in poorly seasonal environments, called B1, with species living permanently in lowland tropics, with “slow pace of life” and weak sexual dimorphism, and one in highly seasonal environments, called B2, with species breeding out‐of‐the‐tropics, migratory, with a “fast pace of life” and high sexual dimorphism.     

Rapid experimental shift in host use traits of a polyphagous marine herbivore reveals fitness costs on alternative hosts

The host breadth of any particular herbivore reflects a compromise between evolutionary forces that promote specialism and those that promote polyphagy. Because most terrestrial herbivorous insects specialize, explorations of this evolutionary balance have focused largely on specialist than on polyphagous herbivores. Here, we experimentally tested whether fitness-based tradeoffs in utilizing alternative hosts can be detected within a polyphagous marine herbivore. The marine amphipod Ampithoe longimana occurs on multiple seaweeds year-round (especially the genera Sargassum, Ulva and Hypnea), but is particularly abundant on the diterpene-rich genus Dictyota during warmer summer months. If fitness-based tradeoffs in using these alternative hosts are present, A. longimana may experience fluctuating selection across seasons. To test this possibility, we performed a controlled natural-selection experiment in which amphipods were isolated on Dictyota or a mixed seaweed assemblage that did not include Dictyota. Within 15 weeks (less than five overlapping generations), Dictyota-lines had greater feeding tolerance for Dictyota and its secondary metabolites than did mixed-seaweed-lines. Dictyota-line females reproduced more quickly than did mixed-seaweed-line females on Dictyota, but mixed-seaweed-line juveniles had greater growth on Sargassum and Ulva and higher fecundity on all hosts than did Dictyota-line juveniles. While experimental shifts in preference and performance are likely genetically-mediated, our experimental protocol does not preclude a role for phenotypic plasticity. The presence of a fitness cost to evolving greater preference for Dictyota suggests that fluctuating selection may operate on feeding preference across seasons, but our test of this hypothesis was equivocal. We suggest that one reason that polyphagy persists within A. longimana and potentially other marine grazers is because polyphagy broadens resource use across seasons, and this benefit outweighs the fitness-based costs that can favor specialism. Our results also reinforce the notion that timescales of ecological and evolutionary dynamics can overlap.     

Biology of Asphondyliini (Diptera: Cecidomyiidae)

The family Cecidomyiidae (Diptera) including about 6100 described species displays diverse feeding habits. The tribe Asphondyliini is a well‐circumscribed monophyletic group of Cecidomyiidae and all species are known as gall inducers. Species belonging to this tribe exhibit fascinating ecological traits such as host alternation, polyphagy, extended diapause, induction of dimorphic galls and association with fungal symbionts. For these reasons, biogeographical and phylogenetic studies of Asphondyliini are of interest in elucidating the evolution of these traits, and particularly the processes of host‐range expansion, host‐plant shift and shifts in gall‐bearing organs. In order to facilitate further evolutionary studies of Asphondyliini, I review studies of systematics, biogeography, phylogeny, speciation, cytology, behavior, ecology, physiology, biological interaction and economic importance in this tribe.     

No effect of host–parasite co‐evolution on host range expansion

Antagonistic co‐evolution between hosts and parasites (reciprocal selection for resistance and infectivity) is hypothesized to play an important role in host range expansion by selecting for novel infectivity alleles, but tests are lacking. Here, we determine whether experimental co‐evolution between a bacterium (Pseudomonas fluorescens SBW25) and a phage (SBW25Φ2) affects interstrain host range: the ability to infect different strains of P. fluorescens other than SBW25. We identified and tested a genetically and phenotypically diverse suite of co‐evolved phage variants of SBW25Φ2 against both sympatric and allopatric co‐evolving hosts (P. fluorescens SBW25) and a large set of other P. fluorescens strains. Although all co‐evolved phage had a greater host range than the ancestral phage and could differentially infect co‐evolved variants of P. fluorescens SBW25, none could infect any of the alternative P. fluorescens strains. Thus, parasite generalism at one genetic scale does not appear to affect generalism at other scales, suggesting fundamental genetic constraints on parasite adaptation for this virus.     

FLUCTUATING TEMPERATURE LEADS TO EVOLUTION OF THERMAL GENERALISM AND PREADAPTATION TO NOVEL ENVIRONMENTS

Environmental fluctuations can select for generalism, which is also hypothesized to increase organisms’ ability to invade novel environments. Here, we show that across a range of temperatures, opportunistic bacterial pathogen Serratia marcescens that evolved in fluctuating temperature (daily variation between 24°C and 38°C, mean 31°C) outperforms the strains that evolved in constant temperature (31°C). The growth advantage was also evident in novel environments in the presence of parasitic viruses and predatory protozoans, but less clear in the presence of stressful chemicals. Adaptation to fluctuating temperature also led to reduced virulence in Drosophila melanogaster host, which suggests that generalism can still be costly in terms of reduced fitness in other ecological contexts. While supporting the hypothesis that evolution of generalism is coupled with tolerance to several novel environments, our results also suggest that thermal fluctuations driven by the climate change could affect both species’ invasiveness and virulence.     

Infection with an insect virus affects olfactory behaviour and interactions with host plant and natural enemies in an aphid

Aphid ecology and population dynamics are affected by a series of factors including behavioural responses to ecologically relevant chemical cues, capacity for population growth, and interactions with host plants and natural enemies. Using the aphid Rhopalosiphum padi (L.) (Homoptera: Aphididae), we showed that these factors were affected by infection with Rhopalosiphum padi virus (RhPV). Uninfected aphids were attracted to odour of uninfected aphids on the host plant, an aggregation mechanism. However, infected aphids were not attracted, and neither infected nor uninfected aphids were attracted to infected aphids on the plant. Infected aphids did not respond to methyl salicylate, a cue denoting host suitability. Infected aphids were more behaviourally sensitive to aphid alarm pheromone, and left the host plant more readily in response to it. RhPV reduced the lifespan and population growth rate of the aphid. The predacious ladybird, Coccinella septempunctata (L.) (Coleoptera: Coccinellidae), consumed more infected aphids than uninfected aphids in a 24‐h period, and the aphid parasitoid Aphidius ervi Haliday (Hymenoptera: Aphidiidae) attacked more infected than uninfected aphids. However, the proportion of mummies formed was lower with infected aphids. The results represent further evidence that associated organisms can affect the behaviour and ecology of their aphid hosts.     

UV‐B impact on aphid performance mediated by plant quality and plant changes induced by aphids

Plants face various abiotic and biotic environmental factors and therefore need to adjust their phenotypic traits on several levels. UV‐B radiation is believed to impact herbivorous insects via host plant changes. Plant responses to abiotic challenges (UV‐B radiation) and their interaction with two aphid species were explored in a multifactor approach. Broccoli plants [Brassica oleracea L. convar. botrytis (L.), Brassicaceae] were grown in two differently covered greenhouses, transmitting either 80% (high UV‐B) or 4% (low UV‐B) of ambient UV‐B. Three‐week‐old plants were infested with either specialist cabbage aphids [Brevicoryne brassicae (L.), Sternorrhyncha, Aphididae] or generalist green peach aphids [Myzus persicae (Sulzer), Sternorrhyncha, Aphididae]. Plants grown under high‐UV‐B intensities were smaller and had higher flavonoid concentrations. Furthermore, these plants had reduced cuticular wax coverage, whereas amino acid concentrations of the phloem sap were little influenced by different UV‐B intensities. Cabbage aphids reproduced less on plants grown under high UV‐B than on plants grown under low UV‐B, whereas reproduction of green peach aphids in both plant light sources was equally poor. These results are likely related to the different specialisation‐dependent sensitivities of the two species. The aphids also affected plant chemistry. High numbers of cabbage aphid progeny on low‐UV‐B plants led to decreased indolyl glucosinolate concentrations. The induced change in these glucosinolates may depend on an infestation threshold. UV‐B radiation considerably impacts plant traits and subsequently affects specialist phloem‐feeding aphids, whereas aphid growth forces broccoli to generate specific defence responses.     

Individual Specialization to Non-Optimal Hosts in a Polyphagous Marine Invertebrate Herbivore

Factors determining the degree of dietary generalism versus specialism are central in ecology. Species that are generalists at the population level may in fact be composed of specialized individuals. The optimal diet theory assumes that individuals choose diets that maximize fitness, and individual specialization may occur if individuals'' ability to locate, recognize, and handle different food types differ. We investigate if individuals of the marine herbivorous slug Elysia viridis, which co-occur at different densities on several green macroalgal species in the field, are specialized to different algal hosts. Individual slugs were collected from three original algal host species (Cladophora sericea, Cladophora rupestris and Codium fragile) in the field, and short-term habitat choice and consumption, as well as long-term growth (proxy for fitness), on four algal diet species (the original algal host species and Chaetomorpha melagonium) were studied in laboratory experiments. Nutritional (protein, nitrogen, and carbon content) and morphological (dry weight, and cell/utricle volume) algal traits were also measured to investigate if they correlated with the growth value of the different algal diets. E. viridis individuals tended to choose and consume algal species that were similar to their original algal host. Long-term growth of E. viridis, however, was mostly independent of original algal host, as all individuals reached a larger size on the non-host C. melagonium. E. viridis growth was positively correlated to algal cell/utricle volume but not to any of the other measured algal traits. Because E. viridis feeds by piercing individual algal cells, the results indicate that slugs may receive more cytoplasm, and thus more energy per unit time, on algal species with large cells/utricles. We conclude that E. viridis individuals are specialized on different hosts, but host choice in natural E. viridis populations is not determined by the energetic value of seaweed diets as predicted by the ODT.     

Variation among individual butterflies along a generalist–specialist axis: no support for the 'neural constraint' hypothesis

Abstract 1. Degree of host specialisation was a continuous variable in a population of Edith’s checkerspot butterfly (Euphydryas editha). A novel host, Collinsia torreyi, had been added to the diet in response to anthropogenic disturbance, and then abandoned prior to the current study. Butterflies either showed no preference or preferred their traditional host, Pedicularis semibarbata. 2. Strength of preference for Pedicularis over Collinsia was measured in the field and used to estimate host specialisation of individual butterflies. Efficiency was estimated from the times taken by each insect to perform two tasks: (i) identification of a Pedicularis plant as a host, and (ii) successful initiation of oviposition after the decision to do so had been made. 3. There was no clear trend for association between host specialisation and either measure of efficiency. Generalists were not slower than specialists at identifying Pedicularis as a host or at handling it after deciding to oviposit. 4. Prior work indicated that generalists paid no detectable cost in terms of reduced discrimination among individuals of their preferred host species. 5. In contrast to other species, generalist E. editha paid in neither time nor accuracy. Why then does the diet not expand? Behavioural adaptations to the traditional host caused maladaptations to the novel host and generated short‐term constraints to evolutionary expansion of diet breadth. To date, however, no long‐term constraints have been found in this system. In those traits investigated to date, increased adaptation to the novel host has not caused reduced adaptation to the traditional host.     

Evidence of weak habitat specialisation in microscopic animals

Macroecology and biogeography of microscopic organisms (any living organism smaller than 2 mm) are quickly developing into fruitful research areas. Microscopic organisms also offer the potential for testing predictions and models derived from observations on larger organisms due to the feasibility of performing lab and mesocosm experiments. However, more empirical knowledge on the similarities and differences between micro- and macro-organisms is needed to ascertain how much of the results obtained from the former can be generalised to the latter. One potential misconception, based mostly on anedoctal evidence rather than explicit tests, is that microscopic organisms may have wider ecological tolerance and a lower degree of habitat specialisation than large organisms. Here we explicitly test this hypothesis within the framework of metacommunity theory, by studying host specificify in the assemblages of bdelloid rotifers (animals about 350 μm in body length) living in different species of lichens in Sweden. Using several regression-based and ANOVA analyses and controlling for both spatial structure and the kind of substrate the lichen grow over (bark vs rock), we found evidence of significant but weak species-specific associations between bdelloids and lichens, a wide overlap in species composition between lichens, and wide ecological tolerance for most bdelloid species. This confirms that microscopic organisms such as bdelloids have a lower degree of habitat specialisation than larger organisms, although this happens in a complex scenario of ecological processes, where source-sink dynamics and geographic distances seem to have no effect on species composition at the analysed scale.     

Genetic architecture of resistance to aphids and mites in a willow hybrid system

Hybrid plants often differ in resistance to arthropods compared to the parental species from which they are derived. To better understand the relative contribution of genetic effects in influencing plant resistance to arthropods, we examined the genetic architecture of resistance in a willow hybrid system, Salix eriocephala, S. sericea, and their interspecific hybrids. Resistance to two arthropods, a willow leaf aphid (Chaitophorus sp.: Aphididae) and an eriophyoid mite (Aculops tetanothrix: Eriophyidae), were compared because resistance to different herbivores may be controlled by different traits and influenced by different genetic effects. We found additive and nonadditive genetic effects to be important in explaining the difference between willow species in resistance to aphids and mites. F2 hybrids exhibited low resistance to aphids, suggesting breakdown of favourable epistatic interactions that confer resistance. F2 hybrids, however, exhibited high resistance to mites, suggesting either the breakdown of interactions that affect traits used by mites in host location or the creation of favourable epistatic interactions. This study demonstrates the potential role of herbivores in affecting plant genetic structure, such that selection by herbivores can potentially lead to the creation of gene interactions that influence host resistance traits or host recognition traits used by the herbivore.     

Fruit‐breeding drosophilids (Diptera) in the Neotropics: playing the field and specialising in generalism?

1. Species of Drosophilidae are frequently used as model organisms, but their relationships with the environment, particularly in immature stages, remain poorly known. 2. This is the most comprehensive survey to date of fruit‐breeding drosophilids and their hosts in the Neotropics. Drosophilid host‐utilisation patterns were analysed as to geographic origin (native versus exotic) and level of specialisation. 3. The 180 species of plants recorded as drosophilid hosts are distributed across the main Angiosperm lineages and fleshy‐fruited orders; plant families that hosted the greatest number of drosophilid species were Arecaceae, Moraceae, and Myrtaceae. The 100 nominal drosophilid species recorded breeding in fruits belong to just over one‐third of Neotropical genera; most species (91) belong to Drosophila. Drosophilid species with the greatest resource breadth were Drosophila simulans, Drosophila nebulosa, and Zaprionus indianus. 4. Exotic drosophilids breed in more plant species than Neotropical drosophilids and use exotic hosts more frequently, possibly because they are generalists that have survived the trial of introduction and establishment in the Neotropics. Native drosophilids are more variable in resource breadth and sometimes adopt exotic hosts. 5. Amongst the 49 drosophilids with enough records for analysis (> 4), 48 were categorised as generalists. One possible explanation for such overwhelming generalism is the high diversity of Neotropical habitat or hosts. A second, non‐exclusive explanation, suggested by recent studies and empirically supported by the absence of host specialisation found in this study, is that drosophilids could be selective of the dominant yeasts and bacteria in host tissue, and not of the hosts themselves.     

Complex trait differentiation between host-populations of the pea aphid Acyrthosiphon pisum (Harris): implications for the evolution of ecological specialisation

Variation in traits affecting preference for, and performance on, new habitats is a key factor in the initiation of ecological specialisation and adaptive speciation. However, habitat and resource use also involves other traits whose influence on ecological and genetic divergence remains poorly understood. In the present study, we investigated the extent of variation of life-history traits among sympatric populations of the pea aphid Acyrthosiphon pisum , which shows several host races that are specialised on various plants of the family Fabaceae plants and is an established model for ecological speciation. First, we assessed the community structure of microbial partners within host populations of the pea aphid. The effect of these microbes on host fitness is uncertain, although there is growing evidence that they may modulate various important adaptive traits of their host such as plant utilisation and resistance against natural enemies. Second, we performed a multivariate analysis on several ecologically relevant features of host populations recorded in the present and previous studies (including microbial composition, colour morph, reproductive mode, and male dispersal phenotype), enabling the identification of correlations between phenotypic traits. We discuss the ecological significance of these associations of traits in relation to the habitat characteristics of pea aphid populations, and their consequences for the evolution of ecological specialisation and sympatric speciation.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 718–727.