Vertically transmitted viral endosymbionts of insects: do sigma viruses walk alone?

Insects are host to a wide range of vertically transmitted bacterial endosymbionts, but we know relatively little about their viral counterparts. Here, we discuss the vertically transmitted viral endosymbionts of insects, firstly examining the diversity of this group, and then focusing on the well-studied sigma viruses that infect dipterans. Despite limited sampling, evidence suggests that vertically transmitted viruses may be common in insects. Unlike bacteria, viruses can be transmitted through sperm and eggs, a trait that allows them to rapidly spread through host populations even when infection is costly to the host. Work on Drosophila melanogaster has shown that sigma viruses and their hosts are engaged in a coevolutionary arms race, in which the spread of resistance genes in the host population is followed by the spread of viral genotypes that can overcome host resistance. In the long-term, associations between sigma viruses and their hosts are unstable, and the viruses persist by occasionally switching to new host species. It therefore seems likely that viral endosymbionts have major impacts on the evolution and ecology of insects.     

When do parasites fail to speciate in response to host speciation?

Cospeciation generally increases the similarity between host and parasite phylogenies. Incongruence between host and parasite phylogenies has previously been explained in terms of host switching, sorting, and duplication events. Here, we describe an additional process, failure of the parasite to speciate in response to host speciation, that may be important in some host-parasite systems. Failure to speciate is likely to occur when gene flow among parasite populations is much higher than that of their hosts. We reconstructed trees from mitochondrial and nuclear DNA sequences for pigeons and doves (Aves: Columbiformes) and their feather lice in the genus Columbicola (Insecta: Phthiraptera). Although comparisons of the trees from each group revealed a significant amount of cospeciation, there was also a significant degree of incongruence. Cophylogenetic analyses generally indicated that host switching may be an important process in the history of this host-parasite association. Using terminal sister taxon comparisons, we also identified three apparent cases where the host has speciated but the associated parasite has not. In two of these cases of failure to speciate, these comparisons involve allopatric sister taxa of hosts whose lice also occur on hosts sympatric with both of the allopatric sisters. These additional hosts for generalist lice may promote gene flow with lice on the allopatric sister species. Relative rate comparisons for the mitochondrial cytochrome oxidase I gene indicate that molecular substitution occurs about 11 times faster in lice than in their avian hosts.     

A test of the sympatric host race formation hypothesis in Neodiprion (Hymenoptera: Diprionidae)

Theory suggests that sympatric speciation is possible; however, its prevalence in nature remains unknown. Because Neodiprion sawflies are host specialists and mate on their hosts, sympatric speciation via host shifts may be common in this genus. Here, we test this hypothesis using near-complete taxonomic sampling of a species group, comprehensive geographical and ecological data, and multiple comparative methods. Host-use data suggest that host shifts contributed to the evolution of reproductive isolation in Neodiprion and previous work has shown that gene flow accompanied divergence. However, geographical data provide surprisingly little support for the hypothesis that host shifts occurred in sympatry. While these data do not rule out sympatric host race formation in Neodiprion, they suggest that this speciation mode is uncommon in the genus and possibly in nature.     

Host specificity of a generalist parasite: genetic evidence of sympatric host races in the seabird tick Ixodes uriae

Due to the close association between parasites and their hosts, many ‘generalist’ parasites have a high potential to become specialized on different host species. We investigated this hypothesis for a common ectoparasite of seabirds, the tick Ixodes uriae that is often found in mixed host sites. We examined patterns of neutral genetic variation between ticks collected from Black‐legged kittiwakes (Rissa tridactyla) and Atlantic puffins (Fratercula arctica) in sympatry. To control for a potential distance effect, values were compared to differences among ticks from the same host in nearby monospecific sites. As predicted, there was higher genetic differentiation between ticks from different sympatric host species than between ticks from nearby allopatric populations of the same host species. Patterns suggesting isolation by distance were found among tick populations of each host group, but no such patterns existed between tick populations of different hosts. Overall, results suggest that host‐related selection pressures have led to the specialization of I. uriae and that host race formation may be an important diversifying mechanism in parasites.     

Host phylogeny determines viral persistence and replication in novel hosts

Pathogens switching to new hosts can result in the emergence of new infectious diseases, and determining which species are likely to be sources of such host shifts is essential to understanding disease threats to both humans and wildlife. However, the factors that determine whether a pathogen can infect a novel host are poorly understood. We have examined the ability of three host-specific RNA-viruses (Drosophila sigma viruses from the family Rhabdoviridae) to persist and replicate in 51 different species of Drosophilidae. Using a novel analytical approach we found that the host phylogeny could explain most of the variation in viral replication and persistence between different host species. This effect is partly driven by viruses reaching a higher titre in those novel hosts most closely related to the original host. However, there is also a strong effect of host phylogeny that is independent of the distance from the original host, with viral titres being similar in groups of related hosts. Most of this effect could be explained by variation in general susceptibility to all three sigma viruses, as there is a strong phylogenetic correlation in the titres of the three viruses. These results suggest that the source of new emerging diseases may often be predictable from the host phylogeny, but that the effect may be more complex than simply causing most host shifts to occur between closely related hosts.     

Population structure of a vector‐borne plant parasite

Parasites are among the most diverse groups of life on Earth, yet complex natural histories often preclude studies of their speciation processes. The biology of parasitic plants facilitates in situ collection of data on both genetic structure and the mechanisms responsible for that structure. Here, we studied the role of mating, dispersal and establishment in host race formation of a parasitic plant. We investigated the population genetics of a vector‐borne desert mistletoe (Phoradendron californicum) across two legume host tree species (Senegalia greggii and Prosopis velutina) in the Sonoran desert using microsatellites. Consistent with host race formation, we found strong host‐associated genetic structure in sympatry, little genetic variation due to geographic site and weak isolation by distance. We hypothesize that genetic differentiation results from differences in the timing of mistletoe flowering by host species, as we found initial flowering date of individual mistletoes correlated with genetic ancestry. Hybrids with intermediate ancestry were detected genetically. Individuals likely resulting from recent, successful establishment events following dispersal between the host species were detected at frequencies similar to hybrids between host races. Therefore, barriers to gene flow between the host races may have been stronger at mating than at dispersal. We also found higher inbreeding and within‐host individual relatedness values for mistletoes on the more rare and isolated host species (S. greggii). Our study spanned spatial scales to address how interactions with both vectors and hosts influence parasitic plant structure with implications for parasite virulence evolution and speciation.     

Socially acquired host-specific mimicry and the evolution of host races in Horsfield's bronze-cuckoo Chalcites basalis

Coevolution between parasites and their hosts typically leads to increasing specialization on host species by the parasite. Where multiple hosts are parasitized, specialization on each host can result in genetic divergence within the parasite population to create host races, and, ultimately, new species. We investigate how host-specific traits arise in Horsfield's bronze-cuckoo Chalcites basalis nestlings. Newly hatched cuckoos evict host young from the nest, yet in the absence of a model they accurately mimic the different begging calls of a primary host (superb fairy-wren, Malurus cyaneus) and a secondary host (buff-rumped thornbill, Acanthiza reguloides). Using cross-fostering experiments, we show that begging calls are modified after parasitism, through experience. Further, we demonstrate the mechanism by which mimetic calls are acquired. All cuckoo nestlings initially produced the call of their primary host. When cross-fostered as eggs to a secondary host, calls increased in variability and were rapidly modified to resemble those of the secondary host through shaping by host parents. We suggest that plasticity in the development of host-specific traits after parasitism is likely to reduce selection for host race formation.     

Recent evolution of host-associated divergence in the seabird tick Ixodes uriae

Ecological interactions are an important source of rapid evolutionary change and thus may generate a significant portion of novel biodiversity. Such changes may be particularly prevalent in parasites, where hosts can induce strong selection for adaptation. To understand the relative frequency at which host-associated divergences occur, it is essential to examine the evolutionary history of the divergence process, particularly when it is occurring over large geographical scales where both geographical and host-associated isolation may playa part. In this study, we use population genetics and phylogeography to study the evolutionary history of host-associated divergence in the seabird tick Ixodes uriae (Acari, Ixodidae). We compare results from microsatellite markers that reflect more ecological timescales with a conserved mitochondrial gene (COIII) that reflects more ancient divergence events. Population structure based on microsatellites showed clear evidence of host-associated divergence in all colonies examined. However, isolated populations of the same host type did not always group together in overall analyses and the genetic differentiation among sympatric host races was highly variable. In contrast, little host or geographical structure was found for the mitochondrial gene fragment. These results suggest that host race formation in I. uriae is a recent phenomenon, that it may have occurred several times and that local interactions are at different points in the divergence process. Rapid divergence in I. uriae implies a strong interaction with its local host species, an interaction that will alter the ecological dynamics of the system and modify the epidemiological landscape of circulating micropathogens.     

Host choice promotes reproductive isolation between host races of the larch budmoth Zeiraphera diniana

The chances for sympatric speciation are improved if ecological divergence leads to assortative mating as a by-product. This effect is known in parasites that find mates using host cues, but studies of larch- and pine-feeding races of the larch budmoth (Zeiraphera diniana, Lepidoptera: Tortricidae) suggest it may also occur when mate attraction is via sex pheromones that are independent of habitat. We have previously shown that females releasing pheromones on or near their own host attract more males of their own race than if placed on the alternative host. This host effect would enhance assortative mating provided adults preferentially alight on their native hosts. Here we investigate alighting preferences in natural mixed forest using a novel likelihood analysis of genotypic clusters based on three semidiagnostic allozyme loci. Both larch and pine females show a realized alighting preference for their own host of 86%. The equivalent preferences of males were 79% for the larch race and 85% for the pine race. These preferences are also detectable in small-scale laboratory experiments, where alighting preferences of larch and pine races towards their own hosts were, respectively, 67 and 66% in females and 69 and 63% in males. Pure larch race moths reared in the laboratory had alighting choice similar to moths from natural populations, while hybrids were intermediate, showing that alighting preferences were heritable and approximately additive. The field estimates of alighting preference, coupled with earlier work on mate choice, yield an estimated rate of natural hybridization between sympatric host races of 2.2-3.8% per generation. Divergent alighting choice enhances pheromone-mediated assortative mating today, and is likely to have been an important cause of assortative mating during initial divergence in host use. Because resources are normally 'coarse-grained' in space and time, assortative mating due to ecological divergence may be a more important catalyst of sympatric speciation than generally realized.     

Asymmetry in host and parasitoid diffuse coevolution: when the red queen has to keep a finger in more than one pie

BACKGROUND: Coevolution between pairs of antagonistic species is generally considered an endless "arms race" between attack and defense traits to counteract the adaptive responses of the other species. PRESENTATION OF THE HYPOTHESIS: When more than two species are involved, diffuse coevolution of hosts and parasitoids could be asymmetric because consumers can choose their prey whereas preys do not choose their predator. This asymmetry may lead to differences in the rate of evolution of the antagonistic species in response to selection. The more long-standing the coevolution of a given pair of antagonistic populations, the higher should be the fitness advantage for the consumer. Therefore, the main prediction of the hypothesis is that the consumer trophic level is more likely to win the coevolution race. TESTING THE HYPOTHESIS: We propose testing the asymmetry hypothesis by focusing on the tritrophic system plant/aphid/aphid parasitoid. The analysis of the genetic variability in the virulence of several parasitoid populations and in the defenses of several aphid species or several clones of the same aphid species could be compared. Moreover, the analysis of the neutral population genetic structure of the parasitoid as a function of the aphid host, the plant host and geographic isolation may complement the detection of differences between host and parasitoid trophic specialization. IMPLICATIONS OF THE HYPOTHESIS: Genetic structures induced by the arms race between antagonistic species may be disturbed by asymmetry in coevolution, producing neither rare genotype advantages nor coevolutionary hotspots. Thus this hypothesis profoundly changes our understanding of coevolution and may have important implications in terms of pest management.     

ALLOZYME AND MORPHOLOGICAL DIFFERENTIATION OF MOUNTAIN PINE BEETLES DENDROCTONUS PONDEROSAE HOPKINS (COLEOPTERA: SCOLYTIDAE) ASSOCIATED WITH HOST TREE

The purpose of this study was to determine whether mountain pine beetles utilizing different host species were differentiated for either morphological or protein variation. Genetic differentiation among host species has been reported for the southern pine beetle, the Douglas-fir beetle, the jeffrey pine beetle, and the mountain pine beetle. However, in these studies, the host trees were sampled at separate sites, and hence geographic variation and variation due to host tree were confounded. The mountain pine beetle occasionally utilizes three host trees (ponderosa pine, lodgepole pine, and limber pine) at single sites in Colorado. Five polymorphic enzyme loci and six morphological characters were used to describe beetles resident in different hosts. Differentiation within a site among host trees was detected at two of five polymorphic proteins, and for both size and morphological shape. The magnitude of genetic differentiation among hosts within a site was approximately equivalent to the magnitude of differentiation among sites. These data suggest that the species of host tree may be an important biotic factor associated with the genetic structure of bark beetle communities. The results are discussed in terms of their potential role in the process of speciation by host race formation.     

Infection success in novel hosts: an experimental and phylogenetic study of Drosophila-parasitic nematodes

Surprisingly little is known about what determines a parasite's host range, which is essential in enabling us to predict the fate of novel infections. In this study, we evaluate the importance of both host and parasite phylogeny in determining the ability of parasites to infect novel host species. Using experimental lab assays, we infected 24 taxonomically diverse species of Drosophila flies (Diptera: Drosophilidae) with five different nematode species (Tylenchida: Allantonematidae: Howardula, Parasitylenchus), and measured parasite infection success, growth, and effects on female host fecundity (i.e., virulence). These nematodes are obligate parasites of mushroom-feeding Drosophila, particularly quinaria and testacca group species, often with severe fitness consequences on their hosts. We show that the potential host ranges of the nematodes are much larger than their actual ranges, even for parasites with only one known host species in nature. Novel hosts that are distantly related from the native host are much less likely to be infected, but among more closely related hosts, there is much variation in susceptibility. Potential host ranges differ greatly between the related parasite species. All nematode species that successfully infected novel hosts produced infective juveniles in these hosts. Most novel infections did not result in significant reductions in the fecundity of female hosts, with one exception: the host specialist Parasitylenchus nearcticus sterilized all quinaria group hosts, only one of which is a host in nature. The large potential host ranges of these parasites, in combination with the high potential for host colonization due to shared mushroom breeding sites, explain the widespread host switching observed in comparisons of nematode and Drosophila phylogenies.     

The coevolutionary dynamics of obligate ant social parasite systems--between prudence and antagonism

In this synthesis we apply coevolutionary models to the interactions between socially parasitic ants and their hosts. Obligate social parasite systems are ideal models for coevolution, because the close phylogenetic relationship between these parasites and their hosts results in similar evolutionary potentials, thus making mutual adaptations in a stepwise fashion especially likely to occur. The evolutionary dynamics of host-parasite interactions are influenced by a number of parameters, for example the parasite's transmission mode and rate, the genetic structure of host and parasite populations, the antagonists' migration rates, and the degree of mutual specialisation. For the three types of obligate ant social parasites, queen-tolerant and queen-intolerant inquilines and slavemakers, several of these parameters, and thus the evolutionary trajectory, are likely to differ. Because of the fundamental differences in lifestyle between these social parasite systems, coevolution should further select for different traits in the parasites and their hosts. Queen-tolerant inquilines are true parasites that exert a low selection pressure on their host, because of their rarity and the fact that they do not conduct slave raids to replenish their labour force. Due to their high degree of specialisation and the potential for vertical transmission, coevolutionary theory would predict interactions between these workerless parasites and their hosts to become even more benign over time. Queen-intolerant inquilines that kill the host queen during colony take-over are best described as parasitoids, and their reproductive success is limited by the existing worker force of the invaded host nest. These parasites should therefore evolve strategies to best exploit this fixed resource. Slavemaking ants, by contrast, act as parasites only during colony foundation, while their frequent slave raids follow a predator prey dynamic. They often exploit a number of host species at a given site, and theory predicts that their associations are best described in terms of a highly antagonistic coevolutionary arms race.     

Evolutionary history of nematodes associated with sweat bees

Organisms that live in close association with other organisms make up a large part of the world’s diversity. One driver of this diversity is the evolution of host-species specificity, which can occur via reproductive isolation following a host-switch or, given the correct circumstances, via cospeciation. In this study, we explored the diversity and evolutionary history of Acrostichus nematodes that are associated with halictid bees in North America. First, we conducted surveys of bees in Virginia, and found six halictid species that host Acrostichus. To test the hypothesis of cospeciation, we constructed phylogenetic hypotheses of Acrostichus based on three genes. We found Acrostichus puri and Acrostichus halicti to be species complexes comprising cryptic, host-specific species. Although several nodes in the host and symbiont phylogenies were congruent and tests for cospeciation were significant, the host’s biogeography, the apparent patchiness of the association across the host’s phylogeny, and the amount of evolution in the nematode sequence suggested a mixture of cospeciation, host switching, and extinction events instead of strict cospeciation. Cospeciation can explain the relationships between Ac. puri and its augochlorine hosts, but colonization of Halictus hosts is more likely than cospeciation. The nematodes are vertically transmitted, but sexual transmission is also likely. Both of these transmission modes may explain host-species specificity and congruent bee and nematode phylogenies. Additionally, all halictid hosts come from eusocial or socially polymorphic lineages, suggesting that sociality may be a factor in the suitability of hosts for Acrostichus.     

The influence of oviposition phenology on survival in host races of Eurosta solidaginis

Phenological differences between host plants can contribute to allochronic isolation of host races of phytophagous insects. Host races of the gallmaking fly, Eurosta solidaginis, that live on different species of goldenrod (Solidago altissima and S. gigantea) exhibit different emergence phenologies. These differences could result from adaptation to corresponding phenological differences between the hosts in periods of optimal suitability for gall formation and survival to adulthood. In order to test this, some flies of each host race were allowed to emerge naturally while the emergence times of others were manipulated to correspond to the emergence and oviposition periods of the other host race. Percent gall formation and survival to adulthood were examined for three oviposition periods: the peak time of emergence and oviposition of the earlier-emerging host race (that from S. gigantea), that of the later-emerging host race (that from S. altissima), and a week after the peak emergence of the host race from S. altissima. Flies of both host races were allowed to ovipuncture plants of the appropriate species during each of these periods. Plant relative growth rates were measured during each of these periods. The experiment was repeated twice over a two-year period. Relative growth rates of both host species were highest during the earliest oviposition period (the period during which the host race from S. gigantea normally emerges). Percent gall formation was significantly correlated with plant relative growth rate, but the coefficient of determination was low. In both years of the study, percent gall formation of both host races was highest during the earliest oviposition period (the period during which the host race from S. gigantea normally oviposits). Likewise, percent survival to adulthood in both host races was highest during the earliest oviposition period. There was no significant effect of oviposition period on the percent of larval death due to parasitism by Eurytoma gigantea or predation by Mordellistena unicolor. These results suggest that the host race from S. altissima does not emerge at the time that its host is optimally suited for gall formation or survival to adulthood. Therefore, differences in emergence phenologies do not appear to be due to corresponding phenological differences between the host species in suitability for gall formation or survival to adulthood.     

Relationships between parasite abundance and the taxonomic distance among a parasite's host species: an example with fleas parasitic on small mammals

Opportunistic parasite species, capable of exploiting several different host species, do not achieve the same abundance on all these hosts. Parasites achieve maximum abundance on their principal host species, and lower abundances on their auxiliary host species. Taxonomic relatedness between the principal and auxiliary host species may determine what abundance a parasite can achieve on its auxiliary hosts, as relatedness should reflect similarities among host species in ecological, physiological and/or immunological characters. We tested this hypothesis with fleas (Siphonaptera) parasitic on small Holarctic mammals. We determined whether the abundance of a flea in its auxiliary hosts decreases with increasing taxonomic distance of these hosts from the principal host. Using data on 106 flea species from 23 regions, for a total of 194 flea-locality combinations, we found consistent support for this relationship, both within and across regions, and even after controlling for the potentially confounding effect of flea phylogeny. These results are most likely explained by a decrease in the efficiency of the parasite's evasive mechanisms against the host's behavioural and immune defences with increasing taxonomic distance from the principal host. Our findings suggest that host switching over evolutionary time may be severely constrained by the coupling of parasite success with the relatedness between new hosts and the original host.     

The life-history impact and implications of multiple parasites for bumble bee queens

Most studies of the consequences of parasitism on fitness have examined single host–parasite systems. However, parasitological studies show that most hosts are constantly challenged by a complex parasite community. Thus, neither the response of hosts to individual parasite species nor the individual impact of these parasite species is likely to be as unconstrained as studies of single host–parasite systems might suggest. In this study, the parasite community structure in spring queens of the common European bumble bee, Bombus pratorum, was assessed. By capturing queens and allowing them to rear colonies in the laboratory, the relative impact of different parasite species on fitness across the annual host life-cycle could be examined. Of 160 queens, 67% were parasitised by one or more members of a five-species parasite community. The impact of parasites varied from being highly virulent to undetectable under benign laboratory conditions. The majority of multi-parasite infections involved a high impact parasite, which resulted in the removal of associated parasites from the host population. This study shows that, whilst multiple infections occur within individual hosts, most parasites act individually on their hosts. However, multiple parasite species in the host population may constrain the host population’s ability to adapt to single parasite species.     

Visual mimicry of host nestlings by cuckoos

Coevolution between antagonistic species has produced instances of exquisite mimicry. Among brood-parasitic cuckoos, host defences have driven the evolution of mimetic eggs, but the evolutionary arms race was believed to be constrained from progressing to the chick stage, with cuckoo nestlings generally looking unlike host young. However, recent studies on bronze-cuckoos have confounded theoretical expectations by demonstrating cuckoo nestling rejection by hosts. Coevolutionary theory predicts reciprocal selection for visual mimicry of host young by cuckoos, although this has not been demonstrated previously. Here we show that, in the eyes of hosts, nestlings of three bronze-cuckoo species are striking visual mimics of the young of their morphologically diverse hosts, providing the first evidence that coevolution can select for visual mimicry of hosts in cuckoo chicks. Bronze-cuckoos resemble their own hosts more closely than other host species, but the accuracy of mimicry varies according to the diversity of hosts they exploit.     

Nestedness in riverine mussel communities: patterns across sites and fish hosts

The pattern of nestedness, where species present in depauperate locations are subsets of species present in locations with higher species diversity, is often found in ecological communities. Mussel communities examined in four rivers in the upper Tennessee River basin appeared significantly nested. Mussel species distributions were mostly unrelated to differences in immigration and only weakly related to downstream direction, giving some indication of structuring by differences in extinction. Mussel species distributions were not related to the number of fish species used as hosts for mussel larvae. Mussel species were more likely to overlap on common fish hosts; however, the host‐use matrix was not nested – groups of mussel species used different sets of host fish species in a pattern that appeared phylogenetically related. Sites with high fish host abundance may support high mussel diversity by promoting the survival of mussel species that are less able to attract and infect hosts. Thus, nestedness in freshwater mussel communities may be driven by the array of host fish resources, combined with differences in species’ abilities to use fish hosts. An understanding of the nested pattern in this region can aid conservation of this imperiled fauna.     

Parasite-driven extinction in spatially explicit host-parasite systems

General host-parasite theory suggests that parasites may be implicated in the extinction of their hosts by causing instability that leads to increased risk of stochastic extinction. In contrast, spatially explicit models suggest that the parasite may directly drive the host population to extinction. Here we examine the ecological characteristics of host-parasite interactions that favor parasite-driven host extinction. Pair approximations and simulations show that parasites only drive their hosts to extinction when they significantly reduce host reproduction. As a matter of interest, parasites that have a relatively small effect on host death rate are more likely to cause host extinction. Parasite-driven host extinction occurs at any population size, whereas extinction caused by stochastic effects is less likely to occur in large host populations. Populations may therefore be under threat from parasites that stop host reproduction, and this type of parasite may prove to be the most effective biological pesticide.