Predators can influence the host‐parasite dynamics of their prey via nonconsumptive effects

Ecological communities are partly structured by indirect interactions, where one species can indirectly affect another by altering its interactions with a third species. In the absence of direct predation, nonconsumptive effects of predators on prey have important implications for subsequent community interactions. To better understand these interactions, we used a Daphnia‐parasite‐predator cue system to evaluate if predation risk affects Daphnia responses to a parasite. We investigated the effects of predator cues on two aspects of host–parasite interactions (susceptibility to infection and infection intensity), and whether or not these effects differed between sexes. Our results show that changes in response to predator cues caused an increase in the prevalence and intensity of parasite infections in female predator‐exposed Daphnia. Importantly, the magnitude of infection risk depended on how long Daphnia were exposed to the cues. Additionally, heavily infected Daphnia that were constantly exposed to cues produced relatively more offspring. While males were ~5× less likely to become infected compared to females, we were unable to detect effects of predator cues on male Daphnia–parasite interactions. In sum, predators, prey, and their parasites can form complex subnetworks in food webs, necessitating a nuanced understanding of how nonconsumptive effects may mediate these interactions.     

Ghost mtDNA haplotypes generated by fortuitous NUMTs can deeply disturb infra‐specific genetic diversity and phylogeographic pattern

Nuclear copies of mitochondrial DNA (NUMTs or mitochondrial pseudogenes) are known to impede the detection of interspecific genetic diversity. But the effect of these artifacts on phylogeographic reconstruction remains under evaluated. In this study, we analysed a set of 115 sequences of a fragment of the cytochrome c oxidase subunit I gene (COI) of Monochamus galloprovincialis (Coleoptera, Cerambycidae) for which overlapping signals in sequencing electropherograms were observed. Comparison of full and corrected ‘ambiguities‐free’ data sets reveals the prevalence of numerous supernumerary haplotypes that deeply affect genetic diversity indices and phylogeographic patterns of this species. Slightly divergent pseudogenes were recovered in 49 of the 115 sequences. These results highlight the potential misdetection of NUMTs using current control methods and the consequences on phylogeographic structure. To test the frequency of unintended amplification of NUMTs, a cloning was performed on 15 individuals. An average of 3.72 and a maximum of six paralogous sequences with different levels of divergence were identified among individual cloned. Within individual pairwise distance between paralogs raised 1.4%. This work calls for awareness to the presence of undetected NUMTs within mitochondrial data sets, especially at infra‐specific level.     

Sex‐specific responses of Asian citrus psyllid to volatiles of conspecific and host‐plant origin

Diaphorina citri Kuwayama (Hemiptera: Psyllidae) is the primary vector of Candidatus Liberibacter spp. bacteria that cause citrus greening, a disease of worldwide importance. Olfactometry was employed to test responses of D. citri to odours from intact citrus plants (Mexican lime, Citrus aurantifolia, sour orange, Citrus aurantium, Marsh grapefruit, Citrus paradisi and Valencia orange, Citrus sinensis), citrus plants previously infested with D. citri, and odours of conspecifics including nymphs, adult insects of same and opposite sex, and their products (honeydew), both alone and in combination. In contrast to other studies, psyllids of both sexes were attracted to volatiles of undamaged Mexican lime leaves, whereas undamaged grapefruit attracted only females, and leaves of Valencia and sour orange did not attract either sex. All four plant species attracted female psyllids when previously infested, but only Mexican lime and sour orange‐attracted males. Thus, Citrus species appear to vary in the production of both constituitive and induced volatiles that attract adult psyllids. Volatiles emitted by nymphs did not attract either sex, but psyllid honeydew was attractive to males, likely due to female pheromone residues. Males oriented to the odour of females, whereas the reverse was not true, and neither males nor females oriented to same‐sex volatiles. The addition of conspecific cues (adults, nymphs or honeydew) did not increase female attraction to previously infested leaves, but male response was increased by the presence of adults and honeydew, regardless of plant species. Thus, female psyllids appear to orient more strongly to volatiles of plant origin, whereas males respond more strongly to cues emanating from females and conspecific excretions. These results suggest that female psyllids drive the initial colonization of host plants, whereas males orient to females and infested plants. Identification of the specific volatiles involved may permit their use in monitoring and management of this pest.     

Geographic and host‐mediated population genetic structure in a cestode parasite of the three‐spined stickleback

Comparative studies of genetic diversity and population structure can shed light on the ecological and evolutionary factors that influence host–parasite interactions. Here we examined whether geography, time and genetic variation in Alaskan three‐spined stickleback (Gasterosteus aculeatus Linneaus) hosts shape the population genetic structure of the diphyllobothridean cestode parasite Schistocephalus solidus (Müller, 1776). Host lineages and haplotypes were identified by sequencing the mitochondrial cytochrome b gene, and host population structure was assessed by Bayesian clustering analysis of allelic variation at 11 microsatellite loci. Parasite population structure was characterized according to allelic variation at eight microsatellite loci. Mantel tests and canonical redundancy analysis were conducted to evaluate the proportion of parasite genetic variation attributable to time and geography vs. host lineage, haplotype, and genotypic cluster. Host and parasite population structure were largely discordant across the study area, probably reflecting differences in gene flow, environmental influences external to the host, and genomic admixture among host lineages. We found that geography explained the greatest proportion of parasite genetic variation, but that variation also reflects time, host lineage, and host haplotype. Associations with host haplotypes suggest that one parasite genotypic cluster exhibits a narrower host range, predominantly infecting the most common host haplotypes, whereas the other parasite cluster infects all haplotypes equally, including rare haplotypes. Although experimental infection trials might prove otherwise, distributional differences in hosts preferentially infected by S. solidus could underlie the observed pattern of population structure.     

Genetic structure and host–parasite co‐divergence: evidence for trait‐specific local adaptation

Host–parasite co‐evolution can lead to genetic differentiation among isolated host–parasite populations and local adaptation between parasites and their hosts. However, tests of local adaptation rarely consider multiple fitness‐related traits although focus on a single component of fitness can be misleading. Here, we concomitantly examined genetic structure and co‐divergence patterns of the trematode Coitocaecum parvum and its crustacean host Paracalliope fluviatilis among isolated populations using the mitochondrial cytochrome oxidase I gene (COI). We then performed experimental cross‐infections between two genetically divergent host–parasite populations. Both hosts and parasites displayed genetic differentiation among populations, although genetic structure was less pronounced in the parasite. Data also supported a co‐divergence scenario between C. parvum and P. fluviatilis potentially related to local co‐adaptation. Results from cross‐infections indicated that some parasite lineages seemed to be locally adapted to their sympatric (home) hosts in which they achieved higher infection and survival rates than in allopatric (away) amphipods. However, local, intrinsic host and parasite characteristics (host behavioural or immunological resistance to infections, parasite infectivity or growth rate) also influenced patterns of host–parasite interactions. For example, overall host vulnerability to C. parvum varied between populations, regardless of parasite origin (local vs. foreign), potentially swamping apparent local co‐adaptation effects. Furthermore, local adaptation effects seemed trait specific; different components of parasite fitness (infection and survival rates, growth) responded differently to cross‐infections. Overall, data show that genetic differentiation is not inevitably coupled with local adaptation, and that the latter must be interpreted with caution in a multi‐trait context.     

Host and parasite life history interplay to yield divergent population genetic structures in two ectoparasites living on the same bat species

Host–parasite interactions are ubiquitous in nature. However, how parasite population genetic structure is shaped by the interaction between host and parasite life history remains understudied. Studies comparing multiple parasites infecting a single host can be used to investigate how different parasite life history traits interplay with host behaviour and life history. In this study, we used 10 newly developed microsatellite loci to investigate the genetic structure of a parasitic bat fly (Basilia nana). Its host, the Bechstein's bat (Myotis bechsteinii), has a social system and roosting behaviour that restrict opportunities for parasite transmission. We compared fly genetic structure to that of the host and another parasite, the wing‐mite, Spinturnix bechsteini. We found little spatial or temporal genetic structure in B. nana, suggesting a large, stable population with frequent genetic exchange between fly populations from different bat colonies. This contrasts sharply with the genetic structure of the wing‐mite, which is highly substructured between the same bat colonies as well as temporally unstable. Our results suggest that although host and parasite life history interact to yield similar transmission patterns in both parasite species, the level of gene flow and eventual spatiotemporal genetic stability is differentially affected. This can be explained by the differences in generation time and winter survival between the flies and wing‐mites. Our study thus exemplifies that the population genetic structure of parasites on a single host can vary strongly as a result of how their individual life history characteristics interact with host behaviour and life history traits.     

Insights into the genetic history of Green‐legged Partridgelike fowl: mtDNA and genome‐wide SNP analysis

The Green‐legged Partridgelike (GP) fowl, an old native Polish breed, is characterised by reseda green‐coloured shanks rather than yellow, white, slate or black commonly observed across most domestic breeds of chicken. Here, we investigate the origin, genetic relationships and structure of the GP fowl using mtDNA D‐loop sequencing and genome‐wide SNP analysis. Genome‐wide association analysis between breeds enables us to verify the genetic control of the reseda green shank phenotype, a defining trait for the breed. Two mtDNA D‐loop haplogroups and three autosomal genetic backgrounds are revealed. Significant associations of SNPs on chromosomes GGA24 and GGAZ indicate that the reseda green leg phenotype is associated with recessive alleles linked to the W and Id loci. Our results provide new insights into the genetic history of European chicken, indicating an admixd origin of East European traditional breeds of chicken on the continent, as supported by the presence of the reseda green phenotype and the knowledge that the GP fowl as a breed was developed before the advent of commercial stocks.     

Genetic signs of multiple colonization events in Baltic ciscoes with radiation into sympatric spring‐ and autumn‐spawners confined to early postglacial arrival

Presence of sympatric populations may reflect local diversification or secondary contact of already distinct forms. The Baltic cisco (Coregonus albula) normally spawns in late autumn, but in a few lakes in Northern Europe sympatric autumn and spring‐ or winter‐spawners have been described. So far, the evolutionary relationships and taxonomic status of these main life history forms have remained largely unclear. With microsatellites and mtDNA sequences, we analyzed extant and extinct spring‐ and autumn‐spawners from a total of 23 Swedish localities, including sympatric populations. Published sequences from Baltic ciscoes in Germany and Finland, and Coregonus sardinella from North America were also included together with novel mtDNA sequences from Siberian C. sardinella. A clear genetic structure within Sweden was found that included two population assemblages markedly differentiated at microsatellites and apparently fixed for mtDNA haplotypes from two distinct clades. All sympatric Swedish populations belonged to the same assemblage, suggesting parallel evolution of spring‐spawning rather than secondary contact. The pattern observed further suggests that postglacial immigration to Northern Europe occurred from at least two different refugia. Previous results showing that mtDNA in Baltic cisco is paraphyletic with respect to North American C. sardinella were confirmed. However, the inclusion of Siberian C. sardinella revealed a more complicated pattern, as these novel haplotypes were found within one of the two main C. albula clades and were clearly distinct from those in North American C. sardinella. The evolutionary history of Northern Hemisphere ciscoes thus seems to be more complex than previously recognized.     

Pace‐of‐life: Relationships among locomotor activity,life history,and circadian rhythm in the assassin bug,Amphibolus venator

The pace‐of‐life syndrome (POLS) hypothesis means that animal behavior is correlated with life history strategies. Studies have reported that the free‐running period of the circadian rhythm (length of the period) is correlated with life history strategies in some animals. Although the length of the circadian rhythm may be associated with the POLS hypothesis, few studies have investigated the relationships among animal behavior, life history traits, and circadian rhythm. We tested the POLS hypothesis in the assassin bug, Amphibolus venator, which shows individual variation in locomotor activity. We found higher repeatability of differences in locomotor activity between individuals. Moreover, we found a trade‐off between locomotor activity and developmental period such that active individuals developed faster. However, locomotor activity was not correlated with the length of the circadian rhythm in A. venator. Therefore, this study suggests that the length of the circadian rhythm in A. venator does not support the POLS hypothesis.     

Food web associations and effect of trophic resources and environmental factors on parasitoids expanding their host range into non‐native hosts

Trophic interactions and environmental conditions determine the structure of food webs and the host expansion of parasitoids into novel insect hosts. In this study, we investigate plant–insect–parasitoid food web interactions, specifically the effect of trophic resources and environmental factors on the presence of the parasitoids expanding their host range after the invasion of Chrysodeixis chalcites (Esper) (Lepidoptera: Noctuidae). We also consider potential candidates for biological control of this non‐native pest. A survey of larval stages of Plusiinae (Lepidoptera: Noctuidae) and their larval parasitoids was conducted in field and vegetable greenhouse crops in 2009 and 2010 in various locations of Essex and Chatham‐Kent counties in Ontario, Canada. Twenty‐one plant–host insect–host parasitoid associations were observed among Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae), C. chalcites, and larval parasitoids in three trophic levels of interaction. Chrysodeixis chalcites, an old‐world species that had just arrived in the region, was the most common in our samples. The larval parasitoids Campoletis sonorensis (Cameron) (Hymenoptera: Ichneumonidae), Cotesia vanessae (Reinhard), Cotesia sp., Microplitis alaskensis (Ashmead), and Meteorus rubens (Nees) (all Hymenoptera: Braconidae) expanded their host range into C. chalcites changing the structure of the food web. Copidosoma floridanum (Ashmead) (Hymenoptera: Encyrtidae) was the most common parasitoid of T. ni that was not found in the invasive species. Plant species, host abundance, and agro‐ecosystem were the most common predictors for the presence of the parasitoids expanding their host range into C. chalcites. Our results indicate that C. sonorensis, C. vanessae, and C. floridanum should be evaluated for their potential use in biological control of C. chalcites and T. ni.     

A novel approach to parasite population genetics: Experimental infection reveals geographic differentiation,recombination and host‐mediated population structure in Pasteuria ramosa,a bacterial parasite of Daphnia

The population structure of parasites is central to the ecology and evolution of host‐parasite systems. Here, we investigate the population genetics of Pasteuria ramosa, a bacterial parasite of Daphnia. We used natural P. ramosa spore banks from the sediments of two geographically well‐separated ponds to experimentally infect a panel of Daphnia magna host clones whose resistance phenotypes were previously known. In this way, we were able to assess the population structure of P. ramosa based on geography, host resistance phenotype and host genotype. Overall, genetic diversity of P. ramosa was high, and nearly all infected D. magna hosted more than one parasite haplotype. On the basis of the observation of recombinant haplotypes and relatively low levels of linkage disequilibrium, we conclude that P. ramosa engages in substantial recombination. Isolates were strongly differentiated by pond, indicating that gene flow is spatially restricted. Pasteuria ramosa isolates within one pond were segregated completely based on the resistance phenotype of the host—a result that, to our knowledge, has not been previously reported for a nonhuman parasite. To assess the comparability of experimental infections with natural P. ramosa isolates, we examined the population structure of naturally infected D. magna native to one of the two source ponds. We found that experimental and natural infections of the same host resistance phenotype from the same source pond were indistinguishable, indicating that experimental infections provide a means to representatively sample the diversity of P. ramosa while reducing the sampling bias often associated with studies of parasite epidemics. These results expand our knowledge of this model parasite, provide important context for the large existing body of research on this system and will guide the design of future studies of this host‐parasite system.     

The influence of life history and climate driven diversification on the mtDNA phylogeographic structures of two southern African Mastomys species (Rodentia: Muridae: Murinae)

The phylogeographic patterns of small mammals in southern Africa are frequently disjunct. This pattern is predominately attributed to vicariant geographical barriers coupled to climate driven diversification. To gain further insights into this hypothesis, we embarked on a comparative mtDNA phylogeographic study of two common rodent species in southern Africa, Mastomys natalensis and Mastomys coucha. Parsimony haplotype networks and SplitsTrees of mtDNA cytochrome oxidase I data showed a large degree of haplotype sharing throughout the sampling range. Within southern Africa, we found no conclusive evidence to support geographic vicariance as a contributing factor towards Mastomys speciation. We proposed that the regional phylogeographic structures detected for M. natalensis and M. coucha are the result of weak isolation by distance coupled to repeated expansions and contractions of suitable habitat. Both species probably survived in multiple refugia during unfavourable periods and mismatch distributions show signs of population expansion. Mitochondrial DNA nucleotide diversity values (π) show marked differences between the two species (M. natalensis: 0.003 and M. coucha: 0.468), and M. coucha also shows a higher level of population differentiation in AMOVA analyses. These differences are most likely due to life history discrepancies between the two species. Mastomys coucha is regarded to be more of a habitat specialist when compared to M. natalensis, and this probably places a higher constraint on M. coucha dispersal abilities. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 114 , 58–68.     

Comparative phylogeography of two sympatric beeches in subtropical China: Species‐specific geographic mosaic of lineages

In subtropical China, large‐scale phylogeographic comparisons among multiple sympatric plants with similar ecological preferences are scarce, making generalizations about common response to historical events necessarily tentative. A phylogeographic comparison of two sympatric Chinese beeches (Fagus lucida and F. longipetiolata, 21 and 28 populations, respectively) was conducted to test whether they have responded to historical events in a concerted fashion and to determine whether their phylogeographic structure is exclusively due to Quaternary events or it is also associated with pre‐Quaternary events. Twenty‐three haplotypes were recovered for F. lucida and F. longipetiolata (14 each one and five shared). Both species exhibited a species‐specific mosaic distribution of haplotypes, with many of them being range‐restricted and even private to populations. The two beeches had comparable total haplotype diversity but F. lucida had much higher within‐population diversity than F. longipetiolata. Molecular dating showed that the time to most recent common ancestor of all haplotypes was 6.36 Ma, with most haplotypes differentiating during the Quaternary. [Correction added on 14 October 2013, after first online publication: the time unit has been corrected to ‘6.36’.] Our results support a late Miocene origin and southwards colonization of Chinese beeches when the aridity in Central Asia intensified and the monsoon climate began to dominate the East Asia. During the Quaternary, long‐term isolation in subtropical mountains of China coupled with limited gene flow would have lead to the current species‐specific mosaic distribution of lineages.     

Parting ways: parasite release in nature leads to sex‐specific evolution of defence

We evaluated the extent to which males and females evolve along similar or different trajectories in response to the same environmental shift. Specifically, we used replicate experimental introductions in nature to consider how release from a key parasite (Gyrodactylus) generates similar or different defence evolution in male vs. female guppies (Poecilia reticulata). After 4–8 generations of evolution, guppies were collected from the ancestral (parasite still present) and derived (parasite now absent) populations and bred for two generations in the laboratory to control for nongenetic effects. These F2 guppies were then individually infected with Gyrodactylus, and infection dynamics were monitored on each fish. We found that parasite release in nature led to sex‐specific evolutionary responses: males did not show much evolution of resistance, whereas females showed the evolution of increased resistance. Given that male guppies in the ancestral population had greater resistance to Gyrodactylus than did females, evolution in the derived populations led to reduction of sexual dimorphism in resistance. We argue that previous selection for high resistance in males constrained (relative to females) further evolution of the trait. We advocate more experiments considering sex‐specific evolutionary responses to environmental change.     

Effects of prohydrojasmon‐treated corn plants on attractiveness to parasitoids and the performance of their hosts

We investigated the effect of prohydrojasmon [propyl (1RS,2RS)‐(3‐oxo‐ 2‐pentylcyclopentyl) acetate] (PDJ) treatment of intact corn plants, on their attractiveness to the specialist endoparasitoid, Cotesia kariyai Watanabe (Hymenoptera: Braconidae), and on the performance of the common armyworm, Mythimna separata (Walker) (Lepidoptera: Noctuidae) under laboratory conditions. Attractiveness of C. kariyai to PDJ‐treated plants was studied in a wind tunnel, whereas performance of M. separata larvae was tested in plastic cages. The attractiveness of the treated plants increased with concentrations of PDJ increasing to 2 mm , which was equivalent to the attractiveness of host‐infested plants. PDJ‐treated corn plants emitted 16 volatile compounds (α‐pinene, β‐myrcene, (Z)‐3‐hexenyl acetate, limonene, (E)‐β‐ocimene, linalool, (E)‐4,8‐dimethyl‐1,3,7‐nonatriene, (+)‐cyclosativene, ylangene, (E)‐β‐farnesene, (E, E)‐4,8,12‐trimethyl‐1,3,7,11‐tridecatetraene, α‐bergamotene, γ‐cadinene, δ‐cadinene, α‐muulolene and nerolidol), most of which were observed in the headspace of host‐infested corn plants with some quantitative and qualitative differences. We also tested the effects of PDJ treatment on the performance of M. separata larvae. The survival rates of the larval and pupal stages were significantly lower at 2 mm level of PDJ. A significant decrease in weight at 6th stadium larvae was observed only at 2 mm level of PDJ. In contrast, PDJ treatment at all PDJ concentration levels caused significant reduction in weight of pupal stage as compared to control. These data suggested that PDJ, originally developed as a plant growth regulator, especially to induce coloring of fruits, has the potential to induce direct and indirect defenses in corn plants against common armyworm, M. separata.