Coupling between tolerance and resistance for two related Eimeria parasite species

Resistance (host capacity to reduce parasite burden) and tolerance (host capacity to reduce impact on its health for a given parasite burden) manifest two different lines of defense. Tolerance can be independent from resistance, traded off against it, or the two can be positively correlated because of redundancy in underlying (immune) processes. We here tested whether this coupling between tolerance and resistance could differ upon infection with closely related parasite species. We tested this in experimental infections with two parasite species of the genus Eimeria. We measured proxies for resistance (the (inverse of) number of parasite transmission stages (oocysts) per gram of feces at the day of maximal shedding) and tolerance (the slope of maximum relative weight loss compared to day of infection on number of oocysts per gram of feces at the day of maximal shedding for each host strain) in four inbred mouse strains and four groups of F1 hybrids belonging to two mouse subspecies, Mus musculus domesticus and Mus musculus musculus. We found a negative correlation between resistance and tolerance against Eimeria falciformis, while the two are uncoupled against Eimeria ferrisi. We conclude that resistance and tolerance against the first parasite species might be traded off, but evolve more independently in different mouse genotypes against the latter. We argue that evolution of the host immune defenses can be studied largely irrespective of parasite isolates if resistance–tolerance coupling is absent or weak (E. ferrisi) but host–parasite coevolution is more likely observable and best studied in a system with negatively correlated tolerance and resistance (E. falciformis).     

Do Parasitic Trematode Cercariae Demonstrate a Preference for Susceptible Host Species?

Many parasites are motile and exhibit behavioural preferences for certain host species. Because hosts can vary in their susceptibility to infections, parasites might benefit from preferentially detecting and infecting the most susceptible host, but this mechanistic hypothesis for host-choice has rarely been tested. We evaluated whether cercariae (larval trematode parasites) prefer the most susceptible host species by simultaneously presenting cercariae with four species of tadpole hosts. Cercariae consistently preferred hosts in the following order: Anaxyrus ( = Bufo) terrestris (southern toad), Hyla squirella (squirrel tree frog), Lithobates ( = Rana) sphenocephala (southern leopard frog), and Osteopilus septentrionalis (Cuban tree frog). These host species varied in susceptibility to cercariae in an order similar to their attractiveness with a correlation that approached significance. Host attractiveness to parasites also varied consistently and significantly among individuals within a host species. If heritable, this individual-level host variation would represent the raw material upon which selection could act, which could promote a Red Queen “arms race” between host cues and parasite detection of those cues. If, in general, motile parasites prefer to infect the most susceptible host species, this phenomenon could explain aggregated distributions of parasites among hosts and contribute to parasite transmission rates and the evolution of virulence. Parasite preferences for hosts belie the common assumption of disease models that parasites seek and infect hosts at random.     

Adaptive population structure shifts in invasive parasitic mites,Varroa destructor

Comparative studies of genetic diversity and population structure can shed light on the ecological and evolutionary factors governing host–parasite interactions. Even though invasive parasites are considered of major biological importance, little is known about their adaptative potential when infesting the new hosts. Here, the genetic diversification of Varroa destructor, a novel parasite of Apis mellifera originating from Asia, was investigated using population genetics to determine how the genetic structure of the parasite changed in distinct European populations of its new host. To do so, mites infesting two categories of hosts in four European regions were compared: (a) adapted hosts surviving through means of natural selection, thereby expected to impose strong selective pressure on the mites, and (b) treated host populations, surviving mite infestations because acaricides are applied, therefore characterized by a relaxed selection imposed by the host on the mites. Significant genetic divergence was found across regions, partially reflecting the invasion pattern of V. destructor throughout Europe and indicating local adaptation of the mite to the host populations. Additionally, varying degrees of genotypic changes were found between mites from adapted and treated colonies. Altogether, these results indicate that V. destructor managed to overcome the genetic bottlenecks following its introduction in Europe and that host‐mediated selection fostered changes in the genetic structure of this mite at diverse geographic scales. These findings highlight the potential of parasites to adapt to their local host populations and confirm that adaptations developed within coevolutionary dynamics are a major determinant of population genetic changes.     

Parasitism of Sympetrum dragonflies by Arrenurus planus mites: maintenance of resistance particular to one species.

Using field surveys and histological methods, we show that a dragonfly species (Sympetrum internum) has an effective resistance, not seen previously in other odonates, to a mite parasite (Arrenurus planus). This mite is a generalist parasite known to effectively engorge on several other odonate species. We argue that selection is likely weak, favouring counter adaptations of Arrenurus planus to Sympetrum internum, in part because other host species are available. We further argue that this pattern is possibly linked to the fact that the mode of resistance is relatively novel, and because Sympetrum internum is rare compared to another host species, Sympetrum obtrusum, at our study site. Although resistance of Sympetrum internum is quite effective against Arrenurus planus, Arrenurus planus larvae still attach to this species, but less often than they attach to Sympetrum obtrusum. Attachment to unsuitable hosts may reflect constraints operating on Arrenurus planus larvae during host discovery. Such factors influencing the evolution of resistance, when several potential host species exist, have not received much attention.     

Biology and control of Varroa destructor

The ectoparasitic honey bee mite Varroa destructor was originally confined to the Eastern honey bee Apis cerana. After a shift to the new host Apis mellifera during the first half of the last century, the parasite dispersed world wide and is currently considered the major threat for apiculture. The damage caused by Varroosis is thought to be a crucial driver for the periodical colony losses in Europe and the USA and regular Varroa treatments are essential in these countries. Therefore, Varroa research not only deals with a fascinating host–parasite relationship but also has a responsibility to find sustainable solutions for the beekeeping.This review provides a survey of the current knowledge in the main fields of Varroa research including the biology of the mite, damage to the host, host tolerance, tolerance breeding and Varroa treatment. We first present a general view on the functional morphology and on the biology of the Varroa mite with special emphasis on host–parasite interactions during reproduction of the female mite. The pathology section describes host damage at the individual and colony level including the problem of transmission of secondary infections by the mite. Knowledge of both the biology and the pathology of Varroa mites is essential for understanding possible tolerance mechanisms in the honey bee host. We comment on the few examples of natural tolerance in A. mellifera and evaluate recent approaches to the selection of Varroa tolerant honey bees. Finally, an extensive listing and critical evaluation of chemical and biological methods of Varroa treatments is given.This compilation of present-day knowledge on Varroa honey bee interactions emphasizes that we are still far from a solution for Varroa infestation and that, therefore, further research on mite biology, tolerance breeding, and Varroa treatment is urgently needed.     

Comparative population genetics of a parasitic nematode and its host community: the trichostrongylid Neoheligmonella granjoni and Mastomys rodents in southeastern Senegal

Contrasting host and parasite population genetic structures can provide information about the population ecology of each species and the potential for local adaptation. Here, we examined the population genetic structure of the nematode Neoheligmonella granjoni at a regional scale in southeastern Senegal, using 11 microsatellite markers. Using the results previously obtained for the two main rodent species of the host community, Mastomys natalensis and Mastomys erythroleucus, we tested the hypothesis that the parasite population structure was mediated by dispersal levels of the most vagile host. The results showed similar genetic diversity levels between host and parasite populations, and consistently lower levels of genetic differentiation in N. granjoni, with the exception of one outlying locus with a high F_ST. The aberrant pattern at this locus was primarily due to two alleles occurring at markedly different frequencies in one locality, suggesting selection at this locus, or a closely linked one. Genetic differentiation levels and isolation by distance analyses suggested that gene flow was high and random in N. granjoni at the spatial scale examined. The correlation between pair-wise genetic differentiation levels in the parasite and its main host was consistent with the hypothesis tested. Models of local adaptation as a function of the dispersal rates of hosts and parasites suggest that opportunities for local adaptation would be low in this biological system.     

Rapid specialization of counter defenses enables two-spotted spider mite to adapt to novel plant hosts

Genetic adaptation, occurring over a long evolutionary time, enables host-specialized herbivores to develop novel resistance traits and to efficiently counteract the defenses of a narrow range of host plants. In contrast, physiological acclimation, leading to the suppression and/or detoxification of host defenses, is hypothesized to enable broad generalists to shift between plant hosts. However, the host adaptation mechanisms used by generalists composed of host-adapted populations are not known. Two-spotted spider mite (TSSM; Tetranychus urticae) is an extreme generalist herbivore whose individual populations perform well only on a subset of potential hosts. We combined experimental evolution, Arabidopsis thaliana genetics, mite reverse genetics, and pharmacological approaches to examine mite host adaptation upon the shift of a bean (Phaseolus vulgaris)-adapted population to Arabidopsis. We showed that cytochrome P450 monooxygenases are required for mite adaptation to Arabidopsis. We identified activities of two tiers of P450s: general xenobiotic-responsive P450s that have a limited contribution to mite adaptation to Arabidopsis and adaptation-associated P450s that efficiently counteract Arabidopsis defenses. In approximately 25 generations of mite selection on Arabidopsis plants, mites evolved highly efficient detoxification-based adaptation, characteristic of specialist herbivores. This demonstrates that specialization to plant resistance traits can occur within the ecological timescale, enabling the TSSM to shift to novel plant hosts.

Mites can evolve highly efficient detoxification-based adaptation in approximately 25 generations on an initially unfavorable plant host, revealing that specialization can occur within the ecological timescale.     

Dose-independent virulence in phoretic mites that parasitize burying beetles

Virulence, the negative impact of parasites on their hosts, typically increases with parasite dose. Parasites and hosts often compete for host resources and more parasites will consume more resources. Depending on the mechanism of competition, increasing host resources can benefit the host. Additional resources can also be harmful when the parasites are the main beneficiaries. Then, the parasites will thrive and virulence increases. While parasite dose is often easy to manipulate, it is less trivial to experimentally scale host resources. Here, we study a system with external host resources that can be easily manipulated: Nicrophorus burying beetles reproduce on vertebrate carcasses, with larger carcasses yielding more beetle offspring. Phoretic Poecilochirus mites reproduce alongside the beetles and reduce beetle fitness. The negative effect of mites could be due to competition for the carrion between beetle and mite offspring. We manipulated mite dose and carcass size to better understand the competition between the symbionts. We found that mite dose itself was not a strong predictor of virulence. Instead, the number of mite offspring determined beetle fitness. At larger doses, there was strong competition among adult parental mites as well as mite offspring. While increasing the carcass size increased both host and parasite fitness, it did surprisingly little to alleviate the negative effect that mites had on beetles. Instead, relative virulence was stronger on large carcasses, indicating that the parasites appropriate more of the additional resources. Our results demonstrate an ecological influence on the selection of parasites on their hosts and suggest that virulence can be dose-independent in principle.     

Conspicuous Coloration in Males of the Damselfly Nehalennia irene (Zygoptera: Coenagrionidae): Do Males Signal Their Unprofitability to Other Males?

In damselflies, sexual colour dimorphism is commonly explained as a consequence of selection on traits that increase male attractiveness to females. However, while many species in the damselfly family Coenagrionidae (Insecta: Odonata) are sexually dimorphic, the males do not engage in displays, and male competition for mates resembles a “scramble”. An alternative explanation for the sexual differences in coloration within these species is that sexual dimorphism has evolved as a sex-related warning signal, with males signalling their uprofitability as mates to other males, thereby avoiding harassment from conspecifics. We evaluated an underlying assumption of the theory that male-male harassment rate is influenced by colour by comparing harassment of males of the species Nehalennia irene that had been painted to make them appear: (i) similar to an unaltered male (blue), (ii) different from a male (orange) and (iii) more similar to a female (black). When caged together we found that blue-painted males experienced significantly lower harassment than black-painted males. When unpainted males were caged with each type of painted male we found that blue-painted males and the unpainted males housed in the same cages experienced lower rates of harassment than males housed in cages where some males were painted black, suggesting that a single, reliable signal of unprofitability may benefit the individuals that carry it. While our results do not in themselves demonstrate that sexual colour dimorphism originally evolved as an intra-specific warning signal, they do show that harassment is influenced by coloration, and that such selection could conceivably maintain male coloration as a warning signal.     

Avoidance of host resistance in the oviposition-site preferences of rose bitterling

A contemporary outcome of dynamic host–parasite coevolution can be driven by the adaptation of a parasite to exploit its hosts at the population and species levels (parasite specialisation) or by local host adaptations leading to greater host resistance to sympatric parasite populations (host resistance). We tested the predominance of these two scenarios using cross-infection experiments with two geographically distant populations of the rose bitterling, Rhodeus ocellatus, a fish brood parasite of freshwater mussels, and four populations of their mussel hosts (two Anodonta woodiana and two Unio douglasiae populations) with varying degrees of geographic sympatry and local coexistence. Our data support predictions for host resistance at the species level but no effect of local coexistence between specific populations. Rhodeus ocellatus showed a preference for allopatric host populations, irrespective of host species. Host mussel response, in terms of ejection of R. ocellatus eggs, was stronger in the more widespread and abundant host species (A. woodiana) and this response tended to be higher in sympatric populations. These outcomes provide support for the importance of host resistance in bitterling oviposition-site decisions, demonstrating that host choice by R. ocellatus is adaptive by minimizing egg ejections. These findings imply that R. ocellatus, and potentially other bitterling species, may benefit from exploiting novel hosts, which may not possess appropriate adaptive responses to parasitism.     

Human Follicular Mites: Ectoparasites Becoming Symbionts

Most humans carry mites in the hair follicles of their skin for their entire lives. Follicular mites are the only metazoans that continuously live on humans. We propose that Demodex folliculorum (Acari) represents a transitional stage from a host-injuring obligate parasite to an obligate symbiont. Here, we describe the profound impact of this transition on the genome and physiology of the mite. Genome sequencing revealed that the permanent host association of D. folliculorum led to an extensive genome reduction through relaxed selection and genetic drift, resulting in the smallest number of protein-coding genes yet identified among panarthropods. Confocal microscopy revealed that this gene loss coincided with an extreme reduction in the number of cells. Single uninucleate muscle cells are sufficient to operate each of the three segments that form each walking leg. While it has been assumed that the reduction of the cell number in parasites starts early in development, we identified a greater total number of cells in the last developmental stage (nymph) than in the terminal adult stage, suggesting that reduction starts at the adult or ultimate stage of development. This is the first evolutionary step in an arthropod species adopting a reductive, parasitic, or endosymbiotic lifestyle. Somatic nuclei show under-replication at the diploid stage. Novel eye structures or photoreceptors as well as a unique human host melatonin-guided day/night rhythm are proposed for the first time. The loss of DNA repair genes coupled with extreme endogamy might have set this mite species on an evolutionary dead-end trajectory.     

Host-Parasite Interactions and Purifying Selection in a Microsporidian Parasite of Honey Bees

To clarify the mechanisms of Nosema ceranae parasitism, we deep-sequenced both honey bee host and parasite mRNAs throughout a complete 6-day infection cycle. By time-series analysis, 1122 parasite genes were significantly differently expressed during the reproduction cycle, clustering into 4 expression patterns. We found reactive mitochondrial oxygen species modulator 1 of the host to be significantly down regulated during the entire infection period. Our data support the hypothesis that apoptosis of honey bee cells was suppressed during infection. We further analyzed genome-wide genetic diversity of this parasite by comparing samples collected from the same site in 2007 and 2013. The number of SNP positions per gene and the proportion of non-synonymous substitutions per gene were significantly reduced over this time period, suggesting purifying selection on the parasite genome and supporting the hypothesis that a subset of N. ceranae strains might be dominating infection.     

A partition of Toxoplasma gondii genotypes across spatial gradients and among host species,and decreased parasite diversity towards areas of human settlement in North America

Toxoplasma gondii counts among the most consequential food-borne parasites, and although the parasite occurs in a wide range of wild and domesticated animals, farms may constitute a specific and important locus of transmission. If so, parasites in animals that inhabit agricultural habitats might be suspected of harbouring genetically distinct parasite types. To better understand habitat effects pertinent to this parasite’s transmission, we compiled and analysed existing genotypic data of 623 samples from animals across a proximity gradient from areas of human settlement to the wilderness in North America. To facilitate such analysis, T. gondii isolates were divided into three groups: (i) from farm-bound animals (with the most limited home ranges on farms); (ii) from free-roaming animals (with wider home ranges on or near farms); and (iii) from wildlife. In addition, parasite genotype distribution in different animal species was analysed. We observed no absolute limitation of any of five major genotypes to any one habitat; however, the frequency of four genotypes decreased across the gradient from the farm-bound group, to the free-roaming group, then the wildlife, whereas a fifth genotype increased along that gradient. Genetic diversity was greater in free-roaming than in farm-bound animals. The genotypic composition of parasites in wildlife differed from those in farm-bound and free-roaming animals. Furthermore, parasite genotypes differed among host species. We conclude that T. gondii genotype distributions are influenced by the spatial habitat and host species composition, and parasite diversity decreases towards areas of human settlement, elucidating facts which may influence transmission dynamics and zoonotic potential in this ubiquitous but regionally variable parasite.     

Lineage-specific positive selection at the merozoite surface protein 1 (msp1) locus of Plasmodium vivax and related simian malaria parasites

Background

The 200 kDa merozoite surface protein 1 (MSP-1) of malaria parasites, a strong vaccine candidate, plays a key role during erythrocyte invasion and is a target of host protective immune response. Plasmodium vivax, the most widespread human malaria parasite, is closely related to parasites that infect Asian Old World monkeys, and has been considered to have become a parasite of man by host switch from a macaque malaria parasite. Several Asian monkey parasites have a range of natural hosts. The same parasite species shows different disease manifestations among host species. This suggests that host immune responses to P. vivax-related malaria parasites greatly differ among host species (albeit other factors). It is thus tempting to invoke that a major immune target parasite protein such as MSP-1 underwent unique evolution, depending on parasite species that exhibit difference in host range and host specificity.

Results

We performed comparative phylogenetic and population genetic analyses of the gene encoding MSP-1 (msp1) from P. vivax and nine P. vivax-related simian malaria parasites. The inferred phylogenetic tree of msp1 significantly differed from that of the mitochondrial genome, with a striking displacement of P. vivax from a position close to P. cynomolgi in the mitochondrial genome tree to an outlier of Asian monkey parasites. Importantly, positive selection was inferred for two ancestral branches, one leading to P. inui and P. hylobati and the other leading to P. vivax, P. fieldi and P. cynomolgi. This ancestral positive selection was estimated to have occurred three to six million years ago, coinciding with the period of radiation of Asian macaques. Comparisons of msp1 polymorphisms between P. vivax, P. inui and P. cynomolgi revealed that while some positively selected amino acid sites or regions are shared by these parasites, amino acid changes greatly differ, suggesting that diversifying selection is acting species-specifically on msp1.

Conclusions

The present results indicate that the msp1 locus of P. vivax and related parasite species has lineage-specific unique evolutionary history with positive selection. P. vivax and related simian malaria parasites offer an interesting system toward understanding host species-dependent adaptive evolution of immune-target surface antigen genes such as msp1.     

Morphological variation in the cosmopolitan fish parasite Neobenedenia girellae (Capsalidae: Monogenea)

Intra-species morphological variation presents a considerable problem for species identification and can result in taxonomic confusion. This is particularly pertinent for species of Neobenedenia which are harmful agents in captive fish populations and have historically been identified almost entirely based on morphological characters. This study aimed to understand how the morphology of Neobenedenia girellae varies with host fish species and the environment. Standard morphological features of genetically indistinct parasites from various host fish species were measured under controlled temperatures and salinities. An initial field-based investigation found that parasite morphology significantly differed between genetically indistinct parasites infecting various host fish species. The majority of the morphological variation observed (60%) was attributed to features that assist in parasite attachment to the host (i.e. the posterior and anterior attachment organs and their accessory hooks) which are important characters in monogenean taxonomy. We then experimentally examined the effects of the interaction between host fish species and environmental factors (temperature and salinity) on the morphology of isogenic parasites derived from a single, isolated hermaphroditic N. girellae infecting barramundi, Lates calcarifer. Experimental infection of L. calcarifer and cobia, Rachycentron canadum, under controlled laboratory conditions did not confer host-mediated phenotypic plasticity in N. girellae, suggesting that measured morphological differences could be adaptive and only occur over multiple parasite generations. Subsequent experimental infection of a single host species, L. calcarifer, at various temperatures (22, 30 and 32?°C) and salinities (35 and 40‰) showed that in the cooler environments (22?°C) N. girellae body proportions were significantly smaller compared with warmer temperatures (30 and 32?°C; P?<?0.0001), whereas salinity had no effect. This is evidence that temperature can drive phenotypic plasticity in key taxonomic characters of N. girellae under certain environmental conditions.     

Differential Water Mite Parasitism,Phenoloxidase Activity,and Resistance to Mites Are Unrelated across Pairs of Related Damselfly Species

Related host species often demonstrate differences in prevalence and/or intensity of infection by particular parasite species, as well as different levels of resistance to those parasites. The mechanisms underlying this interspecific variation in parasitism and resistance expression are not well understood. Surprisingly, few researchers have assessed relations between actual levels of parasitism and resistance to parasites seen in nature across multiple host species. The main goal of this study was to determine whether interspecific variation in resistance against ectoparasitic larval water mites either was predictive of interspecific variation in parasitism for ten closely related species of damselflies (grouped into five “species pairs”), or was predicted by interspecific variation in a commonly used measure of innate immunity (total Phenoloxidase or potential PO activity). Two of five species pairs had interspecific differences in proportions of individuals resisting larval Arrenurus water mites, only one of five species pairs had species differences in prevalence of larval Arrenurus water mites, and another two of five species pairs showed species differences in mean PO activity. Within the two species pairs where species differed in proportion of individuals resisting mites the species with the higher proportion did not have correspondingly higher PO activity levels. Furthermore, the proportion of individuals resisting mites mirrored prevalence of parasitism in only one species pair. There was no interspecific variation in median intensity of mite infestation within any species pair. We conclude that a species’ relative ability to resist particular parasites does not explain interspecific variation in parasitism within species pairs and that neither resistance nor parasitism is reflected by interspecific variation in total PO or potential PO activity.     

Reproduction of parasitic mites Varroa destructor in original and new honeybee hosts

The ectoparasitic mite, Varroa destructor, shifted host from the eastern honeybee, Apis cerana, to the western honeybee, Apis mellifera. Whereas the original host survives infestations by this parasite, they are lethal to colonies of its new host. Here, we investigated a population of A. cerana naturally infested by the V. destructor Korea haplotype that gave rise to the globally invasive mite lineage. Our aim was to better characterize traits that allow for the survival of the original host to infestations by this particular mite haplotype. A known major trait of resistance is the lack of mite reproduction on worker brood in A. cerana. We show that this trait is neither due to a lack of host attractiveness nor of reproduction initiation by the parasite. However, successful mite reproduction was prevented by abnormal host development. Adult A. cerana workers recognized this state and removed hosts and parasites, which greatly affected the fitness of the parasite. These results confirm and complete previous observations of brood susceptibility to infestation in other honeybee host populations, provide new insights into the coevolution between hosts and parasites in this system, and may contribute to mitigating the large‐scale colony losses of A. mellifera due to V. destructor.     

Reproduction of ectoparasitic mites in a coevolved system: Varroa spp.—Eastern honey bees,Apis cerana

Parasite host shifts can impose a high selective pressure on novel hosts. Even though the coevolved systems can reveal fundamental aspects of host–parasite interactions, research often focuses on the new host–parasite relationships. This holds true for two ectoparasitic mite species, Varroa destructor and Varroa jacobsonii, which have shifted hosts from Eastern honey bees, Apis cerana, to Western honey bees, Apis mellifera, generating colony losses of these pollinators globally. Here, we study infestation rates and reproduction of V. destructor and V. jacobsonii haplotypes in 185 A. cerana colonies of six populations in China and Thailand to investigate how coevolution shaped these features. Reproductive success was mostly similar and low, indicating constraints imposed by hosts and/or mite physiology. Infestation rates varied between mite haplotypes, suggesting distinct local co‐evolutionary scenarios. The differences in infestation rates and reproductive output between haplotypes did not correlate with the virulence of the respective host‐shifted lineages suggesting distinct selection scenarios in novel and original host. The occasional worker brood infestation was significantly lower than that of drone brood, except for the V. destructor haplotype (Korea) from which the invasive lineage derived. Whether mites infesting and reproducing in atypical intraspecific hosts (i.e., workers and queens) actually predisposes for and may govern the impact of host shifts on novel hosts should be determined by identifying the underlying mechanisms. In general, the apparent gaps in our knowledge of this coevolved system need to be further addressed to foster the adequate protection of wild and managed honey bees from these mites globally.     

Sexual signalling in female crested macaques and the evolution of primate fertility signals

Background

Host-parasite coevolution can lead to local adaptation of either parasite or host if there is specificity (GxG interactions) and asymmetric evolutionary potential between host and parasite. This has been demonstrated both experimentally and in field studies, but a substantial proportion of studies fail to detect such clear-cut patterns. One explanation for this is that adaptation can be masked by counter-adaptation by the antagonist. Additionally, genetic architecture underlying the interaction is often highly complex thus preventing specific adaptive responses. Here, we have employed a reciprocal cross-infection experiment to unravel the adaptive responses of two components of fitness affecting both parties with different complexities of the underlying genetic architecture (i.e. mortality and spore load). Furthermore, our experimental coevolution of hosts (Tribolium castaneum) and parasites (Nosema whitei) included paired replicates of naive hosts from identical genetic backgrounds to allow separation between host- and parasite-specific responses.

Results

In hosts, coevolution led to higher resistance and altered resistance profiles compared to paired control lines. Host genotype × parasite genotype interactions (G_H × G_P) were observed for spore load (the trait of lower genetic complexity), but not for mortality. Overall parasite performance correlated with resistance of its matching host coevolution background reflecting a directional and unspecific response to strength of selection during coevolution. Despite high selective pressures exerted by the obligatory killing parasite, and host- and parasite-specific mortality profiles, no general pattern of local adaptation was observed, but one case of parasite maladaptation was consistently observed on both coevolved and control host populations. In addition, the use of replicate control host populations in the assay revealed one case of host maladaptation and one case of parasite adaptation that was masked by host counter-adaptation, suggesting the presence of complex and probably dynamically changing fitness landscapes.

Conclusions

Our results demonstrate that the use of replicate naive populations can be a useful tool to differentiate between host and parasite adaptation in complex and dynamic fitness landscapes. The absence of clear local adaptation patterns during coevolution with a sexual host showing a complex genetic architecture for resistance suggests that directional selection for generality may be more important attributes of host-parasite coevolution than commonly assumed.