RESUMEN
Parasite proliferations within/on the host form the basis of the outcome of all infectious diseases. However, within-host dynamics are difficult to study in vertebrates, as it requires regularly following pathogen proliferation from the start of the infection and at the organismal level. Invertebrate models allow for this monitoring under controlled conditions using population approaches. These approaches offer the possibility to describe many parameters of the within-host dynamics, such as rate of proliferation, probability to control the infection, and average time at which the pathogen is controlled. New parameters such as the Pathogen Load Upon Death and the Set-Point Pathogen Load have emerged to characterize within-host dynamics and better understand disease outcome. While contextualizing the potential of studying within-host dynamics in insects to build fundamental knowledge, we review what we know about within-host dynamics using insect models, and what it can offer to our knowledge of infectious diseases.
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Enfermedades Transmisibles , Insectos , Animales , Insectos/parasitologíaRESUMEN
The gut is the primary interface between an animal and food, but how it adapts to qualitative dietary variation is poorly defined. We find that the Drosophila midgut plastically resizes following changes in dietary composition. A panel of nutrients collectively promote gut growth, which sugar opposes. Diet influences absolute and relative levels of enterocyte loss and stem cell proliferation, which together determine cell numbers. Diet also influences enterocyte size. A high sugar diet inhibits translation and uncouples intestinal stem cell proliferation from expression of niche-derived signals, but, surprisingly, rescuing these effects genetically was not sufficient to modify diet's impact on midgut size. However, when stem cell proliferation was deficient, diet's impact on enterocyte size was enhanced, and reducing enterocyte-autonomous TOR signaling was sufficient to attenuate diet-dependent midgut resizing. These data clarify the complex relationships between nutrition, epithelial dynamics, and cell size, and reveal a new mode of plastic, diet-dependent organ resizing.
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Dieta , Drosophila melanogaster/crecimiento & desarrollo , Tracto Gastrointestinal/crecimiento & desarrollo , Animales , Animales Modificados Genéticamente , Proliferación Celular , Drosophila melanogaster/fisiología , Enterocitos/citología , Femenino , Tracto Gastrointestinal/citología , Tracto Gastrointestinal/fisiología , Masculino , Nicho de Células MadreRESUMEN
Developmental plasticity can match organismal phenotypes to ecological conditions, helping populations to deal with the environmental heterogeneity of alternating seasons. In contrast to natural situations, experimental studies of plasticity often use environmental conditions that are held constant during development. To explore potential interactions between day and night temperatures, we tested effects of circadian temperature fluctuations on thermally plastic traits in a seasonally plastic butterfly, Bicyclus anynana. Comparing phenotypes for four treatments corresponding to a full-factorial analysis of cooler and warmer temperatures, we found evidence of significant interaction effects between day and night temperatures. We then focused on comparing phenotypes between individuals reared under two types of temperature fluctuations (warmer days with cooler nights, and cooler days with warmer nights) and individuals reared under a constant temperature of the same daily mean. We found evidence of additive-like effects (for body size), and different types of dominance-like effects, with one particular period of the light cycle (for development time) or one particular extreme temperature (for eyespot size) having a larger impact on phenotype. Differences between thermally plastic traits, which together underlie alternative seasonal strategies for survival and reproduction, revealed their independent responses to temperature. This study underscores the value of studying how organisms integrate complex environmental information toward a complete understanding of natural phenotypic variation and of the impact of environmental change thereon.
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Mariposas Diurnas , Plásticos , Adaptación Fisiológica , Animales , Humanos , Fenotipo , Estaciones del Año , TemperaturaRESUMEN
During an infection, parasites face a succession of challenges, each decisive for disease outcome. The diversity of challenges requires a series of parasite adaptations to successfully multiply and transmit from host to host. Thus, the pathogen genotypes that succeed during one step might be counterselected in later stages of the infection. Using the bacterium Xenorhabdus nematophila and adult Drosophila melanogaster flies as hosts, we showed that such step-specific adaptations, here linked to GASP (i.e., growth advantage in stationary phase) mutations in the X. nematophila master gene regulator lrp, exist and can trade off with each other. We found that nonsense lrp mutations had lowered the ability to resist the host immune response, while all classes of mutations in lrp were associated with a decrease in the ability to proliferate during early infection. We demonstrate that reduced proliferation of X. nematophila best explains diminished virulence in this infection model. Finally, decreased proliferation during the first step of infection is accompanied by improved proliferation during late infection, suggesting a trade-off between the adaptations to each step. Step-specific adaptations could play a crucial role in the chronic phase of infections in any disease organisms that show similar small colony variants (SCVs) to X. nematophilaIMPORTANCE Within-host evolution has been described in many bacterial diseases, and the genetic basis behind the adaptations has stimulated a lot of interest. Yet, the studied adaptations are generally focused on antibiotic resistance and rarely on the adaptation to the environment given by the host, and the potential trade-offs hindering adaptations to each step of the infection are rarely considered. Those trade-offs are key to understanding intrahost evolution and thus the dynamics of the infection. However, understanding these trade-offs supposes a detailed study of host-pathogen interactions at each step of the infection process, with an adapted methodology for each step. Using Drosophila melanogaster as the host and the bacterium Xenorhabdus nematophila, we investigated the bacterial adaptations resulting from GASP mutations known to induce the small colony variant (SCV) phenotype positively selected within the host over the course of an infection, as well as the trade-off between step-specific adaptations.
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Drosophila melanogaster/microbiología , Mutación , Xenorhabdus/genética , Animales , Carga Bacteriana , Proteínas Bacterianas/genética , Proteínas Bacterianas/metabolismo , Regulación Bacteriana de la Expresión Génica , Interacciones Huésped-Patógeno/fisiología , Masculino , Fenotipo , Virulencia/genéticaRESUMEN
Genes of the major histocompatibility complex (MHC) play a pivotal role in parasite resistance, and their allelic diversity has been associated with fitness variations in several taxa. However, studies report inconsistencies in the direction of this association, with either positive, quadratic or no association being described. These discrepancies may arise because the fitness costs and benefits of MHC diversity differ among individuals depending on their exposure and immune responses to parasites. Here, we investigated in black-legged kittiwake (Rissa tridactyla) chicks whether associations between MHC class-II diversity and fitness vary with sex and hatching order. MHC-II diversity was positively associated with growth and tick clearance in female chicks, but not in male chicks. Our data also revealed a positive association between MHC-II diversity and survival in second-hatched female chicks (two eggs being the typical clutch size). These findings may result from condition-dependent parasite infections differentially impacting sexes in relation to hatching order. We thus suggest that it may be important to account for individual heterogeneities in traits that potentially exert selective pressures on MHC diversity in order to properly predict MHC-fitness associations.
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Charadriiformes , Parásitos , Alelos , Animales , Charadriiformes/genética , Femenino , Variación Genética , Antígenos de Histocompatibilidad Clase II/genética , Complejo Mayor de Histocompatibilidad/genética , Masculino , Selección GenéticaRESUMEN
To understand the mechanisms of antagonistic coevolution, it is crucial to identify the genetics of parasite resistance. In the Daphnia magna-Pasteuria ramosa host-parasite system, the most important step of the infection process is the one in which P. ramosa spores attach to the host's foregut. A matching-allele model (MAM) describes the host-parasite genetic interactions underlying attachment success. Here we describe a new P. ramosa genotype, P15, which, unlike previously studied genotypes, attaches to the host's hindgut, not to its foregut. Host resistance to P15 attachment shows great diversity across natural populations. In contrast to P. ramosa genotypes that use foregut attachment, P15 shows some quantitative variation in attachment success and does not always lead to successful infections, suggesting that hindgut attachment represents a less-efficient infection mechanism than foregut attachment. Using a Quantitative Trait Locus (QTL) approach, we detect two significant QTLs in the host genome: one that co-localizes with the previously described D. magna PR locus of resistance to foregut attachment, and a second, major QTL located in an unlinked genomic region. We find no evidence of epistasis. Fine mapping reveals a genomic region, the D locus, of ~13 kb. The discovery of a second P. ramosa attachment site and of a novel host-resistance locus increases the complexity of this system, with implications for both for the coevolutionary dynamics (e.g., Red Queen and the role of recombination), and for the evolution and epidemiology of the infection process.
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Infecciones Bacterianas , Daphnia/genética , Resistencia a la Enfermedad/genética , Pasteuria , Animales , Daphnia/microbiología , Interacciones Huésped-Patógeno/genética , Pasteuria/genética , Sitios de Carácter CuantitativoRESUMEN
In diet metabarcoding analyses, insufficient taxonomic coverage of PCR primer sets generates false negatives that may dramatically distort biodiversity estimates. In this paper, we investigated the taxonomic coverage and complementarity of three cytochrome c oxidase subunit I gene (COI) primer sets based on in silico analyses and we conducted an in vivo evaluation using fecal and spider web samples from different invertivores, environments, and geographic locations. Our results underline the lack of predictability of both the coverage and complementarity of individual primer sets: (a) sharp discrepancies exist observed between in silico and in vivo analyses (to the detriment of in silico analyses); (b) both coverage and complementarity depend greatly on the predator and on the taxonomic level at which preys are considered; (c) primer sets' complementarity is the greatest at fine taxonomic levels (molecular operational taxonomic units [MOTUs] and variants). We then formalized the "one-locus-several-primer-sets" (OLSP) strategy, that is, the use of several primer sets that target the same locus (here the first part of the COI gene) and the same group of taxa (here invertebrates). The proximal aim of the OLSP strategy is to minimize false negatives by increasing total coverage through multiple primer sets. We illustrate that the OLSP strategy is especially relevant from this perspective since distinct variants within the same MOTUs were not equally detected across all primer sets. Furthermore, the OLSP strategy produces largely overlapping and comparable sequences, which cannot be achieved when targeting different loci. This facilitates the use of haplotypic diversity information contained within metabarcoding datasets, for example, for phylogeography and finer analyses of prey-predator interactions.
RESUMEN
The sexes show profound differences in responses to infection and the development of autoimmunity. Dimorphisms in immune responses are ubiquitous across taxa, from arthropods to vertebrates. Drosophila melanogaster shows strong sex dimorphisms in immune system responses at baseline, upon pathogenic challenge, and over aging. We have performed an exhaustive survey of peer-reviewed literature on Drosophila immunity, and present a database of publications indicating the sex(es) analyzed in each study. While we found a growing interest in the community in adult immunity and in reporting both sexes, the main body of work in this field uses only one sex, or does not stratify by sex. We synthesize evidence for sexually dimorphic responses to bacterial, viral, and fungal infections. Dimorphisms may be mediated by distinct immune compartments, and we review work on sex differences in behavioral, epithelial, cellular, and systemic (fat body-mediated) immunity. Emerging work on sexually dimorphic aging of immune tissues, immune senescence, and inflammation are examined. We consider evolutionary drivers for sex differences in immune investment, highlight the features of Drosophila biology that make it particularly amenable to studies of immune dimorphisms, and discuss areas for future exploration.
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Enfermedades de los Animales/etiología , Drosophila melanogaster/inmunología , Interacciones Huésped-Patógeno/inmunología , Inmunidad Innata , Caracteres Sexuales , Factores de Edad , Animales , Conducta Animal , Evolución Biológica , Femenino , MasculinoRESUMEN
Body size is a quantitative trait that is closely associated to fitness and under the control of both genetic and environmental factors. While developmental plasticity for this and other traits is heritable and under selection, little is known about the genetic basis for variation in plasticity that can provide the raw material for its evolution. We quantified genetic variation for body size plasticity in Drosophila melanogaster by measuring thorax and abdomen length of females reared at two temperatures from a panel representing naturally segregating alleles, the Drosophila Genetic Reference Panel (DGRP). We found variation between genotypes for the levels and direction of thermal plasticity in size of both body parts. We then used a Genome-Wide Association Study (GWAS) approach to unravel the genetic basis of inter-genotype variation in body size plasticity, and used different approaches to validate selected QTLs and to explore potential pleiotropic effects. We found mostly "private QTLs", with little overlap between the candidate loci underlying variation in plasticity for thorax versus abdomen size, for different properties of the plastic response, and for size versus size plasticity. We also found that the putative functions of plasticity QTLs were diverse and that alleles for higher plasticity were found at lower frequencies in the target population. Importantly, a number of our plasticity QTLs have been targets of selection in other populations. Our data sheds light onto the genetic basis of inter-genotype variation in size plasticity that is necessary for its evolution.
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Variación Biológica Poblacional/genética , Tamaño Corporal/genética , Drosophila melanogaster/fisiología , Evolución Molecular , Sitios de Carácter Cuantitativo/genética , Alelos , Animales , Animales Modificados Genéticamente , Femenino , Variación Genética , Estudio de Asociación del Genoma Completo , Genotipo , Fenotipo , Selección Genética , TemperaturaRESUMEN
Resistance to insecticides has evolved in multiple insect species, leading to increased application rates and even control failures. Understanding the genetic basis of insecticide resistance is fundamental for mitigating its impact on crop production and disease control. We performed a GWAS approach with the Drosophila Genetic Reference Panel (DGRP) to identify the mutations involved in resistance to two widely used classes of insecticides: organophosphates (OPs, parathion) and pyrethroids (deltamethrin). Most variation in parathion resistance was associated with mutations in the target gene Ace, while most variation in deltamethrin resistance was associated with mutations in Cyp6a23, a gene encoding a detoxification enzyme never previously associated with resistance. A "nested GWAS" further revealed the contribution of other loci: Dscam1 and trpl were implicated in resistance to parathion, but only in lines lacking WolbachiaCyp6a17, the paralogous gene of Cyp6a23, and CG7627, an ATP-binding cassette transporter, were implicated in deltamethrin resistance. We observed signatures of recent selective sweeps at all of these resistance loci and confirmed that the soft sweep at Ace is indeed driven by the identified resistance mutations. Analysis of allele frequencies in additional population samples revealed that most resistance mutations are segregating across the globe, but that frequencies can vary substantially among populations. Altogether, our data reveal that the widely used OP and pyrethroid insecticides imposed a strong selection pressure on natural insect populations. However, it remains unclear why, in Drosophila, resistance evolved due to changes in the target site for OPs, but due to a detoxification enzyme for pyrethroids.
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Drosophila melanogaster/genética , Genoma de los Insectos , Resistencia a los Insecticidas/genética , Animales , Drosophila melanogaster/efectos de los fármacos , Femenino , Variación Genética , Estudio de Asociación del Genoma Completo , Insecticidas/toxicidad , Masculino , Organofosfatos/toxicidad , Piretrinas/toxicidad , Selección GenéticaRESUMEN
Organisms with complex life cycles can differ markedly in their biology across developmental life stages. Consequently, distinct life stages can represent drastically different environments for parasites. This difference is especially striking with holometabolous insects, which have dramatically different larval and adult life stages, bridged by a complete metamorphosis. There is no a priori guarantee that a parasite infecting the larval stage would be able to persist into the adult stage. In fact, to our knowledge, transstadial transmission of extracellular pathogens has never been documented in a host that undergoes complete metamorphosis. We tested the hypothesis that a bacterial parasite originally sampled from an adult host could infect a larva, then survive through metamorphosis and persist into the adult stage. As a model, we infected the host Drosophila melanogaster with a horizontally transmitted, extracellular bacterial pathogen, Providencia rettgeri We found that this natural pathogen survived systemic infection of larvae (L3) and successfully persisted into the adult host. We then discuss how it may be adaptive for bacteria to transverse life stages and even minimize virulence at the larval stage in order to benefit from adult dispersal.
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Drosophila melanogaster/microbiología , Metamorfosis Biológica , Providencia/fisiología , Animales , Larva/microbiologíaRESUMEN
BACKGROUND: Host sexual dimorphism is being increasingly recognized to generate strong differences in the outcome of infectious disease, but the mechanisms underlying immunological differences between males and females remain poorly characterized. Here, we used Drosophila melanogaster to assess and dissect sexual dimorphism in the innate response to systemic bacterial infection. RESULTS: We demonstrated sexual dimorphism in susceptibility to infection by a broad spectrum of Gram-positive and Gram-negative bacteria. We found that both virgin and mated females are more susceptible than mated males to most, but not all, infections. We investigated in more detail the lower resistance of females to infection with Providencia rettgeri, a Gram-negative bacterium that naturally infects D. melanogaster. We found that females have a higher number of phagocytes than males and that ablation of hemocytes does not eliminate the dimorphism in resistance to P. rettgeri, so the observed dimorphism does not stem from differences in the cellular response. The Imd pathway is critical for the production of antimicrobial peptides in response to Gram-negative bacteria, but mutants for Imd signaling continued to exhibit dimorphism even though both sexes showed strongly reduced resistance. Instead, we found that the Toll pathway is responsible for the dimorphism in resistance. The Toll pathway is dimorphic in genome-wide constitutive gene expression and in induced response to infection. Toll signaling is dimorphic in both constitutive signaling and in induced activation in response to P. rettgeri infection. The dimorphism in pathway activation can be specifically attributed to Persephone-mediated immune stimulation, by which the Toll pathway is triggered in response to pathogen-derived virulence factors. We additionally found that, in absence of Toll signaling, males become more susceptible than females to the Gram-positive Enterococcus faecalis. This reversal in susceptibility between male and female Toll pathway mutants compared to wildtype hosts highlights the key role of the Toll pathway in D. melanogaster sexual dimorphism in resistance to infection. CONCLUSION: Altogether, our data demonstrate that Toll pathway activity differs between male and female D. melanogaster in response to bacterial infection, thus identifying innate immune signaling as a determinant of sexual immune dimorphism.
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Proteínas de Drosophila/genética , Proteínas de Drosophila/inmunología , Drosophila melanogaster/genética , Drosophila melanogaster/microbiología , Bacterias Gramnegativas/fisiología , Bacterias Grampositivas/fisiología , Receptores Toll-Like/inmunología , Animales , Resistencia a la Enfermedad/genética , Drosophila melanogaster/inmunología , Femenino , Bacterias Gramnegativas/inmunología , Bacterias Grampositivas/inmunología , Masculino , Caracteres SexualesRESUMEN
A central problem in infection biology is understanding why two individuals exposed to identical infections have different outcomes. We have developed an experimental model where genetically identical, co-housed Drosophila given identical systemic infections experience different outcomes, with some individuals succumbing to acute infection while others control the pathogen as an asymptomatic persistent infection. We found that differences in bacterial burden at the time of death did not explain the two outcomes of infection. Inter-individual variation in survival stems from variation in within-host bacterial growth, which is determined by the immune response. We developed a model that captures bacterial growth dynamics and identifies key factors that predict the infection outcome: the rate of bacterial proliferation and the time required for the host to establish an effective immunological control. Our results provide a framework for studying the individual host-pathogen parameters governing the progression of infection and lead ultimately to life or death.
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Infecciones Bacterianas/inmunología , Infecciones Bacterianas/patología , Drosophila melanogaster/fisiología , Interacciones Huésped-Patógeno , Animales , Modelos Animales de Enfermedad , Drosophila melanogaster/inmunología , Drosophila melanogaster/microbiología , Análisis de SupervivenciaRESUMEN
The infection process of many diseases can be divided into series of steps, each one required to successfully complete the parasite's life and transmission cycle. This approach often reveals that the complex phenomenon of infection is composed of a series of more simple mechanisms. Here we demonstrate that a population biology approach, which takes into consideration the natural genetic and environmental variation at each step, can greatly aid our understanding of the evolutionary processes shaping disease traits. We focus in this review on the biology of the bacterial parasite Pasteuria ramosa and its aquatic crustacean host Daphnia, a model system for the evolutionary ecology of infectious disease. Our analysis reveals tremendous differences in the degree to which the environment, host genetics, parasite genetics and their interactions contribute to the expression of disease traits at each of seven different steps. This allows us to predict which steps may respond most readily to selection and which steps are evolutionarily constrained by an absence of variation. We show that the ability of Pasteuria to attach to the host's cuticle (attachment step) stands out as being strongly influenced by the interaction of host and parasite genotypes, but not by environmental factors, making it the prime candidate for coevolutionary interactions. Furthermore, the stepwise approach helps us understanding the evolution of resistance, virulence and host ranges. The population biological approach introduced here is a versatile tool that can be easily transferred to other systems of infectious disease.
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Daphnia/microbiología , Pasteuria/fisiología , Animales , Evolución Biológica , Daphnia/genética , Ambiente , Especificidad del Huésped , Interacciones Huésped-Patógeno , Pasteuria/genética , Pasteuria/patogenicidad , Filogenia , VirulenciaRESUMEN
The existence of immunological memory in invertebrates remains a contentious topic. Exposure of Daphnia magna crustaceans to a noninfectious dose of the bacterium Pasteuria ramosa has been reported to reduce the chance of future infection upon exposure to higher doses. Using clonal hosts and parasites, we tested whether initial exposure of the host to the parasite (priming), followed by clearing of the parasite with antibiotic, protects the host from a second exposure (challenge). Our experiments included three treatments: priming and challenge with the same or with a different parasite clone, or no priming. Two independent experiments showed that both the likelihood of infection and the degree of parasite proliferation did not differ between treatments, supporting the conclusion that there is no immunological memory in this system. We discuss the possibility that previous discordant reports could result from immune or stress responses that did not fade following initial priming.
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Daphnia/inmunología , Infecciones por Bacterias Grampositivas/inmunología , Memoria Inmunológica , Pasteuria/inmunología , Animales , Antibacterianos/uso terapéutico , Infecciones por Bacterias Grampositivas/tratamiento farmacológico , Interacciones Huésped-Patógeno , Inmunidad Innata , Recurrencia , VacunaciónRESUMEN
Within the mated reproductive tracts of females of many taxa, seminal fluid proteins (SFPs) coagulate into a structure known as the mating plug (MP). MPs have diverse roles, including preventing female remating, altering female receptivity postmating, and being necessary for mated females to successfully store sperm. The Drosophila melanogaster MP, which is maintained in the mated female for several hours postmating, is comprised of a posterior MP (PMP) that forms quickly after mating begins and an anterior MP (AMP) that forms later. The PMP is composed of seminal proteins from the ejaculatory bulb (EB) of the male reproductive tract. To examine the role of the PMP protein PEBme in D. melanogaster reproduction, we identified an EB GAL4 driver and used it to target PEBme for RNA interference (RNAi) knockdown. PEBme knockdown in males compromised PMP coagulation in their mates and resulted in a significant reduction in female fertility, adversely affecting postmating uterine conformation, sperm storage, mating refractoriness, egg laying, and progeny generation. These defects resulted from the inability of females to retain the ejaculate in their reproductive tracts after mating. The uncoagulated MP impaired uncoupling by the knockdown male, and when he ultimately uncoupled, the ejaculate was often pulled out of the female. Thus, PEBme and MP coagulation are required for optimal fertility in D. melanogaster. Given the importance of the PMP for fertility, we identified additional MP proteins by mass spectrometry and found fertility functions for two of them. Our results highlight the importance of the MP and the proteins that comprise it in reproduction and suggest that in Drosophila the PMP is required to retain the ejaculate within the female reproductive tract, ensuring the storage of sperm by mated females.
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Proteínas de Drosophila/metabolismo , Drosophila melanogaster/metabolismo , Eyaculación , Animales , Proteínas de Drosophila/deficiencia , Proteínas de Drosophila/genética , Drosophila melanogaster/fisiología , Femenino , Fertilidad , Técnicas de Silenciamiento del Gen , Masculino , Interferencia de ARN , Conducta Sexual Animal , Espermatozoides/metabolismo , Útero/metabolismoRESUMEN
A parasite's host range can have important consequences for ecological and evolutionary processes but can be difficult to infer. Successful infection depends on the outcome of multiple steps and only some steps of the infection process may be critical in determining a parasites host range. To test this hypothesis, we investigated the host range of the bacterium Pasteuria ramosa, a Daphnia parasite, and determined the parasites success in different stages of the infection process. Multiple genotypes of Daphnia pulex, Daphnia longispina and Daphnia magna were tested with four Pasteuria genotypes using infection trials and an assay that determines the ability of the parasite to attach to the hosts esophagus. We find that attachment is not specific to host species but is specific to host genotype. This may suggest that alleles on the locus controlling attachment are shared among different host species that diverged 100 million year. However, in our trials, Pasteuria was never able to reproduce in nonnative host species, suggesting that Pasteuria infecting different host species are different varieties, each with a narrow host range. Our approach highlights the explanatory power of dissecting the steps of the infection process and resolves potentially conflicting reports on parasite host ranges.
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Daphnia/genética , Evolución Molecular , Especificidad del Huésped/genética , Pasteuria/genética , Polimorfismo Genético , Animales , Daphnia/microbiología , Genotipo , Pasteuria/patogenicidadRESUMEN
The maintenance of genetic variation and sex despite its costs has long puzzled biologists. A popular idea, the Red Queen Theory, is that under rapid antagonistic coevolution between hosts and their parasites, the formation of new rare host genotypes through sex can be advantageous as it creates host genotypes to which the prevailing parasite is not adapted. For host-parasite coevolution to lead to an ongoing advantage for rare genotypes, parasites should infect specific host genotypes and hosts should resist specific parasite genotypes. The most prominent genetics capturing such specificity are matching-allele models (MAMs), which have the key feature that resistance for two parasite genotypes can reverse by switching one allele at one host locus. Despite the lack of empirical support, MAMs have played a central role in the theoretical development of antagonistic coevolution, local adaptation, speciation, and sexual selection. Using genetic crosses, we show that resistance of the crustacean Daphnia magna against the parasitic bacterium Pasteuria ramosa follows a MAM. Simulation results show that the observed genetics can explain the maintenance of genetic variation and contribute to the maintenance of sex in the facultatively sexual host as predicted by the Red Queen Theory.
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Daphnia/inmunología , Daphnia/microbiología , Interacciones Huésped-Parásitos/genética , Pasteuria/patogenicidad , Adaptación Fisiológica , Alelos , Animales , Evolución Biológica , Daphnia/genética , Variación Genética , Genotipo , Interacciones Huésped-Parásitos/inmunologíaRESUMEN
BACKGROUND: Males and females differ in many ways and might present different opportunities and challenges to their parasites. In the same way that parasites adapt to the most common host type, they may adapt to the characteristics of the host sex they encounter most often. To explore this hypothesis, we characterized host sex-specific effects of the parasite Pasteuria ramosa, a bacterium evolving in naturally, strongly, female-biased populations of its host Daphnia magna. RESULTS: We show that the parasite proliferates more successfully in female hosts than in male hosts, even though males and females are genetically identical. In addition, when exposure occurred when hosts expressed a sexual dimorphism, females were more infected. In both host sexes, the parasite causes a similar reduction in longevity and leads to some level of castration. However, only in females does parasite-induced castration result in the gigantism that increases the carrying capacity for the proliferating parasite. CONCLUSIONS: We show that mature male and female Daphnia represent different environments and reveal one parasite-induced symptom (host castration), which leads to increased carrying capacity for parasite proliferation in female but not male hosts. We propose that parasite induced host castration is a property of parasites that evolved as an adaptation to specifically exploit female hosts.
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Daphnia/microbiología , Daphnia/parasitología , Interacciones Huésped-Parásitos/fisiología , Parásitos/crecimiento & desarrollo , Pasteuria/crecimiento & desarrollo , Caracteres Sexuales , Animales , Sesgo , Recuento de Células , Daphnia/anatomía & histología , Femenino , Masculino , Espermatozoides/citología , Espermatozoides/microbiología , Espermatozoides/parasitología , Esporas Bacterianas/crecimiento & desarrollo , Análisis de SupervivenciaRESUMEN
Parasitic infections consist of a succession of steps during which hosts and parasites interact in specific manners. At each step, hosts can use diverse defence mechanisms to counteract the parasite's attempts to invade and exploit them. Of these steps, the penetration of parasites into the host is a key step for a successful infection and the epithelium is the first line of host defence. The shedding of this protective layer (moulting) is a crucial feature in the life cycle of several invertebrate and vertebrate taxa, and is generally considered to make hosts vulnerable to parasites and predators. Here, we used the crustacean Daphnia magna to test whether moulting influences the likelihood of infection by the castrating bacterium Pasteuria ramosa. This parasite is known to attach to the host cuticula before penetrating into its body. We found that the likelihood of successful parasite infection is greatly reduced if the host moults within 12 h after parasite exposure. Thus, moulting is beneficial for the host being exposed to this parasite. We further show that exposure to the parasite does not induce hosts to moult earlier. We discuss the implications of our findings for host and parasite evolution and epidemiology.