Minimal selfing, few clones, and no among-host genetic structure in a hermaphroditic parasite with asexual larval propagation

Little is known about actual mating systems in natural populations of parasites or about what constitutes the limits of a parasite deme. These parameters are interesting because they affect levels of genetic diversity, opportunities for local adaptation, and other evolutionary processes. We expect that transmission dynamics and the distribution of parasites among hosts should have a large effect on mating systems and demic structure, but currently we have mostly speculation and very few data. For example, infrapopulations (all the parasites in a single host) should behave as demes if parasite offspring are transmitted as a clump from host to host over several generations. However, if offspring are well mixed, then the parasite component population (all the parasites among a host population) would function as the deme. Similarly, low mean intensities or a high proportion of worms in single infections should increase the selfing rate. For species having an asexual amplification stage, transmission between intermediate and definitive (final) hosts will control the variance in clonal reproductive success, which in turn could have a large influence on effective sizes and rates of inbreeding. We examined demic structure, selfing rates, and the variance in clonal reproductive success in natural populations of Plagioporus shawi, a hermaphroditic trematode that parasitizes salmon. Overall levels of genetic diversity were very high. An a posteriori inference of population structure overwhelmingly supports the component population as the deme, rather than individual infrapopulations. Only a single pair of 597 adult individuals was identified as clones. Thus, the variance in clonal reproductive success was almost zero. Despite being hermaphroditic, P. shawi appears to be almost entirely outcrossing. Genetic estimates of selfing (<5%) were in accordance with the proportion of parasites from single infections. Thus, it appears that individual flukes outcross whenever possible and only resort to selfing when alone. Finally, our data support the hypothesis that aquatic transmission and the use of several intermediate hosts promotes high genetic diversity and well-mixed infrapopulations.     

The total opportunity for sexual selection and the integration of pre‐ and post‐mating episodes of sexual selection in a complex world

It is well known that sexual selection can target reproductive traits during successive pre‐ and post‐mating episodes of selection. A key focus of recent studies has been to understand and quantify how these episodes of sexual selection interact to determine overall variance in reproductive success. In this article, we review empirical developments in this field but also highlight the considerable variability in patterns of pre‐ and post‐mating sexual selection, attributable to variation in patterns of resource acquisition and allocation, ecological and social factors, genotype‐by‐environment interaction and possible methodological factors that might obscure such patterns. Our aim is to highlight how (co)variances in pre‐ and post‐mating sexually selected traits can be sensitive to changes in a range of ecological and environmental variables. We argue that failure to capture this variation when quantifying the opportunity for sexual selection may lead to erroneous conclusions about the strength, direction or form of sexual selection operating on pre‐ and post‐mating traits. Overall, we advocate for approaches that combine measures of pre‐ and post‐mating selection across contrasting environmental or ecological gradients to better understand the dynamics of sexual selection in polyandrous species. We also discuss some directions for future research in this area.     

Age‐dependent trajectories differ between within‐pair and extra‐pair paternity success

Reproductive success is associated with age in many taxa, increasing in early life followed by reproductive senescence. In socially monogamous but genetically polygamous species, this generates the interesting possibility of differential trajectories of within‐pair and extra‐pair siring success with age in males. We investigate these relationships simultaneously using within‐individual analyses with 13 years of data from an insular house sparrow (Passer domesticus) population. As expected, we found that both within‐ and extra‐pair paternity success increased with age, followed by a senescence‐like decline. However, the age trajectories of within‐ and extra‐pair paternity successes differed significantly, with the extra‐pair paternity success increasing faster, although not significantly, in early life, and showing a delayed decline by 1.5 years on average later in life compared to within‐pair paternity success. These different trajectories indicate that the two alternative mating tactics should have age‐dependent pay‐offs. Males may partition their reproductive effort between within‐ and extra‐pair matings depending on their current age to reap the maximal combined benefit from both strategies. The interplay between these mating strategies and age‐specific mortality may explain the variation in rates of extra‐pair paternity observed within and between species.     

Red Queen dancing in the lek: effects of mating skew on host–parasite interactions

The RQH (Red Queen hypothesis), which argues that hosts need to be continuously finding new ways to avoid parasites that are able to infect common host genotypes, has been at the center of discussions on the maintenance of sex. This is because diversity is favored under the host–parasite coevolution based on negative frequency‐dependent selection, and sexual reproduction is a mechanism that generates genetic diversity in the host population. Together with parasite infections, sexual organisms are usually under sexual selection, which leads to mating skew or mating success biased toward males with a particular phenotype. Thus, strong mating skew would affect genetic variance in a population and should affect the benefit of the RQH. However, most models have investigated the RQH under a random mating system and not under mating skew. In this study, I show that sexual selection and the resultant mating skew may increase parasite load in the hosts. An IBM (individual‐based model), which included host–parasite interactions and sexual selection among hosts, demonstrates that mating skew influenced parasite infection in the hosts under various conditions. Moreover, the IBM showed that the mating skew evolves easily in cases of male–male competition and female mate choice, even though it imposes an increased risk of parasite infection on the hosts. These findings indicated that whether the RQH favored sexual reproduction depended on the condition of mating skew. That is, consideration of the host mating system would provide further understanding of conditions in which the RQH favors sexual reproduction in real organisms.     

Reproductive isolating barriers between colour‐differentiated populations of an African annual killifish,Nothobranchius korthausae (Cyprinodontiformes)

Allopatric populations separated by vicariance events are expected to evolve reproductive isolating mechanisms as a result of disparate selection pressures and genetic drift. The appearance of reproductive isolating mechanisms may vary across taxa with differences in the opportunity for mate choice, and may be asymmetrical. In addition, premating barriers may be affected by individual mating experience. We used choice and no‐choice experiments to investigate reproductive isolation between two allopatric (island and mainland) and colour‐differentiated populations of an African annual fish, Nothobranchius korthausae. Assortative mating under experimental conditions was limited and asymmetrical. Preference for sympatric males was only expressed in nonvirgin females from one population. Virgin fish from both populations mated indiscriminately. No difference in the number of eggs laid, fertilization rate and hatching success was detected in no‐choice experiments. All mating combinations produced viable offspring and no postmating barriers were detected in terms of the performance and fertility of F1 hybrids. Overall, we found little evidence for significant reproductive isolation, which is in contrast with the related killifish taxa in which assortative mating can be strong, even among allopatric populations with no colour differentiation. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 62–72.     

Stochastic exits from dormancy give rise to heavy‐tailed distributions of descendants in bacterial populations

Variance in reproductive success is a major determinant of the degree of genetic drift in a population. While many plants and animals exhibit high variance in their number of progeny, far less is known about these distributions for microorganisms. Here, we used a strain barcoding approach to quantify variability in offspring number among replicate bacterial populations and developed a Bayesian method to infer the distribution of descendants from this variability. We applied our approach to measure the offspring distributions for five strains of bacteria from the genus Streptomyces after germination and growth in a homogenous laboratory environment. The distributions of descendants were heavy‐tailed, with a few cells effectively ‘winning the jackpot’ to become a disproportionately large fraction of the population. This extreme variability in reproductive success largely traced back to initial populations of spores stochastically exiting dormancy, which provided early‐germinating spores with an exponential advantage. In simulations with multiple dormancy cycles, heavy‐tailed distributions of descendants decreased the effective population size by many orders of magnitude and led to allele dynamics differing substantially from classical population genetics models with matching effective population size. Collectively, these results demonstrate that extreme variability in reproductive success can occur even in growth conditions that are far more homogeneous than the natural environment. Thus, extreme variability in reproductive success might be an important factor shaping microbial population dynamics with implications for predicting the fate of beneficial mutations, interpreting sequence variability within populations and explaining variability in infection outcomes across patients.     

Role of parasite transmission in promoting inbreeding: I. Infection intensities drive individual parasite selfing rates

Among parasitic organisms, inbreeding has been implicated as a potential driver of host–parasite co‐evolution, drug‐resistance evolution and parasite diversification. Yet, fundamental topics about how parasite life histories impact inbreeding remain to be addressed. In particular, there are no direct selfing‐rate estimates for hermaphroditic parasites in nature. Our objectives were to elucidate the mating system of a parasitic flatworm in nature and to understand how aspects of parasite transmission could influence the selfing rates of individual parasites. If there is random mating within hosts, the selfing rates of individual parasites would be an inverse power function of their infection intensities. We tested whether selfing rates deviated from within‐host random mating expectations with the tapeworm Oochoristica javaensis. In doing so, we generated, for the first time in nature, individual selfing‐rate estimates of a hermaphroditic flatworm parasite. There was a mixed‐mating system where tapeworms self‐mated more than expected with random mating. Nevertheless, individual selfing rates still had a significant inverse power relationship to infection intensities. The significance of this finding is that the distribution of parasite infection intensities among hosts, an emergent property of the transmission process, can be a key driver in shaping the primary mating system, and hence the level of inbreeding in the parasite population. Moreover, we demonstrated how potential population selfing rates can be estimated using the predicted relationship of individual selfing rates to intensities and showed how the distribution of parasites among hosts can indirectly influence the primary mating system when there is density‐dependent fecundity.     

The epidemiology underlying age‐related avian malaria infection in a long‐lived host: the mute swan Cygnus olor

Quantifying the factors that predict parasite outbreak and persistence is a major challenge for both applied and fundamental biology. Key to understanding parasite prevalence and disease outbreaks is determining at what age individuals show signs of infection, and whether or not they recover. Age‐dependent patterns of the infection of a host population by parasites can indicate among‐individual heterogeneities in their susceptibility to, or rate of recovery from, parasite infections. Here, we present a cross‐sectional study of avian malaria in a long‐lived bird species, the mute swan Cygnus olor, examining age‐related patterns of parasite prevalence and modelling patterns of infection and recovery. One‐hundred and fifteen swans, ranging from one to nineteen years old, were screened for infection with Plasmodium, Haemoproteus and Leucocytozoon parasites. Infections with three cytochrome‐b lineages of Haemoproteus were found (pooled prevalence 67%), namely WW1 (26%), which is common in passerine birds, and two new lineages closely related to WW1: MUTSW1 (25%) and MUTSW2 (16%). We found evidence for age‐related infection in one lineage, MUTSW1. Catalytic models examining patterns of infection and recovery in the population suggested that infections in this population were not life‐long – recovery of individuals was included in the best fitting models. These findings support the results of recent studies that suggest hosts can clear infections, although patterns of infection‐related mortality in older birds remain to be studied in more detail.     

One stimulus—Two responses: Host and parasite life‐history variation in response to environmental stress

Climate change stressors will place different selective pressures on both parasites and their hosts, forcing individuals to modify their life‐history strategies and altering the distribution and prevalence of disease. Few studies have investigated whether parasites are able to respond to host stress and respond by varying their reproductive schedules. Additionally, multiple environmental stressors can limit the ability of a host to respond adaptively to parasite infection. This study compared both host and parasite life‐history parameters in unstressed and drought‐stressed environments using the human parasite, Schistosoma mansoni, in its freshwater snail intermediate host. Snail hosts infected with the parasite demonstrated a significant reproductive burst during the prepatent period (fecundity compensation), but that response was absent in a drought‐stressed environment. This is the first report of the elimination of host fecundity compensation to parasitism when exposed to additional environmental stress. More surprisingly, we found that infections in drought‐stressed snails had significantly higher parasite reproductive outputs than infections in unstressed snails. The finding suggests that climate change may alter the infection dynamics of this human parasite.     

Age‐dependence and individual heterogeneity in reproductive success of greater sage‐grouse

Research on iteroparous species has shown that reproductive success may increase with age until the onset of senescence. However, from the population perspective, increased reproductive success with age could be a consequence of within‐individual variation (e.g. ageing, breeding experience, foraging ability hypotheses), between‐individual variation (e.g. individual heterogeneity, frailty, selection, delayed breeding hypotheses), or a combination thereof. We evaluated within‐ and between‐individual variation in reproductive success of greater sage‐grouse (Centrocercus urophasianus; sage‐grouse), a galliforme of conservation concern throughout western North America. We monitored female reproductive activity from 1998–2010 and used generalized linear mixed models incorporating within‐subject centering to evaluate and separate within‐ and between‐individual effects. We detected positive effects of within‐individual variation on nest initiation and success where ageing increased the likelihood of both parameters, which appears to support the breeding experience and/or foraging ability hypotheses. However, nest initiation was also affected by between‐individual variation whereby the likelihood of initiation was higher for individuals with higher mean age (i.e. survived longer), as is predicted by the frailty and selection hypotheses. Our results indicate both within‐ and between‐individual variation affect reproductive output of sage‐grouse, but the effects of each varied by measure of reproductive output. Our results corroborate previous findings that suggest population age parameters (i.e. cross‐sectional) should be interpreted with caution due to potential entanglement of within‐ and between‐individual processes. Moreover, the relative role and strength of within‐ and between‐individual processes appeared to vary by measure of reproductive output in our results, which further emphasizes the need for longitudinal analysis of age effects, even in relatively short‐lived iteroparous animals, to adequately interpret biological processes.     

Mating status, immune defence, and multi-parasite burden in the damselfly Coenagrion armatum

Immunity and reproductive effort are both physiologically costly and often a trade-off between these functions has been shown. In studies with damselflies, parasite load has been associated with fitness costs, such as reductions in mating success, male condition, and survival. Although each individual may be simultaneously infected by various parasite species, most studies have concentrated on the effects of a single parasite taxon. We examined natural ecto- and endoparasite infection levels in male Coenagrion armatum (Charpentier) (Odonata: Coenagrionidae) damselflies in relation to their mating status, fat reserves, and ability to further mount an immune response, measured as encapsulation of an experimentally introduced foreign object. Encapsulation response was lower for mated (paired) males than for single males and declined with increasing water mite abundance. Mated males had fewer water mites than single males. Male weight or fat reserves did not explain variation in encapsulation response. The number of gregarine gut parasites was not related to the level of encapsulation response and did not differ between mated and single males. However, there was a negative correlation between mite abundance and gregarine load. Our data suggest that current mite infection may compromise a male's resistance against further infections by pathogens and parasites, and there may be a trade-off between reproductive effort and encapsulation response in male C. armatum .     

Morph‐dependent fitness and directional change of morph frequencies over time in a Dutch population of Common buzzards Buteo buteo

How genetic polymorphisms are maintained in a population is a key question in evolutionary ecology. Previous work on a plumage colour polymorphism in the common buzzard Buteo buteo suggested heterozygote advantage as the mechanism maintaining the co‐existence of three morphs (light, intermediate and dark). We took advantage of 20 years of life‐history data collected in a Dutch population to replicate earlier studies on the relationship between colour morph and fitness in this species. We examined differences between morphs in adult apparent survival, breeding success, annual number of fledglings produced and cumulative reproductive success. We found that cumulative reproductive success differed among morphs, with the intermediate morph having highest fitness. We also found assortative mating for colour morph, whereby assortative pairs were more likely to produce offspring and had longer‐lasting pair bonds than disassortative pairs. Over the 20‐year study period, the proportion of individuals with an intermediate morph increased. This apparent evolutionary change did not just arise from selection on individual phenotypes, but also from fitness benefits of assortative mating. The increased frequency of intermediates might also be due to immigration or drift. We hypothesize that genetic variation is maintained through spatial variation in selection pressures. Further studies should investigate morph‐dependent dispersal behaviour and habitat choice.     

Effects of reproductive condition and dominance rank on cortisol responsiveness to stress in free‐ranging female rhesus macaques

The hypothalamic–pituitary–adrenal (HPA) axis modulates individuals' physiological responses to social stress, which is an inevitable aspect of the daily lives of group‐living animals. Previous nonhuman primate studies have reported that sex, age, rank, and reproductive condition influence cortisol levels under stressful conditions. In this study we investigated cortisol responses to stress among 70 multiparous, free‐ranging female rhesus macaques (Macaca mulatta) on the island of Cayo Santiago, PR. Plasma cortisol samples were collected in two consecutive years under similar conditions. Twenty‐two females were sampled both years, and most of those females were lactating in only one of the years. Individual differences in cortisol levels were stable across years, even though reproductive condition changed for most individuals. No relationship was found between age or social rank and cortisol levels. Of the females that changed reproductive conditions, cortisol levels were higher when they were lactating than when they were cycling, and the amount of change in cortisol from cycling to lactating was greatest for low‐ranking individuals. Heightened reactivity to stress during lactation may be the result of concerns about infant safety, and such concerns may be higher among low‐ranking mothers than among higher ranking mothers. Psychosocial stress and hyperactivation of the HPA axis during lactation can suppress immune function and increase vulnerability to infectious diseases, thus explaining why adult females in the free‐ranging rhesus macaque population on Cayo Santiago have a higher probability of mortality during the birth season than during the mating season. Am. J. Primatol. 72:559–565, 2010. © 2009 Wiley‐Liss, Inc.     

EFFECTS OF SOCIAL AND EXTRA‐PAIR MATING ON SEXUAL SELECTION IN BLUE TITS (CYANISTES CAERULEUS)

The contribution of extra‐pair paternity (EPP) to sexual selection has received considerable attention, particularly in socially monogamous species. However, the importance of EPP remains difficult to assess quantitatively, especially when many extra‐pair young have unknown sires. Here, we combine measurements of the opportunity for selection (I), the opportunity for sexual selection (I_S), and the strength of selection on mating success (Bateman gradient, β_SS) with a novel simulation of random mating tailored to the specific mating system of the blue tit (Cyanistes caeruleus). In a population where social polygyny and EPP are common, the opportunity for sexual selection was significantly stronger and Bateman gradients significantly steeper for resident males than for females. In general, success with the social mate(s) contributed most to variation in male reproductive success. Effects of EPP were small, but significantly higher than expected under random mating. We used sibship analysis to estimate the number of unknown sires in our population. Under the assumption that the unknown sires are nonbreeding males, EPP reduced the variance in and the strength of selection on mating success, a possibility that hitherto has not been considered.     

Co‐variation between the intensity of behavioural manipulation and parasite development time in an acanthocephalan–amphipod system

Pomphorhynchus laevis, a fish acanthocephalan parasite, manipulates the behaviour of its gammarid intermediate host to increase its trophic transmission to the definitive host. However, the intensity of behavioural manipulation is variable between individual gammarids and between parasite populations. To elucidate causes of this variability, we compared the level of phototaxis alteration induced by different parasite sibships from one population, using experimental infections of Gammarus pulex by P. laevis. We used a naive gammarid population, and we carried out our experiments in two steps, during spring and winter. Moreover, we also investigated co‐variation between phototaxis (at different stages of infection, ‘young’ and ‘old cystacanth stage’) and two other fitness‐related traits, infectivity and development time. Three main parameters could explain the parasite intra‐population variation in behavioural manipulation. The genetic variation, suggested by the differences between parasite families, was lower than the variation owing to an (unidentified) environmental factor. Moreover, a correlation was found between development rate and the intensity of behavioural change, the fastest growing parasites being unable to induce rapid phototaxis reversal. This suggests that parasites cannot optimize at the same time these two important parameters of their fitness, and this could explain a part of the variation observed in the wild.     

Local diversity reduces infection risk across multiple freshwater host‐parasite associations

相似文献   

Landscape heterogeneity drives intra‐population niche variation and reproduction in an arctic top predator

While intra‐population variability in resource use is ubiquitous, little is known of how this measure of niche diversity varies in space and its role in population dynamics. Here we examined how heterogeneous breeding environments can structure intra‐population niche variation in both resource use and reproductive output. We investigated intra‐population niche variation in the Arctic tundra ecosystem, studying peregrine falcon (Falco peregrinus tundrius, White) breeding within a terrestrial‐marine gradient near Rankin Inlet, Nunavut, Canada. Using stable isotope analysis, we found that intra‐population niches varied at the individual level; we examined within‐nest and among‐nest variation, though only the latter varied along the terrestrial‐marine gradient (i.e., increased among‐nest variability among birds nesting within the marine environment, indicating higher degree of specialization). Terrestrial prey species (small herbivores and insectivores) were consumed by virtually all falcons. Falcons nesting within the marine environment made use of marine prey (sea birds), but depended heavily on terrestrial prey (up to 90% of the diet). Using 28‐years of peregrine falcon nesting data, we found a positive relationship between the proportion of terrestrial habitat surrounding nest sites and annual nestling production, but no relationship with the likelihood of successfully rearing at least one nestling reaching 25 days old. Annually, successful inland breeders raised 0.47 more young on average compared to offshore breeders, which yields potential fitness consequences for this long‐living species. The analyses of niche and reproductive success suggest a potential breeding cost for accessing distant terrestrial prey, perhaps due to additional traveling costs, for those individuals with marine nest site locations. Our study indicates how landscape heterogeneity can generate proximate (niche variation) and ultimate (reproduction) consequences on a population of generalist predator. We also show that within‐individual and among‐individual variation are not mutually exclusive, but can simultaneously arise and structure intra‐population niche variation.     

A longitudinal study of age‐related changes in Haemoproteus infection in a passerine bird

Blood parasites such as malaria and related haemosporidians commonly infect vertebrate species including birds. Understanding age‐specific patterns of parasite infections is crucial for quantifying the fitness consequences of parasitism for hosts and for understanding parasite transmission dynamics. We analyzed longitudinal and cross‐sectional infection data in house martins Delichon urbica, a migratory bird suffering from intense haemosporidian infection. We separated within‐ from among‐individual effects of age on prevalence. Our results showed that the probability of blood parasite infection increased as individual house martins aged. We also showed that the prevalence of infection decreased with age at last reproduction when controlling for age, showing a selective disappearance of infected birds from the population (i.e. selection). The estimated effect of age on prevalence was underestimated two‐ to three‐fold if not accounting for such selection. This study highlights the importance of taking among‐individual heterogeneity in the capacity to fight a disease into account because such heterogeneity can mask age‐related patterns of infection. These findings emphasize the relevance of considering within‐ and among‐individual patterns of infection in order to understand parasite‐induced mortality and the potential for parasite transmission.     

Correlation between Male Social Status,Testosterone Levels,and Parasitism in a Dimorphic Polygynous Mammal

Life history trade-offs have often been assumed to be the consequence of restrictions in the availability of critical resources such as energy and nutrients, which necessitate the differential allocation of resources to costly traits. Here, we examined endocrine (testosterone) and health (parasite burdens) parameters in territorial and non-territorial New Zealand fur seal males. We documented intra-sexual differences in sexual behaviours, testosterone levels, and parasitism that suggest a trade-off exists between reproductive success and physical health, particularly susceptibility to helminths and acanthocephalans, in males displaying different mating tactics (i.e., territorial and non-territorial tactics). Levels of testosterone were higher in territorial males and correlated positively with reproductive effort (i.e., intra- and inter-sexual interactions). However, these territorial males also exhibited high levels of parasitic infection, which may impair survival in the long-term. Our study, while limited in sample size, provides preliminary evidence for a link between male mating tactics, testosterone levels and parasite loads, and potential effects on reproductive success and life history that should be explored further.     

Effects of avian malaria on male behaviour and female visitation in lekking blue‐crowned manakins

Avian malaria, the infection by blood parasites of the genus Plasmodium, can reduce host fitness not only through mortality, but also by impairing the expression of sexual selection traits. Although different studies highlight the association of parasitism with a decrease in host reproductive success, few studies have addressed the role of parasites in honest signalling by lekking species. Hence, it is still uncertain which fitness components are affected by parasites in these species. We investigated whether avian malaria is associated with a decrease in mating behaviour of male blue‐crowned manakins Lepidothrix coronata and whether it affects female visitation in leks of a population in the central Amazon. Through behavioural observations, we estimated the rates of total male activity and social interaction, as well as the frequency of female visits at individual perches. We then examined if individuals were infected with Plasmodium spp. using molecular techniques. Avian malaria was associated with a decrease in male mating behaviour in each lek, and mating behaviour correlated with female visitation. Although rates of social interaction were not correlated with avian malaria among males, we observed that interacting with several individuals within a lek may be advantageous for males, as they also vocalized and displayed more, thus increasing their chances of being visited by females. Although female visitation was not associated with avian malaria in individuals or leks, it is still possible that female visitation is indirectly affected by avian malaria through the latter's effects on male activity. We suggest a role for male activity as an honest sexual signal for females. Thus, male display rate could be used by females as cue for the probability of a male being infected.