Variation among genotypes in responses to increasing temperature in a marine parasite: evolutionary potential in the face of global warming?

Climates are changing worldwide, and populations are under selection to adapt to these changes. Changing temperature, in particular, can directly impact ectotherms and their parasites, with potential consequences for whole ecosystems. The potential of parasite populations to adapt to climate change largely depends on the amount of genetic variation they possess in their responses to environmental fluctuations. This study is, to our knowledge, the first to look at differences among parasite genotypes in response to temperature, with the goal of quantifying the extent of variation among conspecifics in their responses to increasing temperature. Snails infected with single genotypes of the trematode Maritrema novaezealandensis were sequentially acclimatised to two different temperatures, ‘current’ (15 °C) and ‘elevated’ (20 °C), over long periods. These temperatures are based on current average field conditions in the natural habitat and those predicted to occur during the next few decades. The output and activity of cercariae (free-swimming infective stages emerging from snails) were assessed for each genotype at each temperature. The results indicate that, on average, both cercarial output and activity are higher at the elevated acclimation temperature. More importantly, the output and activity of cercariae are strongly influenced by a genotype-by-temperature interaction, such that different genotypes show different responses to increasing temperature. Both the magnitude and direction (increase or decrease) of responses to temperature varied widely among genotypes. Therefore, there is much potential for natural selection to act on this variation, and predicting how the trematode M. novaezealandensis will respond to the climate changes predicted for the next century will prove challenging.     

Ambient fauna impairs parasite transmission in a marine parasite-host system

To understand possible factors controlling transmission of trematode larvae between first and second intermediate hosts we examined the impact of ambient fauna on parasite transmission in a marine intertidal parasite-host association. Cockle hosts (Cerastoderma edule) kept together with selected co-occurring macrozoobenthic species in mesocosms acquired a lower parasite load compared to cockles kept alone, when targeted by cercariae of the trematode Himasthla elongata. The reduction of parasite load in the cockles differed between the 7 macrozoobenthic species tested and was between 35 and 91%. Three different types of reduction could be distinguished: (1) predators (Carcinus maenas, Crangon crangon) actively preying upon cercariae, (2) non-host filter feeders (Crepidula fornicata, Mya arenaria, Crassostrea gigas) filtering cercariae but not becoming infected and (3) alternative hosts (Mytilus edulis, Macoma balthica) becoming infected by the cercariae and thus distracting cercariae from the target hosts. In addition, interference competition may occur in the form of disturbance of cockles by ambient organisms resulting in lower filtration rates and subsequently lower parasite loads. Our results suggest that the species composition and relative abundance of the ambient fauna of parasite-host systems play an important role in controlling trematode transmission rates in benthic marine systems.     

Larval helminths in intermediate hosts: does competition early in life determine the fitness of adult parasites?

Density-dependent effects on parasite fitness have been documented from adult helminths in their definitive hosts. There have, however, been no studies on the cost of sharing an intermediate host with other parasites in terms of reduced adult parasite fecundity. Even if larval parasites suffer a reduction in size, caused by crowding, virtually nothing is known about longer-lasting effects after transmission to the definitive host. This study is the first to use in vitro cultivation with feeding of adult trematodes to investigate how numbers of parasites in the intermediate host affect the size and fecundity of adult parasites. For this purpose, we examined two different infracommunities of parasites in crustacean hosts. Firstly, we used experimental infections of Maritrema novaezealandensis in the amphipod, Paracalliope novizealandiae, to investigate potential density-dependent effects in single-species infections. Secondly, we used the crab, Macrophthalmus hirtipes (Ocypodidae), naturally infected by the trematodes, M. novaezealandensis and Levinseniella sp., the acanthocephalan, Profilicollis spp., and an acuariid nematode. These four helminths all develop and grow in their crustacean host before transmission to their bird definitive host by predation. In experimental infections, we found an intensity-dependent establishment success, with a decrease in the success rate of cercariae developing into infective metacercariae with an increasing dose of cercariae applied to each amphipod. In natural infections, we found that M. novaezealandensis-metacercariae achieved a smaller volume, on average, when infrapopulations of this parasite were large. Small metacercariae produced small in vitro-adult worms, which in turn produced fewer eggs. Crowding effects in the intermediate host thus were expressed at the adult stage in spite of the worms being cultured in a nutrient-rich medium. Furthermore, excystment success and egg-production in M. novaezealandensis in naturally infected crabs were influenced by the number of co-occurring Profilicollis cystacanths, indicating interspecific interactions between the two species. Our results thus indicate that the infracommunity of larval helminths in their intermediate host is interactive and that any density-dependent effect in the intermediate host may have lasting effects on individual parasite fitness.     

Effects of intermediate host genetic background on parasite transmission dynamics: a case study using Schistosoma mansoni

For parasites that require multiple hosts to complete their development, genetic interplay with one host may impact parasite transmission and establishment in subsequent hosts. In this study, we used microsatellite loci to address whether the genetic background of snail intermediate hosts influences life-history traits and transmission patterns of dioecious trematode parasites in their definitive hosts. We performed experimental Schistosoma mansoni infections utilizing two allopatric populations of Biomphalaria glabrata snails and assessed intensities and sex ratios of adult parasites in mouse definitive hosts. Our results suggest that the genetic background of hosts at one point in a parasite’s life cycle can influence the intensities and sex ratios of worms in subsequent hosts.     

The use of fluorescent fatty acid analogs as labels in trematode experimental infections

We examined the utility of fluorescent fatty acid analog dyes for labeling larval trematodes to use in experimental infections. Our goals were to identify two dyes that label larval trematodes belonging to the species Maritrema novaezealandensis and Coitocaecum parvum, determine if the dyes influence survival and infectivity of larval trematodes and/or host mortality, and if larval trematodes labeled with alternative dyes could be distinguished post-infection. The two dyes tested, BODIPY FL C₁₂ and BODIPY 558/568 C₁₂, successfully labeled all treated larval trematodes, did not influence cercariae survival or infectivity, and did not influence host mortality in either host-parasite system. All larval parasites were fluorescent and distinguishable after 5 days in amphipod intermediate hosts. In addition, larval Acanthoparyphium sp. were strongly fluorescent with both dyes after 5 weeks within cockle hosts. This method should be extremely useful for experimental studies using trematode-host systems as models for addressing a range of ecological and evolutionary questions.     

滨鹬马蹄吸虫(复殖目:微茎科)的尾蚴和囊蚴期的季节动态

对科威特湾微茎科滨鹬马蹄吸虫幼虫期的中间宿主双带盾桑椹螺(Clypeomorus bifasciata)及小相手蟹(Nanosesarma minutum)的季节动态进行了研究。调查期超过一年,在检查的1 600只螺和415只蟹中, 11.8 %的螺感染了8种马蹄属线虫中的一种,且以滨鹬马蹄吸虫的感染占优势(9.9 %螺感染) ; 80 %的蟹感染滨鹬马蹄吸虫囊蚴。虽然一年四季两种宿主都会感染,但吸虫的流行和尾蚴(指成熟期感染)在夏季呈现高蜂。从螺体排出的尾蚴具有明显季节性,在此海湾必须要超过最低温度20℃。总的感染率在较大(较老)的螺里有所下降,显示吸虫影响宿主生存并随之影响宿主群体结构。囊蚴的感染丰度与蟹的个体大小有明显相关性;较大的蟹感染较多的囊蚴,显示宿主能耐受更多的吸虫。调查显示,囊蚴的感染率与蟹的大小或性别无相关性。囊蚴体外脱囊以及产卵吸虫的释放证明,成熟虫体终年存在于所有大小和性别不同的蟹里,显示从蟹到鸟的持续感染是可能的。总的来说,滨鹬马蹄吸虫在海湾的传播动态是由这两种无脊椎动物宿主来协调,并似乎是被一系列依赖于温度的活动控制,这些活动影响易感宿主种群及感染性幼虫期尾蚴和囊蚴的存在。     

A trematode infection with no effect on reproductive success of a sand-bubbler crab

The infection effects of the parasitic digenean trematode on the body weight and reproductive success of the sand-bubbler crab were examined. Gynaecotyla squatarolae (Trematoda: Microphallidae) infects the body cavity of Scopimera globosa (Decapoda: Scopimeridae) and uses the crab as its second intermediate host. The parasites infected all reproductive crabs examined to varying degrees. Larger crabs of both sexes had more parasites than smaller ones, probably because body size reflects age, and older crabs had a longer period of exposure to infection. Males had more parasites than females, probably because of sexual difference in acting time on the surface. Ovigerous females stay in closed burrows and do not act on the surface during incubation, and so have less chance of infection than males. The quantity of infecting parasites did not explain variations in either body weight or reproductive success of individual crabs in a field experiment. The life history of this parasite, relative body size of the crabs, and cost and the possible benefit of manipulation for the parasite may explain these results.     

Higher parasite richness, abundance and impact in native versus introduced cichlid fishes

Empirical studies suggest that most exotic species have fewer parasite species in their introduced range relative to their native range. However, it is less clear how, ecologically, the loss of parasite species translates into a measurable advantage for invaders relative to native species in the new community. We compared parasitism at three levels (species richness, abundance and impact) for a pair of native and introduced cichlid fishes which compete for resources in the Panama Canal watershed. The introduced Nile tilapia, Oreochromis niloticus, was infected by a single parasite species from its native range, but shared eight native parasite species with the native Vieja maculicauda. Despite acquiring new parasites in its introduced range, O. niloticus had both lower parasite species richness and lower parasite abundance compared with its native competitor. There was also a significant negative association between parasite load (abundance per individual fish) and host condition for the native fish, but no such association for the invader. The effects of parasites on the native fish varied across sites and types of parasites, suggesting that release from parasites may benefit the invader, but that the magnitude of release may depend upon interactions between the host, parasites and the environment.     

Female biased sex-ratio in Schistosoma mansoni after exposure to an allopatric intermediate host strain of Biomphalaria glabrata

For parasites that require multiple hosts to complete their development, the interaction with the intermediate host may have an impact on parasite transmission and development in the definitive host. The human parasite Schistosoma mansoni needs two different hosts to complete its life cycle: the freshwater snail Biomphalaria glabrata (in South America) as intermediate host and a human or rodents as final host. To investigate the influence of the host environment on life history traits in the absence of selection, we performed experimental infections of two B. glabrata strains of different geographic origin with the same clonal population of S. mansoni. One B. glabrata strain is the sympatric host and the other one the allopatric host. We measured prevalence in the snail, the cercarial infectivity, sex-ratio, immunopathology in the final host and microsatellite frequencies of individual larvae in three successive generations.     

In vitro culture of marine trematodes from their snail first intermediate host

The ability to culture parasites outside their host (i.e. in vitro) is essential for several aspects of parasitological research. Here, a culture medium for marine trematode parthenitae was optimized using Philophthalmus sp. rediae from the intermediate snail host, Zeacumantus subcarinatus. The medium was optimized by sequentially testing the suitability of different levels of osmolality, different commercially available media, and different concentrations of supplemented chicken serum, while controlling for genetic variation among cultures. Philophthalmus sp. rediae survived up to 56 days in cultures of the best tested medium, remaining active and continuously shedding cercariae. The broader suitability of the culture medium was tested using five other trematode species from different families (using either the same or other marine snails as first intermediate hosts): Galactosomum sp., Acanthoparyphium sp., Maritrema novaezealandensis, Curtuteria australis, and an undescribed species of the family Opecoelidae. Survivorship of rediae and sporocysts from these species ranged from eight days to 42 days. The culture procedures developed here can therefore be used in the future as a system under which to culture marine trematode parthenitae for experimental studies.     

A circular analysis of chronobiology of Schistosoma japonicum cercarial emergence from hilly areas of Anhui,China

About 46 mammal species have been suspected as reservoir hosts for Schistosoma japonicum and therefore the track of the target parasites, in relation to definitive host species, may be of great importance in terms of theoretical and practical implications. The circadian rhythm of cercariae emergence, a genetically controlled behavior for parasites to adapt to their definitive hosts, may seem to be a perfect biological marker for S. japonicum. In this study, a late (or nocturnal) cercarial emergence pattern was observed on the parasites from one hilly region in Anhui of China, where rodents serve as reservoirs, and on the first generation of the parasites. Moreover, by using the circular statistics, the homogeneity of parasites in such trait was also demonstrated. All these provide evidence for the genetically controlled biological trait, which seems essential in the investigation of macro- or micro-dynamics of parasite transmission of interest. This is particularly true in the case of S. japonicum when multiple parasite isolates or strains are more likely to exist.     

Effect of sexual segregation on host-parasite interaction: Model simulation for abomasal parasite dynamics in alpine ibex (Capraibex)

We investigated whether sexual segregation might affect parasite transmission and host dynamics, hypothesising that if males are the more heavily infected sex and more responsible for the transmission of parasite infections, female avoidance of males and the space they occupy could reduce infection rates. A mathematical model, simulating the interaction between abomasal parasites and a hypothetical alpine ibex (Capraibex) host population composed of its two sexes, was developed to predict the effect of different degrees of sexual segregation on parasite intensity and on host abundance. The results showed that when females tended to be segregated from males, and males were distributed randomly across space, the impact of parasites was the lowest, resulting in the highest host abundance, with each sex having the lowest parasite intensity. The predicted condition that minimises the impact of parasites in our model was the one closest to that observed in nature where females actively seek out the more segregated sites while males are less selective in their ranging behaviour. The overlapping of field observation with the predicted optimal strategy lends support to our idea that there might be a connection between parasite transmission and sexual segregation. Our simulations provide the biological boundaries of host-parasite interaction needed to determine a parasite-mediated effect on sexual segregation and a formalised null hypothesis against which to test future field experiments.     

Invaders of an invader - Trematodes in Potamopyrgus antipodarum in Poland

The subject of the following study was the natural and experimental invasion of trematode larvae in Potamopyrgus antipodarum from Bory Tucholskie National Park (Poland). Only one out of the 14,908 dissected specimens had oval sporocysts and mature cercariae of fish fluke, which belongs to the Sanguinicolidae family. It is the first recorded case in the European population of P. antipodarum living in inland water. The experimental study showed the possibility of native metacercariae (Echinostoma revolutum, Echinoparyphium aconiatum and Hypoderaeum conoideum) settlement in those immigrant snail species; however, exposure to parasites resulted in an increase in snail mortality. The three out of six used cercariae species were able to transform into metacercariae in P. antipodarum as in the second intermediate host, but the exposure to parasitic larvae of four of the used species resulted in an increase in snails’ mortality. It may suggest that not only metacercariae settlement but also the attack of cercariae (Rubenstrema opisthovitellinum at a temperature of 22 °C) affected the low survival of experimental snails in comparison to control animals. The subject of discussion presented in this paper is also the hypothesis on probable effect of the interaction between P. antipodarum and native snail species (as a source of invasive larvae of parasites) living in the same habitat.     

An example of molecular co-evolution: reactive oxygen species (ROS) and ROS scavenger levels in Schistosoma mansoni/Biomphalaria glabrata interactions

The co-evolution between hosts and parasites involves huge reciprocal selective pressures on both protagonists. However, relatively few reports have evaluated the impact of these reciprocal pressures on the molecular determinants at the core of the relevant interaction, such as the factors influencing parasitic virulence and host resistance. Here, we address this question in a host-parasite model that allows co-evolution to be monitored in the field: the interaction between the mollusc, Biomphalaria glabrata, and its trematode parasite, Schistosoma mansoni. Reactive oxygen species (ROS) produced by the haemocytes of B. glabrata are known to play a crucial role in killing S. mansoni. Therefore, the parasite must defend itself against oxidative damage caused by ROS using ROS scavengers in order to survive. In this context, ROS and ROS scavengers are involved in a co-evolutionary arms race, and their respective production levels by sympatric host and parasite could be expected to be closely related. Here, we test this hypothesis by comparing host oxidant and parasite antioxidant capabilities between two S. mansoni/B. glabrata populations that have co-evolved independently. As expected, our findings show a clear link between the oxidant and antioxidant levels, presumably resulting from sympatric co-evolution. We believe this work provides the first supporting evidence of the Red Queen Hypothesis of reciprocal evolution for functional traits at the field-level in a model involving a host and a eukaryotic parasite.     

Infection by Paragonimus miyazakii cercariae of their crab hosts, Geothelphusa dehaani, by percutaneous penetration

Identification of the transmission routes of the trematode parasite Paragonimus miyazakii into different intermediate hosts would help to explain the natural distribution of the parasite. The behavior of P. miyazakii cercariae released from snails into water and in the presence of a living host or a whole crab leg was observed by stereoscopic or light microscopy at various times after exposure started. On encountering a crab leg or cheliped, the cercariae became entangled with the host via mucoid strands arising from the cercariae. Within 3 hr, most cercariae were attached to the host; cuticular penetration took between 5 and 6 hr, after which cercariae were found in the cavity of the leg. Crabs examined 102-149 days after exposure to the cercariae contained fully developed metacercariae. The metacercariae were fed to 2 rats, and the rats were killed 83 or 111 days later. Some of the metacercariae had reached maturity in the rats. That the cercariae were not ingested by the crabs but penetrated the crabs percutaneously (through hard as well as soft tissue) means that transmission can occur even in areas in which crabs and the host snails do not coexist, as they would if the usual route were oral (when the crabs ate infected snails).     

Interspecific antagonism and virulence in hosts exposed to two parasite species

Co-infection of host organisms by multiple parasite species has evolutionary consequences for all participants in the symbiosis. In this study, we co-exposed aquatic-snails (Biomphalaria glabrata) to two of their trematode parasites, Schistosoma mansoni and Echinostoma caproni. In co-exposed snails, E. caproni prevalence was 63% compared to only 23% for S. mansoni. Co-exposed E. caproni-infected snails exhibited reduced fecundity, higher mortality, and higher parasite reproduction (higher virulence) compared to hosts exposed to echinostomes alone. Conversely, co-exposed S. mansoni-infected snails released fewer parasites and produced greater numbers of eggs compared to hosts exposed to S. mansoni alone. These results suggest that co-exposure not only influences the establishment (presence or absence) of particular parasite species, but also impacts host life history, parasite reproduction, and the virulence of the interaction.     

Male hosts are responsible for the transmission of a trophically transmitted parasite, Pterygodermatites peromysci, to the intermediate host in the absence of sex-biased infection

Field studies have identified that male-biased infection can lead to increased rates of transmission, so we examined the relative importance of host sex on the transmission of a trophically transmitted parasite (Pterygodermatites peromysci) where there is no sex-biased infection. We experimentally reduced infection levels in either male or female white-footed mice (Peromyscus leucopus) on independent trapping grids with an anthelmintic and recorded subsequent infection levels in the intermediate host, the camel cricket (Ceuthophilus pallidipes). We found that anthelmintic treatment significantly reduced the prevalence of infection among crickets in both treatment groups compared with the control, and at a rate proportional to the number of mice de-wormed, indicating prevalence was not affected by the sex of the shedding definitive host. In contrast, parasite abundance in crickets was higher on the grids where females were treated compared with the grids where males were treated. These findings indicate that male hosts contribute disproportionately more infective stages to the environment and may therefore be responsible for the majority of parasite transmission even when there is no discernable sex-biased infection. We also investigated whether variation in nematode length between male and female hosts could account for this male-biased infectivity, but found no evidence to support that hypothesis.     

Endemic infection reduces transmission potential of an epidemic parasite during co-infection

Endemic, low-virulence parasitic infections are common in nature. Such infections may deplete host resources, which in turn could affect the reproduction of other parasites during co-infection. We aimed to determine whether the reproduction, and therefore transmission potential, of an epidemic parasite was limited by energy costs imposed on the host by an endemic infection. Total lipids, triacylglycerols (TAG) and polar lipids were measured in cockroaches (Blattella germanica) that were fed ad libitum, starved or infected with an endemic parasite, Gregarina blattarum. Reproductive output of an epidemic parasite, Steinernema carpocapsae, was then assessed by counting the number of infective stages emerging from these three host groups. We found both starvation and gregarine infection reduced cockroach lipids, mainly through depletion of TAG. Further, both starvation and G. blattarum infection resulted in reduced emergence of nematode transmission stages. This is, to our knowledge, the first study to demonstrate directly that host resource depletion caused by endemic infection could affect epidemic disease transmission. In view of the ubiquity of endemic infections in nature, future studies of epidemic transmission should take greater account of endemic co-infections.     

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.