Invaded Invaders: Infection of Invasive Brown Treesnakes on Guam by an Exotic Larval Cestode with a Life Cycle Comprised of Non-Native Hosts

Background

Multiple host introductions to the same non-native environment have the potential to complete life cycles of parasites incidentally transported with them. Our goal was to identify a recently detected parasitic flatworm in the invasive Brown Treesnake (Boiga irregularis) on the remote Pacific island of Guam. We considered possible factors influencing parasite transmission, and tested for correlations between infection status and potential indicators of host fitness. We used genetic data from the parasite and information about the native ranges of other possible non-native hosts to hypothesize how it arrived on Guam and how its life cycle may be currently supported.

Methods

We identified the parasite by comparing larval morphology and mtDNA sequences with other Pseudophyllid tapeworms. We assessed probability of infection in individual snakes using logistic regression and examined different factors influencing presence of parasites in hosts.

Results

We identified the parasite as the pseudophyllid cestode Spirometra erinaceieuropaei, with all sampled worms from multiple snakes sharing a single mtDNA haplotype. Infection appears to be limited to the only freshwater watershed on the island, where infection prevalence was high (77.5%). Larger snakes had a higher probability of being infected, consistent with the chronic nature of such infections. While infection status was positively correlated with body condition, infected snakes tended to have lower intra-peritoneal fat body mass, potentially indicating a negative effect on energy stores.

Conclusions

We discovered that B. irregularis inhabiting a small area of forested habitat in a freshwater watershed on Guam are often infected by a novel parasite of Asian origin. While further work is needed, this species of Spirometra, itself a non-native species, likely depends on a suite of recently introduced hosts from different parts of the world to complete the life cycle. This baseline study provides little evidence of any effects on host fitness, but additional data are needed to more thoroughly explore the consequences of infection in this invasive snake population.     

Old pythons stay fit; effects of haematozoan infections on life history traits of a large tropical predator

We document the impact of blood parasite infections caused by Hepatozoon sp. on water python (Liasis fuscus) life history traits such as growth rates, condition, reproductive output and survival. Individual snakes maintained similar among-year parasite loads. Hepatozoon infections affected python growth rate, i.e. snakes suffering from high infection levels exhibited significantly slower growth compared to individuals with low parasite loads. Our results suggest that the parasites also affected the pythons nutritional status (condition), as snakes with low condition scores suffered from higher parasite infection levels than snakes with high scores. Furthermore, our data suggest that parasitaemia may affect female reproductive output, as reproductive female pythons harboured lower parasite loads compared to non-reproductive adult females. High levels of parasite infections also affected juvenile python survival, as recaptured snakes harboured significantly lower parasite loads compared to non-recaptured yearling pythons. In our study area, water python have very few natural predators and, hence, experience low mortality rates and commonly reach an age of >15 years. In contrast to results obtained in other studies, parasite loads in larger/older pythons were lower compared to younger snakes, suggesting that only snakes harbouring lower levels of parasitaemia were able to survive to old age. We suggest that a possible cause for the opposing results regarding parasite prevalence and host age may be due to different levels of extrinsic mortality rates and longevity. Long-lived organisms, such as water pythons, may invest relatively more into crucial self-maintenance functions such as parasite defence, compared to short-lived organisms.     

Bioluminescence imaging of chronic Trypanosoma cruzi infections reveals tissue‐specific parasite dynamics and heart disease in the absence of locally persistent infection

Chronic Trypanosoma cruzi infections lead to cardiomyopathy in 20–30% of cases. A causal link between cardiac infection and pathology has been difficult to establish because of a lack of robust methods to detect scarce, focally distributed parasites within tissues. We developed a highly sensitive bioluminescence imaging system based on T. cruzi expressing a novel luciferase that emits tissue‐penetrating orange‐red light. This enabled long‐term serial evaluation of parasite burdens in individual mice with an in vivo limit of detection of significantly less than 1000 parasites. Parasite distributions during chronic infections were highly focal and spatiotemporally dynamic, but did not localize to the heart. End‐point ex vivo bioluminescence imaging allowed tissue‐specific quantification of parasite loads with minimal sampling bias. During chronic infections, the gastro‐intestinal tract, specifically the colon and stomach, was the only site where T. cruzi infection was consistently observed. Quantitative PCR‐inferred parasite loads correlated with ex vivo bioluminescence and confirmed the gut as the parasite reservoir. Chronically infected mice developed myocarditis and cardiac fibrosis, despite the absence of locally persistent parasites. These data identify the gut as a permissive niche for long‐term T. cruzi infection and show that canonical features of Chagas disease can occur without continual myocardium‐specific infection.     

Experimental Validation of Sex Differences in Spatial Behavior Patterns of Free‐Ranging Snakes: Implications for Social Interactions

Social interactions often play a significant role in determining patterns of spatial use. Although snakes are generally thought of as asocial, recent spatial dispersion studies suggest that the spatial ecology of snakes may be more strongly influenced by social interactions than previously thought. We investigated the spatial behavior patterns of a western cottonmouth (Agkistrodon piscivorus) population in east Texas by uniquely combining radio‐telemetry studies on free‐ranging snakes with experimental arena trials with captive individuals from the same population. Observations from the radio‐telemetry study on free‐ranging A. piscivorus indicated that females were more gregarious than males. In the follow‐up study, spatial dispersion data from captive snakes maintained in experimental field arenas yielded similar results to spatial behavior patterns of free‐ranging individuals. When compared to random experimental controls, these data suggest that observed spatial behavior patterns are related to mechanisms associated with both active avoidance among males and conspecific attraction among females. In addition to uniquely combining both free‐ranging and captive observations, this is the first snake study to demonstrate sex differences with both of these divergent (attraction and avoidance) spatial patterns within a single population. Thus, similar to other vertebrate groups, a growing body of literature suggests that social interactions in snakes should be strongly considered in interpretations of spatial ecology and behavior.     

Co‐infections by malaria parasites decrease feather growth but not feather quality in house martin

During moult, stressors such as malaria and related haemosporidian parasites (e.g. Plasmodium and Haemoproteus) could affect the growth rate and quality of feathers, which in turn may compromise future reproduction and survival. Recent advances in molecular methods to study parasites have revealed that co‐infections with multiple parasites are frequent in bird–malaria parasite systems. However, there is no study of the consequences of co‐infections on the moult of birds. In house martins Delichon urbica captured and studied at a breeding site in Europe during 11 yr, we measured the quality and the growth rate of tail feathers moulted in the African winter quarters in parallel with the infection status of blood parasites that are also transmitted on the wintering ground. Here we tested if the infection with two haemosporidian parasite lineages has more negative effects than a single lineage infection. We found that birds with haemosporidian infection had lower body condition. We also found that birds co‐infected with two haemosporidian lineages had the lowest inferred growth rate of their tail feathers as compared with uninfected and single infected individuals, but co‐infections had no effect on feather quality. In addition, feather quality was negatively correlated with feather growth rate, suggesting that these two traits are traded‐off against each other. We encourage the study of haemosporidian parasite infection as potential mechanism driving this trade‐off in wild populations of birds.     

Ticks on snakes: The ecological correlates of ectoparasite infection in free‐ranging snakes in tropical Australia

Parasites profoundly influence the lives of their hosts, yet the dynamics of host–parasite interactions are poorly understood – especially in reptiles. We examined the ecological correlates of parasitism by ixodid ticks in an assemblage of 10 snake species in tropical Australia. In total, we recorded 3803 ticks on 1841 individual snakes of six species (no ticks were found on the other species). Molecular analyses confirmed the tropical reptile tick (Amblyomma fimbriatum: Ixodidae) to be the most common snake tick at our study site, with inter‐ and intraspecific variation in tick prevalence and intensity. Tick attachment sites were random on most snake species, but both male and female ticks congregated on the heads of the colubrid snake Boiga irregularis and the python Simalia amethistina. In these same species, tick loads were higher on snakes captured in woodland than in rainforest. Females of two python species (Aspidites melanocephalus and S. amethistina) had higher tick loads than did males. In B. irregularis, individuals captured in the dry season had higher tick loads than those captured in the wet season. In most parasitized snake species, larger individuals had greater tick loads. Data from snake recaptures confirmed individual tick burdens frequently varied, with little correlation between tick loads on the same snake at successive captures (except for B. irregularis). Finally, tick intensity was not correlated with (and thus, presumably did not influence) the body condition of any snake species in our study. Use of specific types of refuge sites may strongly influence tick loads on snakes in this system.     

Rhesus Macaques (Macaca mulatta) Use Posture to Assess Level of Threat From Snakes

Once prey animals have detected predators, they must make decisions about how to respond based on a cost‐benefit analysis of their risk level. The threat sensitivity hypothesis predicts that prey animals match their response to the level of risk, with high‐risk predator encounters eliciting stronger evasive responses than low‐risk encounters. Primates are known prey of snakes, yet they vary their responses toward snakes. We predicted that primates match their response to the threat level from snakes by assessing posture, with striking postures indicating greater risk than coiled postures and coiled postures indicating greater risk than extended sinusoidal postures. We tested this prediction in a series of experimental trials in which captive rhesus macaques (Macaca mulatta) were exposed to snake models in those postures. Results supported the predictions: macaques responded more strongly to a snake model in a striking posture than in a coiled posture and more to a snake model in a coiled posture than to an extended sinusoidal snake model. We also examined responses of macaques to a partially exposed snake model to mimic the condition of incomplete information, as snakes are often occluded by vegetation. The occluded snake model evoked a response comparable to that of the striking snake. These findings support the threat sensitivity hypothesis. Rhesus macaques use the posture of snakes as a cue in threat assessment, responding more intensely as threat increases, and they also behave as if risk is elevated when their information about snakes is incomplete.     

High parasite infection level in non‐native invasive species: it is just a matter of time

The enemy release hypothesis is often used to explain the success of non‐native species invasions. Growing evidence indicates that parasite or pathogen species richness increases over time in invasive non‐native species; however, this increase should not directly translate into release from enemy pressure as infection intensity of parasites (number of parasites per host) has a more profound impact on host fitness. The changes in intensity of parasitic infections in invasive non‐native species have not yet been thoroughly analysed in newly colonized areas. The goal of this study was to determine whether gastrointestinal parasite (nematode and trematode) infection intensity has increased with time since the populations of American mink Neovison vison were established and how host demographic parameters affect infection intensity. We tested the enemy release hypothesis by substituting space for time, evaluating parasite abundance in American mink at six sites along a chronosequence of mink invasion history. Nematode and trematode abundance increased with time since mink introduction, from a few parasites on average per mink after 16 yr, to 200–250 parasites per mink after 34 yr. The rate of increase in parasite abundance varied among demographic groups of mink (sex and age). Both nematodes and trematodes were more abundant in males than in females, and in subadults than in adults. Higher nematode abundance negatively affected body condition of mink. Our results provide evidence that non‐native species are released from enemy pressure only in the first phase of invasion, and that infection is modulated by host demographics and season. These results contribute to the evaluation of the long‐term patterns of parasite accumulation in invasive non‐native species after their colonization of new territories.     

Predilection Muscles and Physical Condition of Raccoon Dogs (Nyctereutes procyonoides) Experimentally Infected with Trichinella spiralis and Trichinella nativa

The predilection muscles of Trichinella spiralis and T. nativa were studied in 2 experimental groups of 6 raccoon dogs (Nyctereutes procyonoides), the third group serving as a control for clinical signs. The infection dose for both parasites was 1 larva/g body weight. After 12 weeks, the animals were euthanized and 13 sampling sites were analysed by the digestion method. Larvae were found in all sampled skeleton muscles of the infected animals, but not in the specimens from the heart or intestinal musculature. Both parasite species reproduced equally well in the raccoon dog. The median density of infection in positive tissues was 353 larvae per gram (lpg) with T. spiralis and 343 lpg with T. nativa. All the infected animals had the highest larvae numbers in the carpal flexors (M. flexor carpi ulnaris). Also tongue and eye muscles had high infection levels. There were no significant differences in the predilection sites between these 2 parasite species. Trichinellosis increased the relative amount of fat, but not the body weight in the captive raccoon dogs. Thus, Trichinella as a muscle parasite might have catabolic effect on these animals.     

Are gobiid fish more susceptible to predation if parasitized by Eustrongylides excisus? An answer from robbed snakes

Aspects of the predator–prey relationship between dice snake, Natrix tessellata and gobiid fish infected with Eustrongylides excisus were studied in Lake Sinoe, Romania. A population of snakes residing here shows a high prevalence of subcutaneous larvae of this nematode. The hypothesis of the altered motility in infected fish leading to increased depredation by snakes was tested by comparing gobiids collected from dice snakes with gobiids caught via electrofishing. Out of a total of seven identified gobiid species, three were used for analysis: syrman goby Neogobius syrman, mushroom goby Neogobius eurycephalus, and round goby Neogobius melanostomus. No significant differences in prevalence and intensity of E. excisus infection were found between fish caught by snakes and those obtained by electrofishing. However, significantly higher abundance of E. excisus larvae in fish caught by snakes was reported. These findings suggest limited influence of the presence of E. excisus larvae in studied gobiids regarding their susceptibility to predation by dice snakes.     

Impact of the invasive parasitic copepod Mytilicola orientalis on native blue mussels Mytilus edulis in the western European Wadden Sea

Invasive species can indirectly affect native species by modifying parasite–host dynamics and disease occurrence. This scenario applies to European coastal waters where the invasive Pacific oyster (Magallana gigas) co-introduced the parasitic copepod Mytilicola orientalis that spills over to native blue mussels (Mytilus edulis) and other native bivalves. In this study, we investigated the impact of M. orientalis infections on blue mussels by conducting laboratory experiments using controlled infections with larval stages of the parasitic copepod. As the impact of infections is likely to depend on the mussels’ food availability, we also tested whether potential adverse effects of infection on mussels intensify under low food conditions. Blue mussels that were experimentally infected with juvenile M. orientalis had a significantly lower body condition (11–13%) compared with uninfected mussels after nine weeks of infection. However, naturally infected mussels from a mixed mussel and oyster bed did not significantly differ in body condition compared with uninfected mussels. Contrary to effects on mussel condition, we did not find an effect of experimental infections on clearance rates, shell growth or survival of blue mussels and no clear sign of exacerbating effects of food limitation. Our study illustrates that invasive species can indirectly affect native species via parasite co-introductions and parasite spillover. The results of this study call for the integration of such parasite-mediated indirect effects of invasions in impact assessments of invasive species.     

Genetic analyses of Pseudomonas aeruginosa isolated from healthy captive snakes: evidence of high inter‐ and intrasite dissemination and occurrence of antibiotic resistance genes

Faecal carriage of Pseudomonas aeruginosa was investigated by selective plating and PCR identification test, among healthy captive snakes from zoological and private collections from France as well as from wild snakes from Guinea. P. aeruginosa faecal carriage among captive snakes was high (72 out of 83 individuals), but low among wild specimen (3 out of 23 individuals). Genetic diversity analyses of the isolates, based on SpeI‐PFGE profiles, evidenced five dominant clones or clonal complexes spreading among snakes within a site and between sites and persisting over time. Similar clones or clonal complexes were detected from mouth swabs of the owners and from water and preys used to feed the snakes, evidencing various sources of snake colonization and the first cases of P. aeruginosa cross‐contamination between snakes and owners. These observations led to the conclusion that P. aeruginosa behaves as an opportunistic species within snakes in captivity and that colonization and dissemination occurs consecutively to processes similar to those identified within the hospital. Antibiotic susceptibility testing showed that most isolates had a wild‐type resistance profile except for one persistent clone isolated from both snakes and preys that harboured multiple antimicrobial resistance genes mediated by an integron carrying the qacH, aadB, aadA2 and cmlA10 cassettes, and a tetA(C)‐carrying transposon. Biocides or antibiotics used in the zoological garden could have led to the acquisition of this integron.     

Intestinal Parasites of Free-ranging,Semicaptive,and Captive <Emphasis Type="Italic">Pongo abelii</Emphasis> in Sumatra,Indonesia

We collected fecal samples from 32 free-ranging, 19 semicaptive, and 54 captive Sumatran orangutans on Sumatra from 1998 until 2004 and screened them for gastrointestinal parasites. Our objectives were to compare the intestinal parasites of free-ranging, semicaptive, and captive orangutans and to evaluate the risk of parasite transmission in orangutan reintroduction programs. We identified 4 genera of Protozoa, 7 genera of nematodes, 1 trematode sp., and 1 cestode sp. The prevalence of Balantidium coli in free-ranging orangutans was significantly higher than in captive individuals. However, the prevalence of Strongyloides sp. was higher in captive than in free-ranging orangutans. Free-ranging female orangutans had a significantly higher total prevalence of intestinal parasites than that of males. We found no significant difference between parasite prevalences in different age groups. Compared to gorillas and chimpanzees, orangutans carry a smaller variety of protozoan and nematode species. Strongyloides sp. infections form the highest risk in reintroduction programs as crowding, ground-dwelling, and poor hygiene in captive and semicaptive orangutans may cause a constant reinfection.     

Duration of strike-induced chemosensory searching in long-term captive rattlesnakes at national zoo,audubon zoo,and San Diego Zoo

Rattlesnakes typically strike and release adult rodent prey. Striking is followed by a sustained, high rate of tongue flicking that guides the snake to the envenomated, dead prey. Wild-caught rattlesnakes exhibited this chemosensory searching for about 2.5 h, and the present study demonstrated that long-term captive rattlesnakes (Crotalus atrox, C durissus, C horridus, C vegrandis, C unicolor) at three zoos did the same. Because these zoo-raised snakes had always been offered dead rodents and because the snakes had become accustomed to ingesting them without striking, the present snakes had rarely exercised their innate predatory repertoires. The duration of chemosensory searching in these snakes indicates that this important aspect of the predatory repertoire had not been degraded as a consequence of long-term captive husbandry.     

Effects of host condition on susceptibility to infection, parasite developmental rate, and parasite transmission in a snail-trematode interaction

Whether or not organisms become infected by parasites is likely to be a complex interplay between host and parasite genotypes, as well as the physiological condition of both species. Details of this interplay are very important because physiology‐driven susceptibility has the potential to confound genetic coevolutionary responses. Here we concentrate on how physiological aspects of infection may interfere with genetic‐based infectivity in a snail–trematode (Potamopyrgus antipodarum/Microphallus sp.) interaction by asking: (1) how does host condition affect susceptibility to infection? and (2) how does host condition affect the survival of infected individuals? We manipulated host condition by experimentally varying resources. Contrary to our expectation, host condition did not affect susceptibility to infection, suggesting that genetics are more important than physiology in this regard. However, hosts in poor condition had higher parasite‐induced mortality than hosts in good condition. Taken together, these results suggest that coevolutionary interactions with parasites may depend on host condition, not by altering susceptibility, but rather by affecting the likelihood of parasite transmission.     

Fecundity compensation in the three‐spined stickleback Gasterosteus aculeatus infected by the diphyllobothriidean cestode Schistocephalus solidus

Causal explanations for host reproductive phenotypes influenced by parasitism fit into three broad evolutionary models: (1) non‐adaptive side effect; (2) adaptive parasitic manipulation; and (3) adaptive host defence. This study demonstrates fecundity compensation, an adaptive non‐immunological host defence, in the three‐spined stickleback fish (Gasterosteus aculeatus) infected by the diphyllobothriidean cestode Schistocephalus solidus. Both infected and uninfected female sticklebacks produced egg clutches at the same age and size. The reproductive capacity of infected females decreased rapidly with increased parasite : host body mass ratio. Body condition was lower in infected females than uninfected females and decreased with increasing parasite : host mass ratio. Females with clutches had greater body condition than those without clutches. A point biserial correlation showed that there was a body condition threshold necessary for clutch production to occur. Host females apparently had the capacity to produce egg clutches until the prolonged effects of nutrient theft by the parasite and the drain on resources from reproduction precluded clutch formation. Clutch mass, adjusted for female body mass, did not differ significantly between infected and uninfected females. Infected females apparently maintained the same level of reproductive allotment (egg mass as proportion of body mass) as uninfected females. Infected females produced larger clutches of smaller eggs than uninfected females, revealing a trade‐off between egg mass and egg number, consistent with the fecundity compensation hypothesis. The rapid loss of reproductive capacity with severity of infection probably reflects the influence of the parasite combined with a trade‐off between current and future reproduction in the host. Inter‐annual differences in reproductive performance may have reflected ecological influences on host pathology and/or intra‐annual seasonal changes. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Parental defence on the reef: antipredator tactics of coral‐reef fishes against egg‐eating seasnakes

On coral reefs in New Caledonia, the eggs of demersal‐spawning fishes are consumed by turtle‐headed seasnakes (Emydocephalus annulatus). Fish repel nest‐raiding snakes by a series of tactics. We recorded 232 cases (involving 22 fish species) of antipredator behaviour towards snakes on a reef near Noumea. Blennies and gobies focused their attacks on snakes entering their nests, whereas damselfish (Pomacentridae) attacked passing snakes, as well as nest‐raiders (reflecting territorial defence). Biting the snake was the most common form of attack, although damselfish and blennies also slapped snakes with the tail, or (blennies only) plugged the nest entrance with the parent fish's body. Gobies rarely defended the nest, although they sometimes bit or threw sand at the snake. A snake was more likely to flee if it was attacked before it began feeding rather than after it found the eggs (82% versus 3% repelled) and if bitten on the head rather than the body (68% versus 53%). Tail‐slaps were not effective, although plugging the burrow and throwing sand often caused snakes to flee. These strong patterns reflect phylogenetic variation in fish behaviour (e.g. damselfish detect a snake approach sooner than do substrate‐dwelling blennies and gobies) coupled with intraspecific variation in snake diets. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 415–425.     

Reproductive potential of Schistocephalus solidus‐infected male three‐spined stickleback Gasterosteus aculeatus from two U.K. populations

Male three‐spined stickleback Gasterosteus aculeatus from two U.K. populations with endemic infections of the cestode Schistocephalus solidus were brought into the laboratory prior to the breeding season and transferred to nesting tanks under conditions designed to stimulate sexual maturation. Nesting and courtship behaviours were scored over a 35 day period, after which fish were euthanized and the liver, spleen, kidney and gonads were weighed. Among G. aculeatus from a park pond in Leicester, U.K., infected males rarely engaged in reproductive behaviours and exhibited reduced indices of sexual development, body condition and general health, with effects being largely independent of relative parasite mass (parasite index, I_P). In contrast, the reproductive behaviour of infected fish from Kendoon Loch in Dumfriesshire, U.K. appeared to be less severely affected, with infected fish regularly building nests and courting females under laboratory conditions. This was paralleled by a more limited effect of infection on physiological indicators of development, condition and general health. Furthermore, behavioural and physiological variables typically correlated with I_P among infected fish from this population. Although comparing the performance of infected fish from the two populations directly was difficult due to potentially confounding factors, the results support the findings of recent studies showing that the effects of S. solidus on host reproduction are unlikely to be uniform across G. aculeatus populations. One possibility is that variation in the effects of infection arises from differences in the co‐evolutionary association times of G. aculeatus with the parasite.     

Links between blood parasites,blood chemistry,and the survival of nestling American crows

Many studies have used the avian hemosporidians (Leucocytozoon, Plasmodium, and Hemoproteus) to test hypotheses of host–parasite co‐evolution, yet documented health and survival consequences of these blood parasites vary among studies and generalizations about their pathogenicity are debatable. In general, the negative effects of the hemosporidians are likely to be greatest during acute infections of young birds, yet most previous studies in wild passerines have examined chronic effects in adults. Here, we evaluated responses of nestling American crows (Corvus brachyrhynchos) to acute infection (prevalence and burden), as well as its short‐ and long‐term survival consequences. We used panel of nine hematological and biochemical parameters that are regularly used to evaluate the health of domestic animals, including leukocyte profiles, hematocrit, and plasma proteins. We assessed the effects of infection on survival in a mark‐recapture framework. Overall, 56% of crows (n = 321 samples) were infected by at least one of the three genera. Infections by all genera were associated with elevated plasma proteins and globulins, which could indicate an adaptive immune response. However, only Plasmodium infections were associated with low hematocrit (anemia) and lower fledging success, possibly mediated by the negative effect of low hematocrit values on body condition. Moreover, early Plasmodium infection (<40 days of age) had long‐term survival implications: it was associated with lower apparent survival probability within 3 years after fledging. These results suggest that young crows mounted an adaptive immune response to all three genera. Short‐ and long‐term pathological effects, however, were only apparent with Plasmodium infections.     

Virulence and competitive ability in an obligately killing parasite

Mixed infections are thought to have a major influence on the evolution of parasite virulence. During a mixed infection, higher within‐host parasite growth is favored under the assumption that it is critical to the competitive success of the parasite. As within‐host parasite growth may also increase damage to the host, a positive correlation is predicted between virulence and competitive success. However, when parasites must kill their hosts in order be transmitted, parasites may spend energy on directly attacking their host, even at the cost of their within‐host growth. In such systems, a negative correlation between virulence and competitive success may arise. We examined virulence and competitive ability in three sympatric species of obligately killing nematode parasites in the genus Steinernema. These nematodes exist in a mutualistic symbiosis with bacteria in the genus Xenorhabdus. Together the nematodes and their bacteria kill the insect host soon after infection, with reproduction of both species occurring mainly after host death. We found significant differences among the three nematode species in the speed of host killing. The nematode species with the lowest and highest levels of virulence were associated with the same species of Xenorhabdus, indicating that nematode traits, rather than the bacterial symbionts, may be responsible for the differences in virulence. In mixed infections, host mortality rate closely matched that associated with the more virulent species, and the more virulent species was found to be exclusively transmitted from the majority of coinfected hosts. Thus, despite the requirement of rapid host death, virulence appears to be positively correlated with competitive success in this system. These findings support a mechanistic link between parasite growth and both anti‐competitor and anti‐host factors.