Search

Artificial light at night (ALAN) negatively impacts organisms in many ways, from their feeding behaviors to their response and ability to deal with disease. Our knowledge of ALAN is focused on hosts, but we must also consider their parasites, which constitute half of all described animal species. Here, we assessed the impact of light exposure on a model host-parasite system (Poecilia reticulata and the ectoparasitic monogenean Gyrodactylus turnbulli). First, parasite-free fish were exposed to 12:12 h light:dark (control) or 24:0 h light:dark (ALAN) for 21 days followed by experimental infection. Second, naturally acquired G. turnbulli infections were monitored for 28 days during exposure of their hosts to a specified light regime (6:18 h, 12:12 h, or 24:0 h light:dark). Experimentally infected fish exposed to constant light had, on average, a greater maximum parasite burden than controls, but no other measured parasite metrics were impacted. Host feeding behavior was also significantly affected: fish under ALAN fed faster and took more bites than controls, whilst fish exposed to reduced light fed slower. Thus, ALAN can impact parasite burdens, even in the short term, and altering light conditions will impact fish feeding behavior. Such responses could initiate disease outbreaks or perturb food-webs with wider ecological impacts., (© 2024 The Author(s). Journal of Fish Biology published by John Wiley & Sons Ltd on behalf of Fisheries Society of the British Isles.)

Parasites display a wide range of behaviours that are frequently overlooked in favour of host responses. Understanding these behaviours can improve parasite control through a more precise application or development of new behaviour-based strategies. In aquaculture fish lice are an ongoing problem, infections reduce fishery production and control options are limited. Fish lice are distinct in their ability to survive and swim off hosts, allowing the transmission to multiple fish hosts across their lifespan. Here we assessed the off-host behaviour of Argulus foliaceus (a freshwater fish louse) and observed a diurnal rhythmical pattern in their behaviour. This pattern was lost when lice were exposed to constant darkness, indicating that the behaviour is not endogenously driven. Males were consistently active in light with reduced activity in darkness. In contrast, females were active during light and dark phases with peak activity at the start of dark periods. A. foliaceus was also strongly attracted to a light stimulus, preferring white- and blue-coloured lights over green- or red-coloured lights. Light is a strong driver of fish louse activity and could be used to trap parasites. Aquaculture light regimes could also be altered to reduce parasite attraction and activity.

Schistosomiasis, a neglected tropical disease of medical and veterinary importance, transmitted through specific freshwater snail intermediate hosts, is targeted for elimination in several endemic regions in sub-Saharan Africa. Multi-disciplinary methods are required for both human and environmental diagnostics to certify schistosomiasis elimination when eventually reached. Molecular xenomonitoring protocols, a DNA-based detection method for screening disease vectors, have been developed and trialed for parasites transmitted by hematophagous insects, such as filarial worms and trypanosomes, yet few have been extensively trialed or proven reliable for the intermediate host snails transmitting schistosomes. Here, previously published universal and Schistosoma- specific internal transcribed spacer (ITS) rDNA primers were adapted into a triplex PCR primer assay that allowed for simple, robust, and rapid detection of Schistosoma haematobium and Schistosoma bovis in Bulinus snails. We showed this two-step protocol could sensitively detect DNA of a single larval schistosome from experimentally infected snails and demonstrate its functionality for detecting S. haematobium infections in wild-caught snails from Zanzibar. Such surveillance tools are a necessity for succeeding in and certifying the 2030 control and elimination goals set by the World Health Organization.

With expanding human populations, the food sector has faced constant pressure to sustainably expand and meet global production demands. In aquaculture this frequently manifests in an animal welfare crisis, with fish increasingly farmed under high production, high stress conditions. These intense environments can result in fish stocks having a high susceptibility to infection, with parasites and associated disease one of the main factors limiting industry growth. Prediction of infection dynamics is key to preventative treatment and mitigation. Considering the climatic and technology driven changes facing aquaculture, an understanding of how parasites react across a spectrum of conditions is required. Here we assessed the impact of temperature, infection density and host species on the life history traits of Argulus foliaceus, a common palearctic fish louse, representative of a parasite group problematic in freshwater aquaculture and fisheries worldwide. Temperature significantly affected development, growth and survival; parasites hatched and developed faster at higher temperatures, but also experienced shorter lifespans when maintained off the host. At high temperatures, these parasites will likely experience a short generation time as their life history traits are completed more rapidly. A. foliaceus additionally grew faster on natural hosts and at lower infection densities. Ultimately such results contribute to prediction of population dynamics, aiding development of effective control to improve animal welfare and reduce industry loss., (Copyright © 2020 Elsevier Ltd. All rights reserved.)

Background: Urogenital schistosomiasis, caused by infection with Schistosoma haematobium, is endemic in Niger but complicated by the presence of Schistosoma bovis, Schistosoma curassoni and S. haematobium group hybrids along with various Bulinus snail intermediate host species. Establishing the schistosomes and snails involved in transmission aids disease surveillance whilst providing insights into snail-schistosome interactions/compatibilities and biology., Methods: Infected Bulinus spp. were collected from 16 villages north and south of the Niamey region, Niger, between 2011 and 2015. From each Bulinus spp., 20-52 cercariae shed were analysed using microsatellite markers and a subset identified using the mitochondrial (mt) cox1 and nuclear ITS1 + 2 and 18S DNA regions. Infected Bulinus spp. were identified using both morphological and molecular analysis (partial mt cox1 region)., Results: A total of 87 infected Bulinus from 24 sites were found, 29 were molecularly confirmed as B. truncatus, three as B. forskalii and four as B. globosus. The remaining samples were morphologically identified as B. truncatus (n = 49) and B. forskalii (n = 2). The microsatellite analysis of 1124 cercariae revealed 186 cercarial multilocus genotypes (MLGs). Identical cercarial genotypes were frequently (60%) identified from the same snail (clonal populations from a single miracidia); however, several (40%) of the snails had cercariae of different genotypes (2-10 MLG's) indicating multiple miracidial infections. Fifty-seven of the B. truncatus and all of the B. forskalii and B. globosus were shedding the Bovid schistosome S. bovis. The other B. truncatus were shedding the human schistosomes, S. haematobium (n = 6) and the S. haematobium group hybrids (n = 13). Two B. truncatus had co-infections with S. haematobium and S. haematobium group hybrids whilst no co-infections with S. bovis were observed., Conclusions: This study has advanced our understanding of human and bovid schistosomiasis transmission in the Niger River Valley region. Human Schistosoma species/forms (S. haematobium and S. haematobium hybrids) were found transmitted only in five villages whereas those causing veterinary schistosomiasis (S. bovis), were found in most villages. Bulinus truncatus was most abundant, transmitting all Schistosoma species, while the less abundant B. forskalii and B. globosus, only transmitted S. bovis. Our data suggest that species-specific biological traits may exist in relation to co-infections, snail-schistosome compatibility and intramolluscan schistosome development.

While group formation provides antipredatory defences, increases foraging efficiency and mating opportunities, it can be counterintuitive by promoting disease transmission amongst social hosts. Upon introduction of a pathogen, uninfected individuals often modify their social preferences to reduce infection risk. Infected hosts also exhibit behavioural changes, for example, removing themselves from a group to prevent an epidemic. Conversely, here we show how Trinidadian guppies infected with a directly transmitted ectoparasite, Gyrodactylus turnbulli, significantly increase their contact rates with uninfected conspecifics. As uninfected fish never perform this behaviour, this is suggestive of a parasite-mediated behavioural response of infected hosts, presumably to offload their parasites. In the early stages of infection, however, such behavioural modifications are ineffective in alleviating parasite burdens. Additionally, we show that fish exposed to G. turnbulli infections for a second time, spent less time associating than those exposed to parasites for the first time. We speculate that individuals build and retain an infection cue repertoire, enabling them to rapidly recognize and avoid infectious conspecifics. This study highlights the importance of considering host behavioural modifications when investigating disease transmission dynamics.

The major histocompatibility complex (MHC) is crucial to the adaptive immune response of vertebrates and is among the most polymorphic gene families known. Its high diversity is usually attributed to selection imposed by fast-evolving pathogens. Pathogens are thought to evolve to escape recognition by common immune alleles, and, hence, novel MHC alleles, introduced through mutation, recombination, or gene flow, are predicted to give hosts superior resistance. Although this theoretical prediction underpins host-pathogen "Red Queen" coevolution, it has not been demonstrated in the context of natural MHC diversity. Here, we experimentally tested whether novel MHC variants (both alleles and functional "supertypes") increased resistance of guppies ( Poecilia reticulata ) to a common ectoparasite ( Gyrodactylus turnbulli ). We used exposure-controlled infection trials with wild-sourced parasites, and Gyrodactylus -naïve host fish that were F 2 descendants of crossed wild populations. Hosts carrying MHC variants (alleles or supertypes) that were new to a given parasite population experienced a 35-37% reduction in infection intensity, but the number of MHC variants carried by an individual, analogous to heterozygosity in single-locus systems, was not a significant predictor. Our results provide direct evidence of novel MHC variant advantage, confirming a fundamental mechanism underpinning the exceptional polymorphism of this gene family and highlighting the role of immunogenetic novelty in host-pathogen coevolution., Competing Interests: The authors declare no conflict of interest.

Parasites vary widely in the diversity of hosts they infect: some parasite species are specialists-infecting just a single host species, while others are generalists, capable of infecting many. Understanding the factors that drive parasite host-generalism is of basic biological interest, but also directly relevant to predicting disease emergence in new host species, identifying parasites that are likely to have unidentified additional hosts, and assessing transmission risk. Here, we use mathematical models to investigate how variation in host body size and environmental temperature affect the evolution of parasite host-generalism. We predict that parasites are more likely to evolve a generalist strategy when hosts are large-bodied, when variation in host body size is large, and in cooler environments. We then explore these predictions using a newly updated database of over 20 000 fish-macroparasite associations. Within the database we see some evidence supporting these predictions, but also highlight mismatches between theory and data. By combining these two approaches, we establish a theoretical basis for interpreting empirical data on parasites' host specificity and identify key areas for future work that will help untangle the drivers of parasite host-generalism.This article is part of the themed issue 'Opening the black box: re-examining the ecology and evolution of parasite transmission'., (© 2017 The Authors.)

Parasitic infections are ubiquitous in wildlife, livestock and human populations, and healthy ecosystems are often parasite rich. Yet, their negative impacts can be extreme. Understanding how both anticipated and cryptic changes in a system might affect parasite transmission at an individual, local and global level is critical for sustainable control in humans and livestock. Here we highlight and synthesize evidence regarding potential effects of 'system changes' (both climatic and anthropogenic) on parasite transmission from wild host-parasite systems. Such information could inform more efficient and sustainable parasite control programmes in domestic animals or humans. Many examples from diverse terrestrial and aquatic natural systems show how abiotic and biotic factors affected by system changes can interact additively, multiplicatively or antagonistically to influence parasite transmission, including through altered habitat structure, biodiversity, host demographics and evolution. Despite this, few studies of managed systems explicitly consider these higher-order interactions, or the subsequent effects of parasite evolution, which can conceal or exaggerate measured impacts of control actions. We call for a more integrated approach to investigating transmission dynamics, which recognizes these complexities and makes use of new technologies for data capture and monitoring, and to support robust predictions of altered parasite dynamics in a rapidly changing world.This article is part of the themed issue 'Opening the black box: re-examining the ecology and evolution of parasite transmission'., (© 2017 The Authors.)

A common evolutionary response to predation pressure is increased investment in reproduction, ultimately resulting in a fast life history. Theory and comparative studies suggest that short-lived organisms invest less in defence against parasites than those that are longer lived (the pace of life hypothesis). Combining these tenets of evolutionary theory leads to the specific, untested prediction that within species, populations experiencing higher predation pressure invest less in defence against parasites. The Trinidadian guppy, Poecilia reticulata, presents an excellent opportunity to test this prediction: guppy populations in lower courses of rivers experience higher predation pressure, and as a consequence have evolved faster life histories, than those in upper courses. Data from a large-scale field survey showed that fish infected with Gyrodactylus parasites were of a lower body condition (quantified using the scaled mass index) than uninfected fish, but only in lower course populations. Although the evidence we present is correlational, it suggests that upper course guppies sustain lower fitness costs of infection, i.e. are more tolerant, than lower course guppies. The data are therefore consistent with the pace of life hypothesis of parasite defence allocation, and suggest that life-history traits mediate the indirect effect of predators on the parasites of their prey., (© 2015 The Author(s).)

Cryptic species complexes are common among parasites, which tend to have large populations and are subject to rapid evolution. Such complexes may arise through host-parasite co-evolution and/or host switching. For parasites that reproduce directly on their host, there might be increased opportunities for sympatric speciation, either by exploiting different hosts or different micro-habitats within the same host. The genus Gyrodactylus is a specious group of viviparous monogeneans. These ectoparasites transfer between teleosts during social contact and cause significant host mortality. Their impact on the guppy (Poecilia reticulata), an iconic evolutionary and ecological model species, is well established and yet the population genetics and phylogenetics of these parasites remains understudied. Using mtDNA sequencing of the host and its parasites, we provide evidence of cryptic speciation in Gyrodactylus bullatarudis, G. poeciliae and G. turnbulli. For the COII gene, genetic divergence of lineages within each parasite species ranged between 5.7 and 17.2%, which is typical of the divergence observed between described species in this genus. Different lineages of G. turnbulli and G. poeciliae appear geographically isolated, which could imply allopatric speciation. In addition, for G. poeciliae, co-evolution with a different host species cannot be discarded due to its host range. This parasite was originally described on P. caucana, but for the first time here it is also recorded on the guppy. The two cryptic lineages of G. bullatarudis showed considerable geographic overlap. G. bullatarudis has a known wide host range and it can also utilize a killifish (Anablepsoides hartii) as a temporary host. This killifish is capable of migrating overland and it could act as a transmission vector between otherwise isolated populations. Additional genetic markers are needed to confirm the presence of these cryptic Gyrodactylus species complexes, potentially leading to more in-depth genetic, ecological and evolutionary analyses on this multi-host-parasite system.

Introduced exotic species have the potential to spread their associated parasites to native species which can be catastrophic if these hosts are immunologically naïve to the novel parasite. The guppy (Poecilia reticulata) has been disseminated worldwide outside of its native habitat and therefore could be an important source of infection to native fish species. Its parasite fauna is dominated by the ectoparasitic monogeneans, Gyrodactylus turnbulli and Gyrodactylus bullatarudis. The current study tested the host specificity of G. bullatarudis by experimentally infecting a range of isolated fish hosts, including temperate species. Surprisingly, the parasite was capable of establishing and reproducing, for several days, on the three-spined stickleback when transferred directly to this host. We also established that G. bullatarudis could be transmitted under aquarium conditions at both 25 degrees C and 15 degrees C. At the higher temperature, the parasite was even capable of reproducing on this atypical host. The implications of these findings are discussed in terms of host specificity, host switching and climate change.

The directly transmitted viviparous gyrodactylids have high species richness but low morphological and biological diversity, and many species are recorded from only a single host. They therefore constitute a guild of species ideal for studies of the evolutionary significance of host specificity. The group has the widest host range of any monogenean family, being found on 19 orders of bony fish. However, individual species range from narrowly specific (71% of 402 described species recorded from a single host) to extremely catholic (Gyrodactylus alviga recorded from 16 hosts). Gyrodactylid-host interactions extend from 60 mya (G. lotae, G. lucii) down to 150 years (G. derjavini on Oncorhynchus mykiss). Co-evolution with the host is comparatively rare within the gyrodactylids, but host switching or ecological transfer is common, and has been facilitated by the mixing of fish strains that followed glaciation. In this review, we consider the factors responsible for gyrodactylid specificity patterns, using examples from our work on salmonid gyrodactylids including G. salaris, responsible for major epidemics on wild Atlantic salmon (Salmo salar) in Norway since 1975, and G. thymalli from grayling and G. derjavini from trout.G. salaris has a wide host range with highest population growth rates on Norwegian salmon strains. However, growth rates are variable on both host strains and species, because of the multitude of micro- and macro-environmental factors influencing parasite mortality and fecundity. A better predictor of performance is the proportion of fishes of a strain which are innately resistant to the parasite, a measure which is negatively correlated with the time to peak infection in a host strain. Population growth rate is also negatively correlated with age of infection; the initial rate, therefore, predicts best the suitability of a fish as host for G. salaris. The host response to gyrodactylids appears to be the same mechanism in all salmonids with innate resistance as one end of a spectrum, but influenced by stress and probably under polygenic control. Hybrid experiments show that performance of G. salaris on a host is heritable, and usually intermediate between that of the parents. This host response mechanism, coupled with the initial parasite population growth on a fish, determines the host specificity, i.e. whether the fish will be susceptible, a responder or innately resistant. The use of population growth rate parameters allows comparison of different hosts as a resource for a gyrodactylid. In the case of G. salaris, East Atlantic and Baltic strains of Atlantic salmon are core hosts, but other salmonids can physiologically sustain infections for considerable periods, and may be important in parasite dispersal and transmission. A further group of non-salmonid fishes are unable to sustain G. salaris reproduction, but can act as transport hosts.Population growth parameters are very labile to stressors and environmental factors, particularly temperature and salinity, and also other aspects of host ecology and water quality. These factors may also influence the spectrum of hosts that can be infected under particular conditions, and probably favoured ecological transfer of gyrodactylids between host species in periglacial conditions. G. salaris may still be undergoing post-glacial range expansion (aided by anthropogenic spread) as shown by the increase in the species range over the last 25 years. The origin of G. salaris, G. teuchis and G. thymalli is discussed in relation to glacial refugiums during the last ice age.