Two steps to suicide in crickets harbouring hairworms

doi:10.1016/j.anbehav.2008.07.018

Animal Behaviour

Volume 76, Issue 5, November 2008, Pages 1621-1624

https://doi.org/10.1016/j.anbehav.2008.07.018 Get rights and content

The hairworm (Nematomorpha) Paragordius tricuspidatus has the ability to alter the behaviour of its terrestrial insect host (the cricket Nemobius sylvestris), making it jump into the water to reach its reproductive habitat. Because water is a limited and critical resource in the ecosystem, we predicted that hairworms should adaptively manipulate host behaviour to maximize parasite reproductive success. Our results supported the hypothesis that the host manipulation strategy of hairworms consists of at least two distinct steps, first the induction of erratic behaviour and then suicidal behaviour per se. Hairworms secured mating by starting to manipulate their host before being fully mature. Once induced, the cricket's suicidal behaviour was maintained until the host found water but the fecundity of worms decreased over time. As expected, the fecundity of worms was better in crickets with suicidal rather than erratic behaviour.

Section snippets

Origin of Specimens

The host species considered in our study was the cricket Nemobius sylvestris and all specimens came from Avènes les Bains (43°45′N, 3°06′E, southern France) as in previous studies (Thomas et al. 2002). Uninfected N. sylvestris are exclusively found in the forest. Conversely, it is common to find specimens parasitized by the hairworm Paragordius tricuspidatus in atypical habitats surrounding the forest (paved areas such as car parks and beside buildings and near swimming pools). We collected

Behavioural Tests

The analyses were based on 173 infected individuals and 158 uninfected ones. As expected, the rate of suicide was significantly higher among infected individuals than uninfected ones (infected: 81.50%; uninfected: 9.82%; Fisher's exact test: P < 0.001). The proportion of parasitized crickets committing suicide varied significantly over time (Fisher's exact test on table r × k: P = 0.0002; Fig. 1a). A closer examination of the data (and after a Bonferroni correction) revealed that this difference was

Discussion

The ability to fine tune changes in host behaviour to the moment when parasites are ready to be transmitted has been proposed as a convincing piece of evidence supporting the hypothesis that host manipulation may have evolved to enhance parasite transmission (Bethel and Holmes, 1973, Poulin, 1995). Parasites, just like the hosts they infect, must contend with adverse and often unpredictable environmental conditions. This requires an adaptive synchrony of key developmental stages with favourable

Acknowledgments

M.I.S. was supported by a postdoctoral grant from the Ministerio de Ciencia y Tecnología (Spain). F.T. is supported by a grant from ANR project Blanc. We thank the thermal station of Avènes-Les-Bains for their cooperation during the field study. T. Lefevre and C. Lebarbenchon helped with field work. We also thank two anonymous referees, the Editor and P. Heeb for helpful comments on the paper.

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‘Adaptive’ change in the behaviour of parasitized animals: a critical review
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Altered evasive behaviour and responses to light in amphipods harboring acanthocephalan cystacanths
Journal of Parasitology
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‘Suicide’ of crickets harbouring hairworm: a proteomics investigation
Insect Molecular Biology
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The Extended Phenotype
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Contributions to the life histories of Gordius robustus Leidy and Paragordius varius (Leidy)
Illinois Biological Monographs
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Parasites and the Behavior of Animals
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There are more references available in the full text version of this article.

Cited by (28)

Rampant loss of universal metazoan genes revealed by a chromosome-level genome assembly of the parasitic Nematomorpha
2023, Current Biology
Parasites may manipulate host behavior to increase the odds of transmission or to reach the proper environment to complete their life cycle.¹^,² Members of the phylum Nematomorpha (known as horsehair worms, hairworms, or Gordian worms) are large endoparasites that affect the behavior of their arthropod hosts. In terrestrial hosts, they cause erratic movements toward bodies of water,³^,⁴^,⁵^,⁶ where the adult worm emerges from the host to find mates for reproduction. We present a chromosome-level genome assembly for the freshwater Acutogordius australiensis and a draft assembly for one of the few known marine species, Nectonema munidae. The assemblies span 201 Mbp and 213 Mbp in length (N50: 38 Mbp and 716 Kbp), respectively, and reveal four chromosomes in Acutogordius, which are largely rearranged compared to the inferred ancestral condition in animals. Both nematomorph genomes have a relatively low number of genes (11,114 and 8,717, respectively) and lack a high proportion (∼30%) of universal single-copy metazoan orthologs (BUSCO genes⁷). We demonstrate that missing genes are not an artifact of the assembly process, with the majority of missing orthologs being shared by the two independent assemblies. Missing BUSCOs are enriched for Gene Ontology (GO) terms associated with the organization of cilia and cell projections in other animals. We show that most cilium-related genes conserved across eukaryotes have been lost in Nematomorpha, providing a molecular basis for the suspected absence of ciliary structures in these animals.
Infection patterns and new definitive host records for New Zealand gordiid hairworms (phylum Nematomorpha)
2022, Parasitology International
Citation Excerpt :
The primary goal of the current study was to investigate the infection dynamics of gordiid hairworms in their definitive terrestrial hosts across two communities of subalpine invertebrates in New Zealand. Previous studies suggested that hairworms induce erratic movements in their host [16–18], but no direct tests of this hypothesis have been performed to date. Although we discovered multiple new hairworm-host associations in both sampling sites, it was not possible to observe whether mature hairworms affected host behaviour to increase their likelihood of entering water or not.
Some parasites modify the phenotype of their host in order to increase transmission to another host or to an environment suitable for reproduction. This phenomenon, known as host manipulation, is found across many parasite taxa. Freshwater hairworms are known for the behavioural changes they cause in their terrestrial arthropod hosts, increasing their likelihood of entering water to exit the host and reproduce. Understanding how infected arthropods move around in the natural environment could help uncover alterations in spatial distribution or movement induced by hairworms in their terrestrial definitive hosts. Moreover, few hairworm-host records exist for New Zealand, so any additional record could help elucidate their true host specificity. Here, we investigated whether infected terrestrial arthropods were more likely to approach streams in two subalpine communities of invertebrates, using a spatial grid of specialised pitfall traps. Although hairworm infection could not explain the movements of arthropod hosts near streams, we found several new host records for hairworms, including the first records for the recently described Gordionus maori. We also found some new host-parasite associations for mermithid nematodes. These records show that the host specificity of hairworms is quite low, suggesting that their diversity and distribution may be greater than what is currently known for New Zealand.
Host manipulation in the face of environmental changes: Ecological consequences
2015, International Journal for Parasitology: Parasites and Wildlife
Several parasite species, particularly those having complex life-cycles, are known to induce phenotypic alterations in their hosts. Most often, such alterations appear to increase the fitness of the parasites at the expense of that of their hosts, a phenomenon known as “host manipulation”. Host manipulation can have important consequences, ranging from host population dynamics to ecosystem engineering. So far, the importance of environmental changes for host manipulation has received little attention. However, because manipulative parasites are embedded in complex systems, with many interacting components, changes in the environment are likely to affect those systems in various ways. Here, after reviewing the ecological importance of manipulative parasites, we consider potential causes and consequences of changes in host manipulation by parasites driven by environmental modifications. We show that such consequences can extend to trophic networks and population dynamics within communities, and alter the ecological role of manipulative parasites such as their ecosystem engineering. We suggest that taking them into account could improve the accuracy of predictions regarding the effects of global change. We also propose several directions for future studies.
Phylum Nematomorpha
2015, Thorp and Covich's Freshwater Invertebrates: Ecology and General Biology: Fourth Edition
The Nematomorpha represent one of three entirely parasitic animal phyla. However, hairworms have often been called one of the most understudied and underappreciated groups of animals. Two classes exist within the phylum and include the marine, Nectonematida, and the freshwater, Gordiida. Freshwater hairworms, can be over 2 m long and seem to appear suddenly in domestic sources of water (swimming pools, toilets, pet bowls, etc.), thus making human interactions with them quite common. As juveniles, gordiids infect terrestrial arthropods but are free-living in various aquatic habitats as adults. They have complex life-cycles which include multiple hosts and a free-living aquatic phase. More recently, nematomorphs have gone through a scientific renaissance. This recent work on gordiids has focused on understanding their taxonomy, distribution, life history and ecology. Additional emphasis has been placed on using nematomorphs as model systems to study the biochemical mechanisms of host manipulation and as indicators of environmental stressors. In this chapter, we review all pertinent information on the general biology of freshwater gordiids and we provide new information on hairworm life cycles and novel sampling and culturing techniques for this fascinating group of freshwater invertebrates.
Parasites and forest chronosequence: Long-term recovery of nematomorph parasites after clear-cut logging
2014, Forest Ecology and Management
Temporal scales at which anthropogenic disturbances affect ecosystem linkages are often unclear. The nematomorph parasites tightly link forests to stream ecosystems via manipulation of their terrestrial hosts. We examined the abundance and species/genetic diversities of nematomorphs with their terrestrial hosts along a forest-recovery gradient after clear-cut logging, using a chronosequence. Only one nematomorph species was found from eight watersheds with different forest ages (3–48 years). The nematomorphs suffered local extinction immediately after logging and then increased linearly with forest age. Their relative abundances were highest in September in older forests, but in October in younger forests, suggesting clear-cut logging can cause not only long-term (>50 years) disruption of the magnitude but also timing of the forest–stream linkage mediated by the nematomorphs. Camel crickets (Diestrammena tsushimensis and D. elegantissima), dominant definitive hosts of the nematomorphs, recovered with a peak at around 30-year-old forests, which was insufficient to explain the long-term recovery of the nematomorphs. This study provided an empirical example of the time-scale (>50 years) at which forests and streams should be managed as integrated systems.
Intraspecific variability in host manipulation by parasites
2011, Infection, Genetics and Evolution
Citation Excerpt :
Accordingly, senescence effects would be rare. Sanchez et al. (2008) indeed found that when crickets harbouring a mature hairworm were experimentally prevented from reaching an aquatic area (where the adult parasites reproduce), the fecundity of the worm decreases through time but the manipulative effort exerted by the parasite is maintained. It is also possible that senescence effects are not common in natural conditions because host manipulation (timing, intensity, etc.) has evolved to ensure an efficient transmission prior to senescence.
Manipulative parasites have the capacity to alter a broad range of phenotypic traits in their hosts, extending from colour, morphology and behaviour. While significant attention has been devoted to describing the diversity of host manipulation among parasite clades, and testing the adaptive value of phenotypic traits that can be manipulated, there is increasing evidence that variation exists in the frequency and intensity of the changes displayed by parasitized individuals within single host-manipulative parasite systems. Such variability occurs within individuals, between individuals of a same population, and across populations. Here we review the non-genetic (i.e. environmental) and genetic causes of variability in host behaviour manipulation, discuss its evolutionary significance, and propose directions for further researches.

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¹: A. Schmidt-Rhaesa is at Zoomorphologie und Systematik, Universität Bielefeld, Postfach 100131, D-33501 Bielefeld, Germany.

²: D. P. Hughes is at the Centre for Social Evolution, Institute of Biology, Universitetsparken 15, DK-21000 Copenhagen.

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Animal Behaviour

Section snippets

Origin of Specimens

Behavioural Tests

Discussion

Acknowledgments

References (13)

‘Adaptive’ change in the behaviour of parasitized animals: a critical review

International Journal of Parasitology

Altered evasive behaviour and responses to light in amphipods harboring acanthocephalan cystacanths

Journal of Parasitology

‘Suicide’ of crickets harbouring hairworm: a proteomics investigation

Insect Molecular Biology

The Extended Phenotype

Contributions to the life histories of Gordius robustus Leidy and Paragordius varius (Leidy)

Illinois Biological Monographs

Parasites and the Behavior of Animals

Cited by (28)

Rampant loss of universal metazoan genes revealed by a chromosome-level genome assembly of the parasitic Nematomorpha

Infection patterns and new definitive host records for New Zealand gordiid hairworms (phylum Nematomorpha)

Host manipulation in the face of environmental changes: Ecological consequences

Phylum Nematomorpha

Parasites and forest chronosequence: Long-term recovery of nematomorph parasites after clear-cut logging

Intraspecific variability in host manipulation by parasites