Elucidating the hidden infection dynamics between hairworms and their aquatic and terrestrial hosts
Parasitism, the act of acquiring nutrients at the expense of a host organism, has arguably become the most prevalent mode of life on this planet. Despite the remarkable diversity of parasite species, their life strategies can be grouped mainly into only six general categories. This is reflected by a convergent evolution in life cycle attributes and how parasites successfully transition from one development stage to the next. In parallel to the evolution of these general life strategies, many parasite lineages have been selected to adaptively increase the odds of successfully completing their life cycle through phenotypic changes in their hosts, a phenomenon known as host manipulation. Perhaps one of the best-known examples of parasites capable of host manipulation are freshwater hairworms (phylum Nematomorpha), which somehow cause their terrestrial host to enter water, for the parasite to exit and reproduce. Despite their notoriety, there is still much left to discover about this group of highly specialised organisms. In fact, I show that much of what is known about the host manipulation of hairworms has been largely misrepresented in both the popular media and the scientific literature. Therefore, due to the cryptic nature of parasite life cycles in general, understanding host-parasite interactions, including host manipulation, requires an in-depth investigation. This thesis aims to elucidate some of the hidden interactions between hairworms and their aquatic and terrestrial hosts in New Zealand. In the core chapters, I take the reader through the complex life cycle of hairworms to answer some of the broad research questions on the ecology and host-parasite interactions of this group. First, by observing naturally infected aquatic hosts, I show that the internal defence reactions of these hosts toward hairworm larvae and cysts are more complex than previously thought, casting doubt on the true lethality of aquatic host immunity towards hairworms. Then, I quantify the losses of hairworms in dead-end hosts from two communities of aquatic macroinvertebrates, showing that certain aquatic species can represent important population sinks for hairworms. Here, I reveal that, depending on the species, hairworms follow distinct host transmission routes to reach land, depending on where and when they are consumed by the aquatic hosts in the streams. In light of these challenges that hairworms face in the water, I present some evidence, from a controlled observational study, that they may in turn accelerate their transition to land by decreasing the development time of aquatic hosts, thus increasing the odds of successfully completing their life cycle. Finally, I show that different species of hairworm are capable of infecting a diverse range of terrestrial hosts through a survey of two communities of terrestrial arthropods in subalpine habitats, which suggests that hairworms may be less host-specific and more widespread than what is currently known in New Zealand. This thesis uncovers some of the complex and hidden interactions between hairworms and their aquatic and terrestrial hosts. Still, there remains much to explore of the ecology and infection dynamics of this fascinating, yet poorly understood group of parasites.
Advisor: Poulin, Robert
Degree Name: Doctor of Philosophy
Degree Discipline: Department of Zoology
Publisher: University of Otago
Keywords: host-parasite interaction; Nematomorpha; hairworm; New Zealand; parasite
Research Type: Thesis