Abstract
Numerous parasite species have evolved complex life cycles with multiple, subsequent hosts. For trematodes, life cycles have evolved from exploiting a single vertebrate host to incorporating intermediate hosts, with most trematodes now utilising three consecutive hosts. Each transmission event in multi-host life cycles creates obstacles selecting for various adaptations, one of which is facultative life cycle abbreviation.
In trematodes, facultative life cycle abbreviation occurs through progenesis, i.e. precocious maturity and reproduction via self-fertilisation within the second intermediate host. Progenesis eliminates the need for the definitive host and facilitates life cycle completion. Adopting a progenetic cycle may be a conditional strategy in response to environmental cues related to low probability of transmission to the definitive host. In this study, the effects of environmental factors on the reproductive strategy of the progenetic trematode, Stegodexamene anguillae, were investigated using laboratory and field studies. In the three-host life cycle, S. anguillae sexually reproduces within definitive hosts, two eel species, whereas in the progenetic life cycle, S. anguillae reproduces by selfing within the metacercarial cyst in tissues of the second intermediate fish host.
Environmental factors that affect the probability of transmission to a definitive eel host, such as longevity of the current host and abundance of eels, should strongly influence the reproductive strategy of S. anguillae. The results suggest that cues from hosts under stressful conditions and encystment site within the host may signal transmission opportunities to the parasite so that it may adjust its developmental strategy accordingly. However, presence or abundance of the definitive eel host does not seem to affect the frequency of progenesis in S. anguillae.
Progenetic individuals face egg dispersal challenges associated with reproducing within metacercarial cysts inside a second intermediate host. Most progenetic species await host death for their eggs to be released into the environment. The present study investigated natural temporal variation of progenesis in S. anguillae in its second intermediate fish host and the effect of the fish’s reproductive cycle on progenesis. A greater proportion of individuals became progenetic in the gonads of female fish hosts than in other tissues. Additionally, progenesis of worms in the gonads was correlated with seasonal day length and temperature changes, major factors controlling fish reproduction. Host spawning events are likely to be an avenue of egg dispersal for the parasite, with the adoption of progenesis being conditional on whether or not the parasite can benefit from fish spawning.
This is the first study investigating variation in the frequency of progenesis among populations. Geographic variation was found in S. anguillae, independently of eel abundance or parasite population structure. Although not associated with geography, strong genetic differentiation existed between two clades of S. anguillae.
Altogether, this thesis provides evidence that life cycle abbreviation in S. anguillae is affected by various factors. This study is the first to compare life cycle strategies among parasite populations and provide insight into the real plasticity of life cycle abbreviation in nature. These findings highlight the often unrecognised plasticity in parasite developmental and transmission strategies.