Host-parasite associations in the globally invasive Xenopus laevis

Abstract

In the Anthropocene, the movement of species takes place at unprecedented rates. As ranges shift in reaction to climate change or through human mediation, we need to understand the complex novel interactions that arise. In the present study, a multidisciplinary approach to invasion biology, exemplifying the application of parasite data, is advanced. To this end, the world’s most widespread frog, Xenopus laevis (Daudin, 1802) (Anura: Pipidae), and its diverse assemblage of metazoan parasites are proposed as a model host-parasite system during range expansion. As a baseline for further bio-invasion investigations, ¨ıntegrative taxonomy”was applied to address knowledge gaps regarding the associations between native X. laevis and nematode parasites. Thus followed the redescription of three members of the Camallanidae, providing indispensable molecular data, as well as the first report of seven more nematode species that are associated with X. laevis. The parasite dynamics revealed in this survey highlights the need for the inclusion of DNA barcodes, emphasises the role of X. laevis as a parasite reservoir and provides insight on the origin of the parasite species of X. laevis in the invasive range. As a next step, the geographic replicates of parasitological surveys of X. laevis in its native southern Africa and the invasive populations in France, Portugal, California and Chile, acted as a ”natural experiment”to identify over-arching patterns in the host-parasite dynamics of invasive species. This approach demonstrates the Enemy Release Hypothesis for this globally invasive amphibian host yet also reveals complex parasite dynamics of X. laevis populations in South Africa and western France upon closer inspection. The parasite communities of expanding populations of X. laevis are typified as more variable than the communities from host populations from natural habitats. The divergent responses of parasite taxa to range expansion show that these systems merit further study to predict the future of host-parasite associations amidst global change. Finally, this study proves the concept that parasite data sets can provide an independent line of evidence to address questions in invasion biology. This approach was applied to trace the intraspecific cryptic invasions of X. leavis in its native range with the help of its highly associated polystomatid parasite, Protopolystoma xenopodis (Price, 1943)

Bychowsky, 1957 (Monogenea: Polystomatidae). The comparative phylogeography of these ”holistic specimens”revealed widespread lineage-level invasion events of X. laevis across southern Africa, provided insight on the origin of the French invasive population of the host and even revealed the role of small-scale human-mediated translocation of this frog via the recreational fishing community in shaping its dispersal patterns in the native range. In order to aid future investigators in the development of mitochondrial markers when using polystomatid parasites as tags for host phylogeography, the complete mitochondrial genome of P. xenopodis was sequenced and annotated. Intraspecific comparison of the mitogenome sequences of this polystomatid identified promising gene regions for phylogeographic analyses. Ultimately, a multidisciplinary approach that incorporates both host and parasite data holds great potential in invasion biology. This study demonstrates this approach via the lens of a well-studied model host-parasite system.