Studies on parasite biogeography and host spectrum provide insights into the processes driving parasite diversification. Global geographical distribution and a multi-host spectrum make the tapeworm Ligula intestinalis a promising model for studying both the vicariant and ecological modes of speciation in parasites. To understand the relative importance of host association and biogeography in the evolutionary history of this tapeworm, we analysed mtDNA and reduced-represented genomic SNP data for a total of 139 specimens collected from 18 fish-host genera across a distribution range representing 21 countries. Our results strongly supported the existence of at least 10 evolutionary lineages and estimated the deepest divergence at approximately 4.99-5.05 Mya, which is much younger than the diversification of the fish host genera and orders. Historical biogeography analyses revealed that the ancestor of the parasite diversified following multiple vicariance events and was widespread throughout the Palearctic, Afrotropical, and Nearctic between the late Miocene and early Pliocene. Cyprinoids were inferred as the ancestral hosts for the parasite. Later, from the late Pliocene to Pleistocene, new lineages emerged following a series of biogeographic dispersal and host-switching events. Although only a few of the current Ligula lineages show narrow host-specificity (to a single host genus), almost no host genera, even those that live in sympatry, overlapped between different Ligula lineages. Our analyses uncovered the impact of historical distribution shifts on host switching and the evolution of host specificity without parallel host-parasite co-speciation. Historical biogeography reconstructions also found that the parasite colonized several areas (Afrotropical and Australasian) much earlier than was suggested by only recent faunistic data.

Čakovice Týnec nad Sázavou Czech Republic

Department of Environmental Science Faculty of Natural Resources University of Tehran Karaj Iran

Department of Life and Environmental Sciences Marche Polytechnic University Ancona Italy

Department of Zoology University of Otago Dunedin New Zealand

Faculty of Science University of South Bohemia České Budějovice Czech Republic; Institute of Parasitology Biology Centre CAS České Budějovice Czech Republic

Institute of Parasitology Biology Centre CAS České Budějovice Czech Republic

Research Administration and Development and 2 DSI NRF SARChI Chair Department of Biodiversity University of Limpopo South Africa

Research Center for Fisheries and Aquaculture Institute of Aquaculture and Environmental Safety Hungarian University of Agriculture and Life Sciences Szarvas Hungary

School of Environmental Studies University of Eldoret Kenya

Tanzania Fisheries Research Institute Kyela Mbeya Tanzania

UMR 5174 EDB CNRS IRD Université Toulouse 3 Paul Sabatier France

References provided by Crossref.org

Host-Associated Genetic Differentiation in the Face of Ongoing Gene Flow: Ecological Speciation in a Pathogenic Parasite of Freshwater Fish

Testing the radiation cascade in postglacial radiations of whitefish and their parasites: founder events and host ecology drive parasite evolution

Integrating phylogenetic, phylogeographic, and morphometric analyses to reveal cryptic lineages within the genus Asaccus (Reptilia: Squamata: Phyllodactylidae) in Iran

Highly resolved genome assembly and comparative transcriptome profiling reveal genes related to developmental stages of tapeworm Ligula intestinalis