Reciprocal effects of adaptive radiations on the evolution of interspecific interactions, like parasitism, remain barely explored. We test whether the recent radiations of European whitefish (Coregonus spp.) across and within perialpine and subarctic lakes promote its parasite Proteocephalus fallax (Platyhelminthes: Cestoda) to undergo host repertoire expansion via opportunity and ecological fitting, or adaptive radiation by specialization. Using de novo genomic data, we examined P. fallax differentiation across lakes, within lakes across sympatric host species, and the contributions of host genetics versus host habitat use and trophic preferences. Whitefish intralake radiations prompted parasite host repertoire expansion in all lakes, whereas P. fallax differentiation remains incipient among sympatric fish hosts. Whitefish genetic differentiation per se did not explain the genetic differentiation among its parasite populations, ruling out codivergence with the host. Instead, incipient parasite differentiation was driven by whitefish phenotypic radiation in trophic preferences and habitat use in an arena of parasite opportunity and ecological fitting to utilize resources from emerging hosts. Whilst the whitefish radiation provides a substrate for the parasite to differentiate along the same water-depth ecological axis as Coregonus spp., the role of the intermediate hosts in parasite speciation may be overlooked. Parasite multiple-level ecological fitting to both fish and crustacean intermediate hosts resources may be responsible for parasite population substructure in Coregonus spp. We propose parasites' delayed arrival was key to the initial burst of postglacial intralake whitefish diversification, followed by opportunistic tapeworm host repertoire expansion and a delayed nonadaptive radiation cascade of incipient tapeworm differentiation. At the geographical scale, dispersal, founder events, and genetic drift following colonization of spatially heterogeneous landscapes drove strong parasite differentiation. We argue that these microevolutionary processes result in the mirroring of host-parasite phylogenies through phylogenetic tracking at macroevolutionary and geographical scales.

Aquatic Restoration and Fisheries section Federal Office for the Environment Bern Switzerland

Department of Arctic Biology The Arctic University of Norway Tromsø Norway

Department of Evolutionary Parasitology Institute of Parasitology Biology Centre of the Czech Academy of Sciences České Budějovice Czech Republic

Department of Fish Ecology and Evolution Centre of Ecology Evolution and Biogeochemistry Eawag Swiss Federal Institute of Aquatic Science and Technology Kastanienbaum Switzerland

Department of Forestry and Wildlife Management Inland Norway University of Applied Science Elverum Norway

Department of Genetics and Evolution University of Geneva Geneva Switzerland

Department of Invertebrates Natural History Museum of Geneva Geneva Switzerland

Division of Aquatic Ecology and Evolution Institute of Ecology and Evolution University of Bern Bern Switzerland

Norwegian College of Fishery Science UiT The Arctic University of Norway Tromsø Norway

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Redescription of Proteocephalus fallax La Rue, 1911 (Cestoda) and a list of proteocephalid tapeworms of whitefish (Coregonus spp.)