Taxon pulse dynamics, episodic dispersal and host colonization across Beringia drive diversification of a Holarctic tapeworm assemblage

Abstract

AbstractAimWe test the predictions of the Stockholm Paradigm, a synthesis of eco‐evolutionary theory explaining the nature of faunal assembly, host range and parasite diversification. Faunal diversification and assembly, manifested in patterns of host colonization, co‐adaptation and parasite speciation, are predicted to emerge as a consequence of alternating episodes of ecological disruption and stability. Specifically, for a diverse cestode genus (Arostrilepis), we evaluate the number and direction of Pleistocene dispersal events across Beringia, the number and relative timing of host colonization events and the relationship between host and parasite biogeographic histories and associations through time.LocationBeringia and adjacent temperate to arctic biomes in North America and Eurasia.TaxonArostrilepis (Cyclophyllidea: Hymenolepididae) and its rodent hosts.MethodsMulti‐locus phylogenetic reconstruction and biogeographic ancestral range estimation.ResultsArostrilepis lineages crossed Beringia eastward into North America a minimum of four times and westward into Asia twice in association with temporally disjunct geographic expansions of three major tribes of cricetid rodents (Arvicolini, Myodini, Lemmini). Inferences of ancestral host associations support at least nine instances of host colonization involving shifts from one rodent tribe or family to another. Several previously unrecognized lineages of Arostrilepis are revealed.Main conclusionsConsistent with expectations of the Stockholm Paradigm, episodes of intercontinental dispersal were both frequent in the history of Arostrilepis and preceded a majority of inferred host‐colonization events. Events of historical geographic expansion created numerous opportunities for development of novel host–parasite associations through ecological fitting, as parasites tracked historically conserved resources available across diverse host taxa. Beringia played a major role in shaping rodent/parasite assemblages by mediating dispersal between the northern continents during glacial episodes of the Pleistocene, rather than by serving as a zone of refugial isolation.