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

Aim: We 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, is 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. Location:
Beringia and adjacent temperate to arctic biomes in North America and
Eurasia. Taxon: Arostrilepis (Cyclophyllidea: Hymenolepididae) and its
rodent hosts. Methods: Multi-locus phylogenetic reconstruction and
biogeographic ancestral range estimation. Results: Arostrilepis 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 conclusions: Consistent 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.