A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host–parasite systems

Aim  To integrate ecological fitting, the oscillation hypothesis and the taxon pulse hypothesis into a coherent null model for the evolution of complex host–parasite associations.
Location  Global.
Methods  This paper reviews and synthesizes literature that focuses on phylogenetic analyses and reciprocal mapping of a model system of hosts and their parasites to determine patterns of host–parasite associations and geographical distributions through time.
Results  Host-switching and geographical dispersal of parasites are common phenomena, occurring on many temporal and spatial scales. Diversification involving both co-evolution and colonization explains complex host–parasite associations. Across the expanse of Earth history, the major radiations in host–parasite assemblages have been preceded by ecological disruption, ecological breakdown and host-switching in a context that can be defined by the concept of ecological fitting. This cyclical process sets the stage for co-diversification during periods of relative stability, punctuated by host-switching during episodes of regional to global environmental disruption and climatological change.
Main conclusions  Most observed host–parasite associations can be explained by an historical interaction between ecological fitting, oscillation (episodes of increasing host range alternating with isolation on particular hosts) and taxon pulses (cyclical episodes of expansion and isolation in geographical range). Major episodes of environmental change appear to be the main drivers for both the persistence and diversification of host–parasite systems, creating opportunities for host-switching during periods of geographical expansion and allowing for co-evolution and co-speciation during periods of geographical isolation.