Calatayud, J., Hórreo, J.L., Madrigal-González, J., Migeon, A., Rodríguez, M.Á., Magalhães, S. & Hortal, J. (2016) Geography and major host evolutionary transitions shape the resource use of plant parasites. Proceedings of the National Academy of Sciences USA, 113, 9840-9845. doi:10.1073/pnas.1608381113

Significance. Patterns of host use by parasites are commonly thought to be limited by phylogenetic constraints, yet little is known about the role of the geographic distribution of hosts and parasites in such patterns. We show that evolutionary patterns in host use by a family of plant parasites are largely determined by the geographical distribution of hosts and parasites. Such phylogenetic lability in host use results in repeated colonizations of distantly related plant lineages, even across major plant evolutionary transitions. Still, these transitions constitute significant adaptive barriers in the evolution of host use. Our results thus show that host plant use by parasitic mites hinges more on where the plant and the mite are than on phylogenetic constraints.

The evolution of resource use in herbivores has been conceptualized as an analog of the theory of island biogeography, assuming that plant species are islands separated by phylogenetic distances. Despite its usefulness, this analogy has paradoxically led to neglecting real biogeographical processes in the study of macroevolutionary patterns of herbivore–plant interactions. Here we show that host use is mostly determined by the geographical cooccurrence of hosts and parasites in spider mites (Tetranychidae), a globally distributed group of plant parasites. Strikingly, geography accounts for most of the phylogenetic signal in host use by these parasites. Beyond geography, only evolutionary transitions among major plant lineages (i.e., gymnosperms, commelinids, and eudicots) shape resource use patterns in these herbivores. Still, even these barriers have been repeatedly overcome in evolutionary time, resulting in phylogenetically diverse parasite communities feeding on similar hosts. Therefore, our results imply that patterns of apparent evolutionary conservatism may largely be a byproduct of the geographic cooccurrence of hosts and parasites.