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Geography and major host evolutionary transitions shape the resource use of plant parasites

Joaquín Calatayud, José Luis Hórreo, Jaime Madrigal-González, Alain Migeon, Miguel Á. Rodríguez, Sara Magalhães, and Joaquín Hortal
PNAS published ahead of print August 17, 2016 https://doi.org/10.1073/pnas.1608381113
Joaquín Calatayud
aDepartamento de Ciencias de la Vida, Universidad de Alcalá, 28871 Madrid, Spain;bDepartamento de Biogeografía y Cambio Global, Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones CientÍficas (CSIC), 28006 Madrid, Spain;
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  • For correspondence: j.calatayud.ortega@gmail.com
José Luis Hórreo
cInstituto Pirenaico de Ecología (CSIC), 22700 Jaca, Spain;dDepartment of Ecology and Evolution, University of Lausanne, CH1015 Lausanne, Switzerland;
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Jaime Madrigal-González
aDepartamento de Ciencias de la Vida, Universidad de Alcalá, 28871 Madrid, Spain;
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Alain Migeon
eINRA, UMR CBGP, F-34988 Montferrier-sur-Lez, France;
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Miguel Á. Rodríguez
aDepartamento de Ciencias de la Vida, Universidad de Alcalá, 28871 Madrid, Spain;
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Sara Magalhães
fCentre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisboa, Portugal
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Joaquín Hortal
bDepartamento de Biogeografía y Cambio Global, Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones CientÍficas (CSIC), 28006 Madrid, Spain;fCentre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisboa, Portugal
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  1. Edited by Douglas Futuyma, Stony Brook University, Stony Brook, NY, and approved July 5, 2016 (received for review June 3, 2016)

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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.

Abstract

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.

  • evolutionary conservatism
  • geographic signal
  • host use evolution
  • parasite–host interactions
  • spider mites

Footnotes

  • ↵1To whom correspondence should be addressed. Email: j.calatayud.ortega{at}gmail.com.
  • ↵2S.M. and J.H. contributed equally to this work.

  • Author contributions: J.C., S.M., and J.H. designed research; J.C., A.M., S.M., and J.H. performed research; J.C., J.L.H., and J.M.-G. analyzed data; and J.C., J.L.H., J.M.-G., A.M., M.Á.R., S.M., and J.H. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1608381113/-/DCSupplemental.

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Evolution of host use in plant parasite
Joaquín Calatayud, José Luis Hórreo, Jaime Madrigal-González, Alain Migeon, Miguel Á. Rodríguez, Sara Magalhães, Joaquín Hortal
Proceedings of the National Academy of Sciences Aug 2016, 201608381; DOI: 10.1073/pnas.1608381113

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Evolution of host use in plant parasite
Joaquín Calatayud, José Luis Hórreo, Jaime Madrigal-González, Alain Migeon, Miguel Á. Rodríguez, Sara Magalhães, Joaquín Hortal
Proceedings of the National Academy of Sciences Aug 2016, 201608381; DOI: 10.1073/pnas.1608381113
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