Cascading speciation among mutualists and antagonists in a tree-beetle-fungi interaction

• Published in: Proceedings of the Royal Society. B, Biological sciences Vol. 285; no. 1881; p. 20180694
• Main Authors: Bracewell, R R, Vanderpool, D, Good, J M, Six, D L
• Format: Journal Article
• Language: English
• Published: England The Royal Society Publishing 27.06.2018; The Royal Society
• Edition: Royal Society (Great Britain)
• Subjects: Animals; Antagonists; Basidiomycota - genetics; Basidiomycota - physiology; Canada; Coevolution; Dendroctonus brevicomis; Divergence; Ecological effects; Evolution; Fungi; Genetic Speciation; Genome, Fungal; Genome, Insect; Genomes; Geographical isolation; Ophiostomatales - genetics; Ophiostomatales - physiology; Pine trees; Pinus - genetics; Pinus - microbiology; Pinus - physiology; Pinus ponderosa; Reproductive isolation; Speciation; Species; Symbionts; Symbiosis; Trees; Trophic levels; United States; Weevils - genetics; Weevils - microbiology; Weevils - physiology; Canada; United States; diversification; ectosymbiosis; coevolution; symbiosis; mutualism
• ISSN: 0962-8452; 1471-2954
• DOI: 10.1098/rspb.2018.0694

Cascading speciation is predicted to occur when multiple interacting species diverge in parallel as a result of divergence in one species promoting adaptive differentiation in other species. However, there are few examples where ecological interactions among taxa have been shown to result in speciation that cascades across multiple trophic levels. Here, we test for cascading speciation occurring among the western pine beetle ( ), its primary host tree ( ), and the beetle's fungal mutualists ( and sp. B). We assembled genomes for the beetle and a fungal symbiont and then generated reduced representation genomic data (RADseq) from range-wide samples of these three interacting species. Combined with published data for the host tree, we present clear evidence that the tree, the beetle, and the fungal symbionts are all genetically structured into at least two distinct groups that have strongly codiverged with geographical isolation. We then combine our genomic results with diverse population and laboratory-based data to show evidence for reproductive isolation at each level of the cascade and for coevolution of both antagonistic and mutualistic species interactions within this complex network.