The adaptive radiation of lichen-forming Teloschistaceae is associated with sunscreening pigments and a bark-to-rock substrate shift.
Adaptive radiations play key roles in the generation of biodiversity and biological novelty, and therefore understanding the factors that drive them remains one of the most important challenges of evolutionary biology. Although both intrinsic innovations and extrinsic ecological opportunities contribute to diversification bursts, few studies have looked at the synergistic effect of such factors. Here we investigate the Teloschistales (Ascomycota), a group of >1,000 lichenized species with variation in species richness and phenotypic traits that hinted at a potential adaptive radiation. We found evidence for a dramatic increase in diversification rate for one of four families within this order--Teloschistaceae--which occurred ∼ 100 Mya (Late Cretaceous) and was associated with a switch from bark to rock and from shady to sun-exposed habitats. This adaptation to sunny habitats is likely to have been enabled by a contemporaneous key novel phenotypic innovation: the production in both vegetative structure (thallus) and fruiting body (apothecia) of anthraquinones, secondary metabolites known to protect against UV light. We found that the two ecological factors (sun exposure and rock substrate) and the phenotypic innovation (anthraquinones in the thallus) were all significant when testing for state-dependent shifts in diversification rates, and together they seem likely to be responsible for the success of the Teloschistaceae, one of the largest lichen-forming fungal lineages. Our results support the idea that adaptive radiations are driven not by a single factor or key innovation, but require a serendipitous combination of both intrinsic biotic and extrinsic abiotic and ecological factors.
Department of Biology, Duke University, Durham, NC 27708-0338; Department of Comparative Plant and Fungal Biology, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, United Kingdom; e.gaya@kew.org.
Ester
E
Gaya
Department of Plant Biology (Botany Unit), Facultat de Biologia, Universitat de Barcelona, 08028 Barcelona, Spain; Department of Botany, Swedish Museum of Natural History, SE-104 05 Stockholm, Sweden;
Samantha
S
Fernández-Brime
Departamento de Biología, Universidad Metropolitana de Ciencias de la Educación, Santiago, 7760197, Chile;
Reinaldo
R
Vargas
Department of Biological and Experimental Psychology, Queen Mary University of London, London, E1 4NS, United Kingdom;
Robert F
RF
Lachlan
Australian National Herbarium, Commonwealth Scientific and Industrial Research Organisation, Canberra, ACT 2601, Australia; Department of Life Sciences, Natural History Museum, London, SW7 5BD, United Kingdom.
Cécile
C
Gueidan
Department of Biology, Duke University, Durham, NC 27708-0338;
Martín
M
Ramírez-Mejía
Department of Biology, Duke University, Durham, NC 27708-0338;
François
F
Lutzoni
D000222:Adaptation, Physiological / Q000235:genetics; D000880:Anthraquinones / Q000737:chemistry; D001203:Ascomycota / Q000502:physiology*; D044822:Biodiversity; D005075:Biological Evolution; D004463:Ecology; D017753:Ecosystem; D008011:Lichens / Q000502:physiology*; D008969:Molecular Sequence Data; D010641:Phenotype; D010802:Phylogeny; D010858:Pigmentation; D017422:Sequence Analysis, DNA; D013472:Sunlight; D014197:Trees; D014466:Ultraviolet Rays
D000880:Anthraquinones
Teloschistaceae; adaptive radiation; lichens; substrate switch; sunlight protection