Heterostyly accelerates diversification via reduced extinction in primroses.
The exceptional species diversity of flowering plants, exceeding that of their sister group more than 250-fold, is especially evident in floral innovations, interactions with pollinators and sexual systems. Multiple theories, emphasizing flower-pollinator interactions, genetic effects of mating systems or high evolvability, predict that floral evolution profoundly affects angiosperm diversification. However, consequences for speciation and extinction dynamics remain poorly understood. Here, we investigate trajectories of species diversification focusing on heterostyly, a remarkable floral syndrome where outcrossing is enforced via cross-compatible floral morphs differing in placement of their respective sexual organs. Heterostyly evolved at least 20 times independently in angiosperms. Using Darwin's model for heterostyly, the primrose family, we show that heterostyly accelerates species diversification via decreasing extinction rates rather than increasing speciation rates, probably owing to avoidance of the negative genetic effects of selfing. However, impact of heterostyly appears to differ over short and long evolutionary time-scales: the accelerating effect of heterostyly on lineage diversification is manifest only over long evolutionary time-scales, whereas recent losses of heterostyly may prompt ephemeral bursts of speciation. Our results suggest that temporal or clade-specific conditions may ultimately determine the net effects of specific traits on patterns of species diversification.
Institute of Systematic Botany, University of Zürich, , Zollikerstrasse 107, 8008 Zürich, Switzerland, Department of Ecology and Evolutionary Biology, Brown University, , 80 Waterman Street, Box G-W, Providence, RI 02912, USA, Department of Botany and Biodiversity Research, University of Vienna, , Rennweg 14, Vienna 1030, Austria, Department of Evolution and Ecology, University of California, , Davis, 1 Shields Avenue, CA 95616, USA.
Jurriaan M
JM
de Vos
Colin E
CE
Hughes
Gerald M
GM
Schneeweiss
Brian R
BR
Moore
Elena
E
Conti
D044822:Biodiversity; D005075:Biological Evolution; D060365:Chloroplast Proteins / Q000235:genetics; D053476:Extinction, Biological; D035264:Flowers / Q000235:genetics / Q000502:physiology; D008969:Molecular Sequence Data; D010802:Phylogeny; D016133:Polymerase Chain Reaction; D029623:Primulaceae / Q000235:genetics / Q000502:physiology*; D012098:Reproduction; D017422:Sequence Analysis, DNA
D060365:Chloroplast Proteins
angiosperm evolution; heterostyly; phylogenetic methods; plant breeding system; speciation