Exogenous selection rather than cytonuclear incompatibilities shapes asymmetrical fitness of reciprocal Arabidopsis hybrids.
Reciprocal crosses between species often display an asymmetry in the fitness of F1 hybrids. This pattern, referred to as isolation asymmetry or Darwin's corollary to Haldane's rule, is a general feature of reproductive isolation in plants, yet factors determining its magnitude and direction remain unclear. We evaluated reciprocal species crosses between two naturally hybridizing diploid species of Arabidopsis to assess the degree of isolation asymmetry at different postmating life stages. We found that pollen from Arabidopsis arenosa will usually fertilize ovules from Arabidopsis lyrata; the reverse receptivity being less complete. Maternal A. lyrata parents set more F1 hybrid seed, but germinate at lower frequency, reversing the asymmetry. As predicted by theory, A. lyrata (the maternal parent with lower seed viability in crosses) exhibited accelerated chloroplast evolution, indicating that cytonuclear incompatibilities may play a role in reproductive isolation. However, this direction of asymmetrical reproductive isolation is not replicated in natural suture zones, where delayed hybrid breakdown of fertility at later developmental stages, or later-acting selection against A. arenosa maternal hybrids (unrelated to hybrid fertility, e.g., substrate adaptation) may be responsible for an excess of A. lyrata maternal hybrids. Exogenous selection rather than cytonuclear incompatibilities thus shapes the asymmetrical postmating isolation in nature.
Centre for Organismal Studies, Department of Biodiversity and Plant Systematics, University of Heidelberg D-69120, Heidelberg, Germany.
Graham
G
Muir
Centre for Organismal Studies, Department of Biodiversity and Plant Systematics, University of Heidelberg D-69120, Heidelberg, Germany.
Paola
P
Ruiz-Duarte
Centre for Organismal Studies, Department of Biodiversity and Plant Systematics, University of Heidelberg D-69120, Heidelberg, Germany.
Nora
N
Hohmann
Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow Glasgow, G12 8QQ, U.K.
Barbara K
BK
Mable
Gregor Mendel Institute, Austrian Academy of Sciences Vienna, Austria.
Polina
P
Novikova
Centre for Organismal Studies, Department of Biodiversity and Plant Systematics, University of Heidelberg D-69120, Heidelberg, Germany.
Roswitha
R
Schmickl
Institute of Integrative Biology, ETH Zürich 8092, Zürich, Switzerland.
Alessia
A
Guggisberg
Centre for Organismal Studies, Department of Biodiversity and Plant Systematics, University of Heidelberg D-69120, Heidelberg, Germany.
Marcus A
MA
Koch
Asymmetric reproductive isolation; Darwin's corollary to Haldane's rule; cytonuclear incompatibilities; hybrid inviability; postzygotic selection