What causes mating system shifts in plants? Arabidopsis lyrata as a case study.
The genetic breakdown of self-incompatibility (SI) and subsequent mating system shifts to inbreeding has intrigued evolutionary geneticists for decades. Most of our knowledge is derived from interspecific comparisons between inbreeding species and their outcrossing relatives, where inferences may be confounded by secondary mutations that arose after the initial loss of SI. Here, we study an intraspecific breakdown of SI and its consequences in North American Arabidopsis lyrata to test whether: (1) particular S-locus haplotypes are associated with the loss of SI and/or the shift to inbreeding; (2) a population bottleneck may have played a role in driving the transition to inbreeding; and (3) the mutation(s) underlying the loss of SI are likely to have occurred at the S-locus. Combining multiple approaches for genotyping, we found that outcrossing populations on average harbour 5 to 9 S-locus receptor kinase (SRK) alleles, but only two, S1 and S19, are shared by most inbreeding populations. Self-compatibility (SC) behaved genetically as a recessive trait, as expected from a loss-of-function mutation. Bulked segregant analysis in SC × SI F2 individuals using deep sequencing confirmed that all SC plants were S1 homozygotes but not all S1 homozygotes were SC. This was also revealed in population surveys, where only a few S1 homozygotes were SC. Together with crossing data, this suggests that there is a recessive factor that causes SC that is physically unlinked to the S-locus. Overall, our results emphasise the value of combining classical genetics with advanced sequencing approaches to resolve long outstanding questions in evolutionary biology.
Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, UK.
B K
BK
Mable
Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany.|Computomics GmbH, Tübingen, Germany.
J
J
Hagmann
Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany.|Centre for Genome Engineering, Institute for Basic Science, Daejeon, South Korea.
S-T
ST
Kim
Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, UK.
A
A
Adam
Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, UK.
E
E
Kilbride
Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany.
D
D
Weigel
Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, UK.|Department of Biology and Ecology, University of Konstanz, Konstanz, Germany.
M
M
Stift
D017360:Arabidopsis / Q000235:genetics* / Q000502:physiology; D005075:Biological Evolution; D017343:Genes, Plant; D005828:Genetics, Population; D006114:Great Lakes Region; D006239:Haplotypes; D007178:Inbreeding; D010940:Plant Proteins / Q000235:genetics*; D020641:Polymorphism, Single Nucleotide; D011494:Protein Kinases / Q000235:genetics*; D060436:Self-Incompatibility in Flowering Plants / Q000235:genetics*
D010940:Plant Proteins; D011494:Protein Kinases; C079832:S-receptor kinase