What causes mating system shifts in plants? Arabidopsis lyrata as a case study

Mable, B.K. , Hagmann, J., Kim, S.-T., Adam, A., Kilbride, E., Weigel, D. and Stift, M. (2017) What causes mating system shifts in plants? Arabidopsis lyrata as a case study. Heredity, 118(1), pp. 52-63. (doi: 10.1038/hdy.2016.99) (PMID:27925617) (PMCID:PMC5176115)

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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.

Item Type:Articles
Additional Information:Updated online 7 December 2016: This article was originally published under a standard licence, but has now been made available under a CC BY 4.0 licence. The PDF and HTML versions of the paper have been modified accordingly. A corrigendum has also been published.
Glasgow Author(s) Enlighten ID:Adam, Ms Aileen and Stift, Mr Marc and Kilbride, Mrs Elizabeth and Mable, Professor Barbara
Authors: Mable, B.K., Hagmann, J., Kim, S.-T., Adam, A., Kilbride, E., Weigel, D., and Stift, M.
College/School:College of Medical Veterinary and Life Sciences > School of Biodiversity, One Health & Veterinary Medicine
Journal Name:Heredity
Publisher:Nature Publishing Group
ISSN (Online):1365-2540
Published Online:02 November 2016
Copyright Holders:Copyright © 2016 BK Mable et al
First Published:First published in Heredity 118(1):52-63
Publisher Policy:Reproduced under a creative commons license

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
374091Genomes, pathogens and mate choice - implications for the evolution and maintenance of genetic diversityBarbara MableNatural Environment Research Council (NERC)NE/B50094X/1RI BIODIVERSITY ANIMAL HEALTH & COMPMED
426221Mating systems and genetic diversity in Arabidopsis lyrataBarbara MableNatural Environment Research Council (NERC)NE/D013461/1RI BIODIVERSITY ANIMAL HEALTH & COMPMED