Abstract
The shift from outcrossing to self-fertilization is among the most common evolutionary transitions in flowering plants. Until recently, however, a genome-wide view of this transition has been obscured by both a dearth of appropriate data and the lack of appropriate population genomic methods to interpret such data. Here, we present a novel population genomic analysis detailing the origin of the selfing species, Capsella rubella, which recently split from its outcrossing sister, Capsella grandiflora. Due to the recency of the split, much of the variation within C. rubella is also found within C. grandiflora. We can therefore identify genomic regions where two C. rubella individuals have inherited the same or different segments of ancestral diversity (i.e. founding haplotypes) present in C. rubella's founder(s). Based on this analysis, we show that C. rubella was founded by multiple individuals drawn from a diverse ancestral population closely related to extant C. grandiflora, that drift and selection have rapidly homogenized most of this ancestral variation since C. rubella's founding, and that little novel variation has accumulated within this time. Despite the extensive loss of ancestral variation, the approximately 25% of the genome for which two C. rubella individuals have inherited different founding haplotypes makes up roughly 90% of the genetic variation between them. To extend these findings, we develop a coalescent model that utilizes the inferred frequency of founding haplotypes and variation within founding haplotypes to estimate that C. rubella was founded by a potentially large number of individuals between 50 and 100 kya, and has subsequently experienced a twenty-fold reduction in its effective population size. As population genomic data from an increasing number of outcrossing/selfing pairs are generated, analyses like the one developed here will facilitate a fine-scaled view of the evolutionary and demographic impact of the transition to self-fertilization.
Highlights
Most flowering plants are hermaphroditic, but many have evolved elaborate mechanisms to avoid self-fertilization and the associated costs of inbreeding [1,2]
We use dense genome sequence data to identify where in the genome two individuals have inherited the same or different segments of ancestral diversity present in the founders of the selfing species, Capsella rubella to obtain a genome-wide view of this transition
This identification of founding haplotypes allows us to partition mutations into those that occurred before and after C. rubella separated from its outcrossing progenitor, C. grandiflora
Summary
Most flowering plants are hermaphroditic, but many have evolved elaborate mechanisms to avoid self-fertilization and the associated costs of inbreeding [1,2]. An estimated 15% of flowering plant species are predominantly self-fertilizing [3,4] and many of these species have evolved floral morphologies that promote this means of reproduction. This shift from outcrossing to inbreeding by self-fertilization is among the most common transitions in flowering plants [5,6], and can occur when the short-term benefits of selfing (e.g. assured fertilization [7], the ‘automatic’ transmission advantage [8], and the maintenance of locally adapted genotypes [9]) overwhelm the immediate costs of inbreeding depression [10,11]. We can distinguish two factors that can lead to low diversity in selfers: the loss of ancestral polymorphism that occurred at the transition to selfing and a long term small effective population size since the transition
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