Reconstructing Origins of Loss of Self-Incompatibility and Selfing in North American Arabidopsis Lyrata: A Population Genetic Context

Abstract

Theoretical and empirical comparisons of molecular diversity in selfing and outcrossing plants have primarily focused on long-term consequences of differences in mating system (between species). However, improving our understanding of the causes of mating system evolution requires ecological and genetic studies of the early stages of mating system transition. Here, we examine nuclear and chloroplast DNA sequences and microsatellite variation in a large sample of populations of Arabidopsis lyrata from the Great Lakes region of Eastern North American that show intra-and interpopulation variation in the degree of self-incompatibility and realized outcrossing rates. Populations show strong geographic clustering irrespective of mating system, suggesting that selfing either evolved multiple times or has spread to multiple genetic backgrounds. Diversity is reduced in selfing populations, but not to the extent of the severe loss of variation expected if selfing evolved due to selection for reproductive assurance in connection with strong founder events. The spread of self-compatibility in this region may have been favored as colonization bottlenecks following glaciation or migration from Europe reduced standing levels of inbreeding depression. However, our results do not suggest a single transition to selfing in this system, as has been suggested for some other species in the Brassicaceae.Arabidopsis, bottlenecks, breakdown of self-incompatibility, demography, effective population size, inbreeding depression, mating system evolution, population genetics.

The demography and population genomics of evolutionary transitions to self-fertilization in plants

“…a weakening of dichogamy appears to be the critical first step causing increased selfing [25], whereas in Eichhornia paniculata the loss of herkogamy through stamen elongation, governed by recessive modifiers of large effect, is of primary importance [26]. In North American populations of Arabidopsis lyrata, the breakdown of selfincompatibility system is associated with increased selfing rates [27], but this physiological change does not appear to be associated with obvious morphological modifications to flowers causing autonomous self-pollination. In Capsella rubella, flower size reduction appears to have followed the loss of self-incompatibility [28].…”

Inbreeding depression in self-incompatible North-American Arabidopsis lyrata: disentangling genomic and S-locus-specific genetic load

“…Given the potential purging history in PB3 (F1 progeny derived from a cross between the outcrossing PIN and selfing RON population), this may seem surprising. The RON population has been predominantly inbreeding for at least several generations, with low outcrossing rates (T m ¼ 0.29 in 2003 and T m ¼ 0.28 in 2007), and characteristically low genetic diversity and heterozygosity Foxe et al, 2010). Alternatively, heterotic effects in the F1 cross-progeny used as control could explain upward bias of the estimate of inbreeding depression in PB3, although PIN and RON are geographically and genetically similar based on analyses of microsatellites, nuclear DNA SNPs and chloroplast DNA Foxe et al, 2010).…”

“…The RON population has been predominantly inbreeding for at least several generations, with low outcrossing rates (T m ¼ 0.29 in 2003 and T m ¼ 0.28 in 2007), and characteristically low genetic diversity and heterozygosity Foxe et al, 2010). Alternatively, heterotic effects in the F1 cross-progeny used as control could explain upward bias of the estimate of inbreeding depression in PB3, although PIN and RON are geographically and genetically similar based on analyses of microsatellites, nuclear DNA SNPs and chloroplast DNA Foxe et al, 2010). Estimation of inbreeding depression in relation to outcrossing rates in multiple populations, ideally using within-population crosses as control would provide better insights into the potential role of purging throughout the North-American populations of A. lyrata.…”

“…Seeds originated from two North-American populations of A. lyrata that have been described previously Mable and Adam, 2007;Foxe et al, 2010): Pinery Provincial Park on Lake Huron (PIN: outcrossing (T m ¼ 0.84), with self-incompatible individuals predominating) and Rondeau Provincial Park on Lake Erie (RON: inbreeding (T m ¼ 0.28), with self-compatible individuals predominating). Reciprocal crosses were performed between three independent pairs of plants of which the S-locus genotype had been at least partly determined previously (see supporting information for details).…”

“…As F1 seeds retained for estimating o outcrossed in PB3 resulted from a cross between parents from different populations (inbreeding RON and outcrossing PIN), there is a potential issue of heterosis inflating the o outcrossed estimate, causing overestimation of overall genomic inbreeding depression. Therefore, although we chose two genetically similar populations (Foxe et al, 2010) our estimate of genomic inbreeding depression should be interpreted with care for PB3. However, the estimation of S-linked genetic load (see next paragraph) is not affected by these complications, as it was assessed within selfed families.…”