The effect of sheltered load on reproduction in Solanum carolinense, a species with variable self-incompatibility

Abstract

In previous studies, we have investigated the strength of self-incompatibility (SI) in Solanum carolinense, a highly successful weed with a fully functional SI system that inhabits early successional and other disturbed habitats. We have found that the SI response in S. carolinense is a plastic trait-its strength being affected by the age of the flowers, and the presence of developing fruits and that there are genetic differences among families in their self-fertility. However, in species with a fully functional SI response, selfing would not be that common. As a result, deleterious recessives scattered though the genome of horsenettle are only occasionally exposed to selection. It has been suggested that deleterious recessives accumulate near S-alleles in strong SI species because the S-locus is located in a non-recombining region of the genome and because strong S-alleles are never in the homozygous state, thus sheltering some of the genetic load near the S-locus from selection. We performed a series of laboratory and greenhouse experiments to determine the extent to which sheltered load adds to the overall magnitude of inbreeding depression in horsenettle. Specifically, we amplified and sequenced the S-alleles from 16 genets collected from a large population in Pennsylvania and performed a series of controlled self-pollinations. We then grew the selfed progeny in the greenhouse; recorded various measures of growth and reproductive output; and amplified and sequenced their S-allele(s). We found that the heterozygous progeny of self-pollinations produce more flowers and have a greater ability to set both self and cross seed than S-homozygous progeny. We also found evidence of variation in the magnitude of load among S-alleles. These results suggest that sheltered load might slow the fixation of weak (partially compatible) S-alleles in this population, thus adding to the maintenance of a mixed mating system rather than leading to the fixation of the selfing alleles.

The Sheltered Genetic Load Linked to the S Locus in Plants: New Insights From Theoretical and Empirical Approaches in Sporophytic Self-Incompatibility

“…Furthermore, we showed segregation bias against S15 in offspring from both self and incompatible crosses (Table 1). Our study in SSI corroborates with the results obtained in GSI in S. carolinense (i) by Stone (2004), who found a sheltered load associated to two alleles at the S locus, and (ii) by Mena-Ali et al (2009), who showed some variations in the strength of the sheltered load carried by different S alleles.…”

“…Other stages that have a great importance for the fitness of the progeny like number of flowers and male and female fertility could also be affected by the effect of the sheltered load and require further study. Mena-Ali et al (2009) indeed showed that sheltered load may have an effect on the number of flowers and on the seed set in S. carolinense, a species with GSI.…”

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

“…Overall, our results add to the growing body of evidence that alleles at a locus under balancing selection can build up a deleterious load (Stone, 2004;Llaurens et al, 2009b;Mena-Ali et al, 2009), as predicted by theory (Uyenoyama, 2005;van Oosterhout, 2009). As all studies so far, we found evidence for such a load for some, but not all alleles.…”

“…In addition, S-locus homozygotes were underrepresented in the viable progeny. A similar study in the same species found the opposite-that S-locus homozygotes were over-represented in selfed progeny-but revealed that homozygotes had reduced fitness in terms of growth (Mena-Ali et al, 2009). Both studies suggested that different S-alleles were associated with a different genetic load, depending on the evolutionary time for mutations to accumulate, or due to different purging histories.…”

“…The few studies that have been performed so far, both in Solanum carolinense (Solanaceae), indeed found differences between S-haplotypes in the amount of genetic load (Stone, 2004;Mena-Ali et al, 2009). Stochastic differences due to the random nature of the mutation process have been suggested as an explanation for this pattern (Stone, 2004).…”