Costs of selfing prevent the spread of a self‐compatibility mutation that causes reproductive assurance

Abstract

In flowering plants, shifts from outcrossing to partial or complete self-fertilization have occurred independently thousands of times, yet the underlying adaptive processes are difficult to discern. Selfing's ability to provide reproductive assurance when pollination is uncertain is an oft-cited ecological explanation for its evolution, but this benefit may be outweighed by costs diminishing its selective advantage over outcrossing. We directly studied the fitness effects of a self-compatibility mutation that was backcrossed into a self-incompatible (SI) population of Leavenworthia alabamica, illuminating the direction and magnitude of selection on the mating-system modifier. In array experiments conducted in two years, self-compatible (SC) plants produced 17-26% more seed, but this advantage was counteracted by extensive seed discounting-the replacement of high-quality outcrossed seeds by selfed seeds. Using a simple model and simulations, we demonstrate that SC mutations with these attributes rarely spread to high frequency in natural populations, unless inbreeding depression falls below a threshold value (0.57 ≤ δ ≤ 0.70) in SI populations. A combination of heavy seed discounting and inbreeding depression likely explains why outcrossing adaptations such as self-incompatibility are maintained generally, despite persistent input of selfing mutations, and frequent limits on outcross seed production in nature.

Digest: Prudent self-denial: The advantage of incompatibility inLeavenworthia alabamica*

“…One answer is that not all self-fertilized ovules would necessarily have been left unfertilized; some might have been cross-fertilized instead. This is exactly what Layman et al (2017) find: the increased net seed production comes at an average cost of reducing cross-fertilized seed by 72 percent. Additionally, self-fertilized seeds are expected…”

“…However, if self-fertilization does detract from outcross pollen success, then this disadvantage must be subtracted to calculate the net advantage through pollen. Layman et al (2017) find that SC plants sire 55.8 percent of cross-fertilized seeds, significantly more than those sired by an approximately equal number of SI plants. Rather than sacrificing outcross pollen success to achieve self-fertilization, SC plants gain the best of both worlds.…”

“…This might occur if access to mates or pollen vectors is unreliable, which Layman et al (2017) find to be true in L. alabamica through observation of pollinators. They find that SC plants produce 17-26 percent more seeds than SI plants.…”

“…In this issue, Layman et al (2017) supply just such an empirical grounding in their study of the costs and benefits of loss-of-function mutations in Leavenworthia alabamica. Since this species has both SI and self-compatible (SC) populations, Layman et al (2017) emulating new loss-of-function mutations, they can quantify effects of self-incompatibility on factors affecting fitness such as pollination rates and outcrossing rates.…”

“…Since this species has both SI and self-compatible (SC) populations, Layman et al (2017) emulating new loss-of-function mutations, they can quantify effects of self-incompatibility on factors affecting fitness such as pollination rates and outcrossing rates.…”