Reproductive Compensation and Selection among Viable Embryos Drive the Evolution of Polyembryony.

AbstractSimple polyembryony, where one gametophyte produces multiple embryos with different sires but the same maternal haplotype, is common among vascular plants. We develop an infinite-sites, forward population genetics model showing that together polyembryony's two benefits-"reproductive compensation" achieved by providing a backup for inviable embryos and the opportunity to favor the fitter of surviving embryos-can favor its evolution. Our model tests how these factors can favor the evolution of polyembryony and how these underlying benefits of polyembryony shape the genetic load under a range of biological parameters. While these two benefits are difficult to disentangle in nature, we construct variant models of polyembryony that either only include or only exclude the opportunity for reproductive compensation. We find that reproductive compensation strongly favors the evolution of polyembryony and that polyembryony is favored much more weekly in its absence, suggesting that the benefit of a backup embryo is the major force favoring polyembryony. Remarkably, we find nearly identical results in cases in which mutations impact either embryonic or postembryonic fitness (no pleiotropy) and in cases in which mutations have identical effects on embryonic and postembryonic fitness (extreme pleiotropy). Finally, we find that the consequences of polyembryony depend on its function-polyembryony results in a decrease in mean embryonic fitness when acting as a mechanism of embryo compensation and ultimately increases mean embryonic fitness when we exclude this potential benefit.

Non-self recognition-based self-incompatibility can alternatively promote or prevent introgression.

Self-incompatibility alleles (S-alleles), which prevent self-fertilisation in plants, have historically been expected to benefit from negative frequency-dependent selection and invade when introduced to a new population through gene flow. However, the most taxonomically widespread form of self-incompatibility, the ribonuclease-based system ancestral to the core eudicots, functions through collaborative non-self recognition, which can affect both short-term patterns of gene flow and the long-term process of S-allele diversification. We analysed a model of S-allele evolution in two populations connected by migration, focussing on comparisons among the fates of S-alleles initially unique to each population and those shared among populations. We found that both shared and unique S-alleles from the population with more unique S-alleles were usually fitter compared with S-alleles from the population with fewer S-alleles. Resident S-alleles often became extinct and were replaced by migrant S-alleles, although this outcome could be averted by pollen limitation or biased migration. Collaborative non-self recognition will usually either result in the whole-sale replacement of S-alleles from one population with those from another or else disfavour introgression of S-alleles altogether.

Diversification or Collapse of Self-Incompatibility Haplotypes as a Rescue Process.

AbstractIn angiosperm self-incompatibility systems, pollen with an allele matching the pollen recipient at the self-incompatibility locus is rejected. Extreme allelic polymorphism is maintained by frequency-dependent selection favoring rare alleles. However, two challenges result in a chicken-or-egg problem for the spread of a new allele (a tightly linked haplotype in this case) under the widespread "collaborative non-self-recognition" mechanism. A novel pollen function mutation alone would merely grant compatibility with a nonexistent style function allele: a neutral change at best. A novel pistil function mutation alone could be fertilized only by pollen with a nonexistent pollen function allele: a deleterious change that would reduce seed set to zero. However, a pistil function mutation complementary to a previously neutral pollen mutation may spread if it restores self-incompatibility to a self-compatible intermediate. We show that novel haplotypes can also drive elimination of existing ones with fewer siring opportunities. We calculate relative probabilities of increase and collapse in haplotype number given the initial collection of incompatibility haplotypes and the population gene conversion rate. Expansion in haplotype number is possible when population gene conversion rate is large, but large contractions are likely otherwise. A Markov chain model derived from these expansion and collapse probabilities generates a stable haplotype number distribution in the realistic range of 10-40 under plausible parameters. However, smaller populations might lose many haplotypes beyond those lost by chance during bottlenecks.

The evolutionary response of mating system to heterosis.

Isolation allows populations to diverge and to fix different alleles. Deleterious alleles that reach locally high frequencies contribute to genetic load, especially in inbred or selfing populations, in which selection is relaxed. In the event of secondary contact, the recessive portion of the genetic load is masked in the hybrid offspring, producing heterosis. This advantage, only attainable through outcrossing, should favour evolution of greater outcrossing even if inbreeding depression has been purged from the contributing populations. Why, then, are selfing-to-outcrossing transitions not more common? To evaluate the evolutionary response of mating system to heterosis, we model two monomorphic populations of entirely selfing individuals, introduce a modifier allele that increases the rate of outcrossing and investigate whether the heterosis among populations is sufficient for the modifier to invade and fix. We find that the outcrossing mutation invades for many parameter choices, but it rarely fixes unless populations harbour extremely large unique fixed genetic loads. Reversions to outcrossing become more likely as the load becomes more polygenic, or when the modifier appears on a rare background, such as by dispersal of an outcrossing genotype into a selfing population. More often, the outcrossing mutation instead rises to moderate frequency, which allows recombination in hybrids to produce superior haplotypes that can spread without the mutation's further assistance. The transience of heterosis can therefore explain why secondary contact does not commonly yield selfing-to-outcrossing transitions.