Reproductive compensation and selection among viable embryos drive the evolution of polyembryony

Abstract

Simple polyembryony – where a single gametophyte produces multiple embryos with different sires but the same maternal haplotype – is common in conifers, ferns, horsetails and other vascular plants. Polyembryony could be favored as a mechanism of reproductive compensation, providing a backup for inviable embryos, or as a mechanism of embryo competition and eliminating plants with low fitness, perhaps acting as a mechanism of Self-Incompatibility (SI). However as the evolution of polyembryony from monoembryony has not been modeled these long standing verbal models have not been evaluated. We develop an infinite-site, forward population genetics model to test how these factors can favor the evolution of polyembryony, and how these underlying benefits of polyembryony shape the genetic load under a range of selfing rates, dominance, and selection coefficients. We find that the benefit of reproductive compensation strongly favors the evolution of polyembryony, while the benefits of embryo competition are much weaker. Importantly, when embryo competition favors the evolution of polyembryony it increases embryo competitiveness, but does not act as an SI mechanism, as it does not effectively trade low-fitness selfed offspring for high fitness outcrossed offspring. We find that the impact of polyembryony on the genetic load depends on its function – increasing the embryo load when acting as a mechanism of embryo compensation and decreasing the embryo load when acting as a mechanism of competition.

Early acting inbreeding depression can evolve as an inbreeding avoidance mechanism

“…For simplicity, we model reproductive compensation by providing each seed with a single backup - such that if the first ‘primary’ seed is inviable, it can be replaced by another, which may or may not be viable. This roughly follows the case of polyembryony in pines which we modeled previously (25), with the distinction that in this model maternal half-sibs do not necessarily inherit the same maternal allele. For tractability, we further assume that inbreeding depression is expressed after seed development (such that initially all embryos live to become full seeds), and that this inbreeding depression is both unpurgeable (i.e.…”

“…Such a scenario is likely found in polyembryonic gymnosperms which lack a self-incompatibility mechanism, cannot avoid geitonogamous selfing, and display high inbreeding depression (30). In fact, a recent study of the evolution of polyembryony (25) found a subtle shift towards an excess of common alleles that decrease embryonic fitness when there is reproductive compensation and embryos do not compete. Taken together, these two studies suggest that (i) reproductive compensation is initially favored as a mechanism to make up for inviable embryos (25), and (ii) the opportunity for reproductive compensation can further favor early inviability of inbred embryos.…”

“…Such a scenario is likely found in polyembryonic gymnosperms which lack a self-incompatibility mechanism, cannot avoid geitonogamous selfing, and display high inbreeding depression (30). In fact, a recent study of the evolution of polyembryony (25) found a subtle shift towards an excess of common alleles that decrease embryonic fitness when there is reproductive compensation and embryos do not compete.…”

“…After introducing the plausibility of this argument, we show that, depending on the mutation rate, ongoing evolution of this early-acting “altrusitic” adaptive load will lead to patterns of variation that are difficult to distinguish from standard models of mutation selection balance. This second result potentially explains why no signal of this load was observed in a recent study of the evolution of polyembryony and its consequences (25). As such, while self-sacrifice may favor an elevated genetic load, Occam’s razor argues for a null interpretation of early embryonic death as a simple consequence of standard mutation selection balance, rather than a panglossian (26) interpretation of embryonic death as an altruistic act.…”

Some sexual consequences of being a plant

“…Where female gametophytes with many archegonia have access to sperm from multiple individuals, as in ferns receiving sperm from numerous neighbours or in gymnosperms receiving numerous pollen grains, multiple embryos may form with identical maternal haploid genotypes, but different sires. As only one sporophyte usually survives, the sperm genotypes compete (as diploids) in an identical maternal background [22]. In bryophytes, the possibility of female choice has recently been raised and that the male genotype may influence the amount of nutrients a female allocates to a particular sporophyte [6].…”