Mitosis, stature and evolution of plant mating systems: low-Φ and high-Φ plants

Abstract

There is a long-recognized association in plants between small stature and selfing, and large stature and outcrossing. Inbreeding depression is central to several hypotheses for this association, but differences in the evolutionary dynamics of inbreeding depression associated with differences in stature are rarely considered. Here, we propose and test the F model of plant mating system evolution, which assumes that the per-generation mutation rate of a plant is a function of the number of mitoses (F) that occur from zygote to gamete, and predicts fundamental differences between low-F (small-statured) and high-F (largestatured) plants in the outcomes of the joint evolution of outcrossing rate and inbreeding depression. Using a large dataset of published population genetic studies of angiosperms and conifers, we compute fitted values of inbreeding depression and deleterious mutation rates for small-and large-statured plants. Consistent with our F model, we find that populations of small-statured plants exhibit a range of mating systems, significantly lower mutation rates, and intermediate inbreeding depression, while large-statured plants exhibit very high mutation rates and the maximum inbreeding depression of unity. These results indicate that (i) inbred progeny typically observed in large-statured plant populations are completely lost prior to maturity in nearly all populations; (ii) evolutionary shifts from outcrossing to selfing are generally not possible in large-statured species, rather, large-statured species are more likely to evolve mating systems that avoid selfing such as self-incompatibility and dioecy; (iii) destabilization of the mating system-high selfing rate with high-inbreeding depression-might be a common occurrence in largestatured species; and (iv) large-statured species in fragmented populations might be at higher risk of extinction than previously thought. Our results help to unify and simplify a large and diverse field of research, and serve to emphasize the importance that developmental and genetic constraints play in the evolution of plant mating systems.

Mutation–selection balance in mixed mating populations

“…Thus, selective interference becomes (proportionally) more important as s declines. Scofield and Schultz (2006) hypothesize that selective interference is responsible for the rarity of highly selfing, long-lived plants. It is thus important to determine the region of parameter space over which this process has substantial effects.…”

Frugivore loss limits recruitment of large-seeded trees

“…For both B. tarairi and C. laevigatus, movement of seeds between forest patches may prevent local extinction of small, isolated populations and contribute to gene flow among populations. Inbreeding appears to be particularly detrimental in large-statured plants (trees and shrubs), with inbred offspring almost never surviving to maturity [54], including in two New Zealand trees [55]. Consequently, fragmented tree populations may be particularly vulnerable to extinction [54], and even more dependent on their dispersers.…”

Variation of selfing rate and inbreeding depression among individuals and across generations within an admixed Cedrus population

“…In C. atlantica, sex allocation to male and female functions is highly variable and Krouchi et al (2004) have found that this variation is stable at least across several years. From an evolutionary perspective, such a tendency to dioecy in trees can be interpreted in the light of ID avoidance (Scofield and Schultz, 2006). Our selfing rate estimates might be down biased because they were computed from the number of mature seeds and not directly from the number of fertilized ovules.…”

“…ID that is caused by a small number of recessive genes that have major deleterious effects on fitness is expected to vary among individuals depending on their genotype at these few major genes and, therefore, to respond rapidly to selection. Purging is less efficient when selfed offspring do not contribute to the next generation (Scofield and Schultz, 2006), or when dominance and epistatic interactions among major genes occur (Williams et al, 2003). By contrast, ID because of many genes with small individual effects is not expected to vary drastically among individuals and is less easily purged in the population.…”

“…This diversity is maintained at the expense of a high mutation load (Ledig, 1986;Petit and Hampe, 2006;Scofield and Schultz, 2006), which can only be purged whenever inbreeding occurs. Investigating the processes that dynamically maintain the genetic load and the adaptive genetic variation within populations cannot rely only on a theory that assumes a demographic and genetic equilibrium.…”