Mixed mating populations have higher fitness than outcrossing populations for tens to hundreds of generations following colonization, suggesting a consistent early advantage to mixed mating populations in responding to selection . The magnitude of this fitness advantage each generation is slight, but it has biologically important consequences for colonization success by decreasing the time to local adaptation and thus reducing the risk of extinction relative to obligate outcrossing. Alternatively, the rapid erosion of genetic variation in obligately self-fertilizing populations inhibits the response to selection . When the sink habitat exerts strong selection, obligate self-fertilization results in a longer timescale for adaptation and faster extinction than mixed mating . These general patterns are observed for a range of sink habitat severity and genetic architectures .In addition to effects on genetic variance, inbreeding due to mating system plasticity can increase the frequency or expression of deleterious alleles. The overall fitness effects of inbreeding may be best understood by examining inbreeding depression and genetic load together, since the former clarifies fitness differences between outcrossed and self-fertilized progeny within a population, 30 litre plant pots whereas the latter encompasses the mean fitness effects of deleterious alleles for a population with a given breeding system. The consequences of mating system plasticity for inbreeding depression and genetic load depends on the mutation class considered.
Following colonization of the sink environment, individuals produced by self fertilization exhibit both greater variance for the quantitative trait under selection and increased expression of segregating recessive deleterious alleles. Patterns of inbreeding depression reflect the balance of these two effects. In the absence of recessive deleterious mutations, inbreeding depression in sink populations is initially negative following colonization, indicating that progeny produced by self fertilization have on average higher fitness in the sink habitat than progeny produced by random outcrossing . As populations become locally adapted, inbreeding depression slowly evolves towards slightly positive values for all self fertilization rates. This pattern reflects the role of fitness variation under stabilizing selection: greater fitness variance in self-fertilized progeny is beneficial in maladapted populations, but becomes costly as populations approach a fitness peak . Weakly deleterious codominant alleles do not contribute to inbreeding depression, since their expression is not dependent on mating system, and patterns reflect those observed in the absence of deleterious mutations . Incorporating recessive deleterious mutations alters the initial effects of self fertilization as well as the final magnitude of inbreeding depression. Strongly deleterious recessive alleles drive a pulse of inbreeding depression following colonization that decreases with time and greater self-fertilization rates . This pulse reflects the increased expression of segregating recessive alleles in self fertilized individuals, and decreases through time by purging.
Purging occurs more rapidly with greater self-fertilization, as recessive alleles are exposed to selection. Similarly, the evolution of genetic load also depends on the dominance and selection coefficients of deleterious mutations. Immediately following colonization, mating system plasticity has little effect on the genetic load due to codominant alleles . In contrast, the colonization bottleneck causes a spike in the genetic load due to recessive alleles that increases with greater self-fertilization . Over time, alleles under weak purifying selection become fixed by drift, slowly increasing the genetic load, whereas strongly deleterious alleles are rapidly purged. Genetic load changes most long term under obligate self-fertilization, whereas mixed mating populations maintain similar genetic load as obligate outcrossing populations. This effect is greatest for weakly deleterious alleles, which in turn contribute to a slight increase in the time to adaptation and an increased risk of extinction for all self-fertilization rates. These qualitative patterns are observed for a range of N . For high frequencies of strongly deleteriousrecessive mutations, the pulse of inbreeding depression and genetic load induced by mating system plasticity can outweigh the benefits of increased genetic variance, increasing the risk of extinction relative to obligate outcrossing .Pollen dispersal from the source population inhibits niche evolution by increasing the time to adaptation and decreasing local adaptation in obligately outcrossing sink populations . Self-fertilization reduces the opportunity for gene flow by decreasing the proportion of ovules that can be fertilized by immigrant gametes. For even limited pollen dispersal, mixed mating increases local adaptation and reduces the time to local adaptation relative to obligate outcrossing by acting as a partial reproductive barrier while maintaining high genetic variation and adaptive potential. When the potential for gene flow is high , the benefits of obligate self-fertilization as a reproductive barrier outweigh its costs in terms of reduced adaptive potential, and any self-fertilization rate increases local adaptation relative to obligate outcrossing.
Interestingly, pollen flow does not affect the extinction rate . This is because extinction is most likely within the first 10 generations following colonization , when populations are highly maladapted and pollen flow is just as likely to increase as decrease local fitness. The overall fitness of sink populations depends on the interaction between pollen dispersal, mutation class, and self-fertilization rate. In general, consideration of deleterious mutations decreases fitness in sink populations via genetic load relative to simulations in which fitness is determined solely by a quantitative trait. However, this fitness decrease is small relative to the effects of pollen dispersal from source populations . In the absence of pollen dispersal, obligately self fertilizing populations exhibit lower fitness than populations with at least some outcrossing . When the potential for gene flow is high , the fitness benefit of reproductive isolation exceeds the costs of decreased selection efficiency in obligately self fertilizing populations . These general patterns are observed for all mutation classes.Niche evolution requires that colonizing populations persist in the sink environment. In general, extinction risk increases with ecological or genetic factors that act to reduce sink population fitness, including strong selection and deleterious mutations . Incorporating pollen limitation greatly increases the risk of extinction in obligately outcrossing sink populations , but does not affect the timing or degree of local adaptation for populations that persist . Thus, pollen limitation inhibits niche evolution demographically by preventing population persistence. Even moderate pollen limitation can result in high extinction risk when the sink habitat imposes strong selection . In these cases, increased self-fertilization due to mating system plasticity decreases the risk of extinction by providing reproductive assurance. When pollen limitation and habitat severity are moderate , even limited self-fertilization or obligate self-fertilization can greatly decrease the risk of extinction relative to obligately outcrossing populations . Similar patterns are observed when self-fertilization is delayed .A plastic shift to mixed mating promotes niche evolution under a broad range of ecological conditions. Mixed mating allows populations to respond more rapidly to selection, reduces the risk of extinction, and has little effect on the accumulation of genetic load. Alternatively, a shift to obligate self-fertilization may inhibit niche evolution by slowing the response to selection, increasing the risk of extinction, and allowing the fixation of deleterious alleles. However, even obligate self-fertilization provides important reproductive assurance and isolation benefits. The interactions between mating system plasticity and pollen limitation, selection, 25 liter pot plastic and gene flow determine its overall consequences for niche evolution, and are discussed in greater detail below. Extinction risk and reproductive assurance Even moderate pollen limitation can greatly increase the extinction risk of colonizing populations, particularly when coupled with strong selection in a novel environment. Pollen limitation is common among angiosperms, occurring in some form in 62-63% of species examined . Estimates of the magnitude of pollen limitation are subject to various methodological and publication biases , but several meta-analyses have found that fruit or seed setreductions may range from 15-75% on average . Interestingly, pollen limitation and strong selection interact during colonization to greatly increase the risk of extinction and potential importance of reproductive assurance. Given this interaction, mixed mating can promote colonization of harsh environments even when the magnitude of pollen limitation is relatively low . Previous work has emphasized the importance of immigration in allowing sink population persistence ; here, we demonstrate a similar demographic rescue effect caused by self-fertilization. The relative benefits of immigration vs. self-fertilization for population persistence will depend on the fitness of immigrant genotypes and the strength of inbreeding depression.
Although inbreeding depression decreases rapidly following colonization, selection against immigrant genotypes remains high. Thus, we find strong support for the hypothesis that self-fertilization, particularly mixed mating, will promote persistence in novel environments through reproductive assurance. A general role for self-fertilization in range expansion is supported empirically. Baker’s Law emphasizes an association between self-compatibility and colonization success , and is widely supported in native , invasive and several island floras . Further, pollen limitation and self-fertilization are associated with the colonization of human-disturbed environments . Previous theoretical work has examined the role of reproductive assurance during colonization in a meta population framework, with mixed support for Baker’s Law . However, our model represents the first attempt to integrate pollen limitation and niche evolution during colonization of a novel selective environment. Our results suggest that at least partial self-fertilization may be critical for the persistence of colonizing populations under a broad set of ecological scenarios.Pollen dispersal from source populations decreases fitness in sink populations by introducing maladaptive alleles and reducing local adaptation. The potential for gene flow to swamp local adaptation is well supported empirically , and self-fertilization is an important reproductive barrier in a variety of systems . Here, we show that mixed mating increases fitness in colonizing populations when gamete dispersal is moderate . Even obligate self-fertilization, which reduces fitness by limiting adaptive potential and accumulating deleterious mutations, increases fitness relative to outcrossing when gamete dispersal is high . Interestingly, these values may not be uncommon in systems with mobile gametes, such as plants or marine invertebrates. Estimates of pollen flow between plant populations range between 8-17% in Raphanus sativus and 8% in Phlox drummondii . Sperm dispersal in marine invertebrates is highly variable, with estimates from 0% as close as 8 m to 20% as far as 100 m . Sessile organisms may frequently experience distinct selective environments well within the spatial scale of gamete dispersal. In such cases, self fertilization can provide an important reproductive barrier to allow local adaptation.In the absence of pollen limitation or gene flow, mating system plasticity can have immediate effects on the adaptive potential of colonizing sink populations. A shift from outcrossing to mixed mating confers a temporary increase in genetic variation that can accelerate adaptation and reduce the risk of extinction when adaptation is limited by low genetic variance. Although the effects of mixed mating on genetic variance and response to selection are small and transient, they occur during a critical stage in colonization and have biologically important consequences for the persistence of small populations. Obligate self-fertilization, however, limits adaptive potential by rapidly eroding genetic variation and increasing the timescale of adaptation. These effects only occur in colonizing populations if the response to selection is limited relative to the demographic risk of extinction, such as when heritability in the trait under selection is low. There is some evidence that heritability in wild populations is reduced under unfavorable conditions , and adaptation to novel environments may further be limited by negative genetic correlations under multivariate selection . The effect of mating system on genetic variance and the response to selection is consistent with predictions from deterministic models. Lande found that inbreeding temporarily increases the rate of recovery of genetic variation after abottleneck, but that this is quickly eroded to levels below random mating when inbreeding is high . Glémin and Ronfort found a similar pattern for the time to adaptation when selection favors a partially recessive allele at a single locus. Dominance or epistatic interactions may further increase the effect of self-fertilization on genetic variance , relative to our model, which only considers selection on an additive trait. In an artificial selection experiment in Mimulus, Holeski and Kelly found that inbreeding increased the genetic variance of traits under selection. Further, when mating system had a significant positive effect on the response to selection, it was greatest for mixed mating and reduced for complete self-fertilization. Here, we show that a plastic shift to mixed mating may enhance adaptive potential in maladapted populations when selection acts on an additive, polygenic trait.