Data from: Fitness consequences of occasional outcrossing in a functionally asexual plant (Oenothera biennis)

Many clonal organisms occasionally outcross, but the long-term consequences of such infrequent events are often unknown. During five years, representing three to five plant generations, we followed 16 experimental field populations of the forb, Oenothera biennis, originally planted with the same 18 original genotypes. Oenothera biennis usually self-fertilizes, which due to its genetic system (Permanent Translocation Heterozygosity), results in seeds that are clones of the maternal plant. However, rare outcrossing produces genetically novel offspring (but without recombination or increased heterozygosity). We sought to understand whether novel genotypes produced through natural outcrossing had greater fecundity or different multigenerational dynamics compared to our original genotypes. We further assessed whether any differences in fitness or abundances through time between original and novel genotypes were exaggerated in the presence versus absence of insect herbivores. Over the course of the experiment, we genotyped >12,500 plants using microsatellite DNA markers to identify and track the frequency of specific genotypes and estimated fecundity on a subset (>3000) of plants. The effective outcrossing rate was 7.3% in the first year and ultimately 50% of the plants were of outcrossed origin by the final year of the experiment. Lifetime fruit production per plant was on average 32% higher across all novel genotypes produced via outcrossing compared to the original genotypes, and this fecundity advantage was significantly enhanced in populations lacking herbivores. Among 43 novel genotypes that were abundant enough to phenotype with replication, plants produced nearly 30% more fruits than the average of their specific two parental genotypes, and marginally more fruits (8%) than their most fecund parent. Mean per capita fecundity of novel genotypes predicted their relative frequencies at the end of the experiment. Novel genotypes increased more dramatically in herbivore-present compared to suppressed populations (45% vs. 27% of all plants), countering the increased competition from dandelions (Taraxacum officinale) that resulted from herbivore suppression. Increased interspecific competition likely also lead to the lower realized fitness of novel versus original genotypes in herbivore-suppressed populations. These results demonstrate that rare outcrossing and the generation of novel genotypes can create high-fecundity progeny, with the biotic environment influencing the dynamical outcome of such advantages.

多数无性繁殖生物会偶尔发生异交，但这类罕见事件带来的长期后果往往尚不明确。本研究针对阔叶草本植物月见草（Oenothera biennis）的16个实验田间种群开展了为期5年的跟踪观测，涵盖3至5个植物世代，所有初始种群均由18种原始基因型定植。月见草通常进行自花授粉，由于其独特的遗传系统——永久易位杂合性（Permanent Translocation Heterozygosity），其结出的种子实为母株的克隆体。但罕见的异交事件则会产生遗传上全新的后代（不过不会发生重组，也不会提升杂合性）。本研究旨在探究：通过自然异交产生的全新基因型，相较于原始基因型，是否具备更强的繁殖力，或是呈现出不同的多世代种群动态。我们进一步评估了：在有无昆虫植食者的两种情境下，原始基因型与全新基因型之间随时间变化的适合度和种群丰度差异是否会被放大。实验期间，我们借助微卫星DNA标记（microsatellite DNA markers）对超过12500株植株进行基因分型，以识别并追踪特定基因型的种群频率；同时对其中超过3000株的亚样本开展繁殖力评估。实验首年的有效异交率为7.3%，至实验末期，异交起源的植株占比最终达到50%。所有异交产生的全新基因型植株的终身结实量，平均较原始基因型高出32%；且在无植食者的种群中，这种繁殖力优势表现得更为显著。在43种丰度足够开展重复表型观测的全新基因型中，其植株结实量较其两个亲本基因型的平均水平高出近30%，相较于繁殖力最强的亲本，也略微高出8%。全新基因型的单位个体平均繁殖力，可预测其在实验末期的相对种群频率。相较于植食者被抑制的种群，有植食者存在的种群中，全新基因型的占比增长更为迅猛（分别为总植株的45%与27%），这抵消了因植食者抑制而加剧的蒲公英（Taraxacum officinale）种间竞争压力。种间竞争的加剧，或许也是植食者抑制种群中，全新基因型相较于原始基因型实际适合度更低的原因。本研究结果表明，罕见的异交事件与全新基因型的产生，可培育出高繁殖力的后代；而生物环境会对这类优势带来的种群动态结果产生调控作用。