How does a plant give up on love?

Self-pollination or selfing, a mating system where a flower fertilizes itself, is not uncommon. Yet, the evolutionary history and dynamics behind this intriguing process largely remain unknown. This puzzle forms the heart of the research conducted by Han and colleagues, published in the ‘Annals of Botany’. Their study focused on the wild shrub, Daphne kiusiana, endemic to East Asia. It offers insights into the fascinating journey from outcrossing, where a plant is fertilized by another, to self-fertilization. The research deciphers the subtle genetic and morphological changes that have been quietly unfolding for over 100,000 years.

Han’s team discovered that the plants in the eastern region of the Daphne kiusiana distribution, which includes southeastern Korea and Kyushu, Japan, exhibit fewer and smaller flowers compared to their counterparts in the western region (southwestern Korea). This decrease in visibility, coupled with the increased rate of selfing and higher levels of homozygosity—genetic similarity within an individual—are characteristics of what is known as the ‘selfing syndrome.’ This is a shift in the mating system that has been closely observed in the evolution of many flowering plants.

What makes this study interesting is that Han and colleagues are studying this shift in two closely related populations of plants. In a commentary on the paper, Zhang and colleagues say:

…[S]tudies of the selfing syndrome have so far rarely focused on intraspecific groups of populations (subspecies, varieties, etc.) with opposite mating systems, variable selfing rates and/or floral traits. Indeed, intraspecific variants should be particularly suitable for studying this phenomenon, as they probably represent instances of recent divergence, making it more feasible to infer the population demographic and/or (palaeo-)environmental (e.g. climatic) conditions under which shifts in mating system might have occurred. 

Zhang et al. 2023

Han’s team used a series of advanced genetic analyses to unravel this story. They employed nuclear microsatellites—repetitive DNA sequences used to measure genetic diversity—and chloroplast DNA, for a multiplexed phylogenetic marker sequencing. These techniques allowed them to trace the independent phylogeographical histories of the two lineages, and identify the traits associated with each.

The results unveiled that the eastern lineage of Daphne kiusiana showed a gradual reduction in effective population size, despite no signs of a severe bottleneck—an event leading to a significant reduction in population. This was in contrast to the western lineage, which suggested that the eastern plants had been selfing for a long period. The eastern lineage’s morphological changes, marked by smaller and fewer flowers, were associated with a high selfing rate and increased homozygosity, where both the maternal and paternal copies of a gene are the same.

The results suggest that these selfing-associated morphological changes date back at least 100,000 years, driven by directional selection for efficient self-pollination. Unlike previous assumptions, the evolution of the selfing syndrome in Daphne kiusiana is not strongly associated with a severe population bottleneck. Han and colleagues state in their paper:

Our results suggest that the selfing lineage in D. kiusiana has been largely driven by gradual directional selection towards lower levels of floral visibility and herkogamy for efficient self-pollination in response to historical environmental changes. The transition to selfing accompanied by morphological modifications may have been triggered by severe competitive interactions among/within species. Intrinsic factors of D. kiusiana, such as its life-history traits and niche in the ecological succession, may also have been important in facilitating its evolution. Thus, the selfing syndrome lineage or species may exhibit a demographic signature of a gradually reduced effective population size, as evidence of adaptation.

Han et al. 2023

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Han, E.-K., Tamaki, I., Oh, S.-H., Park, J.-S., Cho, W.-B., Jin, D.-P., Kim, B.-Y., Yang, S., Son, D.C., Choi, H.-J., Gantsetseg, A., Isagi, Y. and Lee, J.-H. (2023) “Genetic and demographic signatures accompanying the evolution of the selfing syndrome in Daphne kiusiana, an evergreen shrub,” Annals of Botany, 131(5), pp. 751–767. Available at: https://doi.org/10.1093/aob/mcac142.