A new biological species in the Mercurialis annua polyploid complex

In eastern Spain (and many other places if you look) you can find Mercurialis annua, a plant with a complicated sex life. A new paper by Wen-Juan Ma and colleagues examine two polyploid species that formed after Mercurialis annua hybridised, duplicated its genome, and became polyploid.

The paper, A new biological species in the Mercurialis annua polyploid complex: functional divergence in inflorescence morphology and hybrid sterility, examines two hexaploid populations. Hexaploid means that instead of having one pair of chromosomes, like a diploid plant, it has three pairs.

When genomes duplicate, it’s not like the genome has been photocopied. Interactions get complicated. Dr Wen-Juan Ma, a post-doc working with Prof. John Pannell, explained that this does not mean that polyploids of the same plant should always be able to interbreed. “It depends on many factors, one of them is ploidy level. Recent polyploids with the same ploidy level may interbreed, regardless of their evolutionary origin, but the first hybrid generation (F1) might be viable but not fertile (which depends on divergence of the progenitor species to form each polyploid species).”

“It is not entirely true that Mercurialis annua can interbreed. M. annua with various ploidy levels might be able to cross; the hybrids are viable but largely sterile (see the paper by Russell and Pannell 2015). So for any new polyploids descended from them might be able to cross, but the hybrid offspring are likely to be sterile.”

Dr Ma’s and colleagues found that there were good reasons to examine Mercurialis annua‘s offspring closely. “Mercurialis annua is an ideal system to test our ideas because within this species complex, we have variation in flower inflorescences, sexual systems, ploidy level variation, now we can test reproductive isolation for individuals with the same ploidy level but with distinctive male inflorescence, also with possible different evolutionary origins.”

Images of three different sexual phenotypes of hexaploid M. annua
Images of three different sexual phenotypes of hexaploid M. annua: (a) a male individual, showing flowers on peduncles; (b) a P– monoecious individual, with male and female flowers held in leaf axils; and (c) a P+ monoecious individual, with flowers held on erect inflorescence stalks, or ‘peduncles’. Photos: Xinji Li.

The differences in the male flower are striking with the P+ species holding their flowers on stalks or penducles. In contrast, the P- species have sub-sessile flowers, meaning they sit directly on the stem. Dr Ma said: “For wind-pollinated plants, the male flower inflorescence structure is important for the success of pollen dispersal. For example, the newly discovered polyploid species P+, with male flowers on erect peduncles rather than in the sub-sessile axillary inflorescence that are more typical of hexaploidy M. annua like P-, it has shown P+ significantly increases the pollen dispersal and enjoys much greater siring success (see results from Santos del Blanco et al. 2019).”

You might wonder if the P+ form is so much better at dispersing its pollen, how can the P- form persist? Dr Ma said: “We asked the same question in our paper. Given the superiority in both pollen production and dispersal ability of the P+ over the P– hexaploid hermaphrodites, we might expect that, over time, the P+ phenotype will eventually displace the P– phenotype as a result of pollen swamping similar to that experienced by the P– lineage when it encounters dioecious diploid M. annua (Buggs and Pannell 2006).

Being swamped by pollen from the opposite morphology is bad news for a plant. While the two plants can exchange pollen, it doesn’t produce long term results. “The genetic differences between P+ and P- species might be larger than or equally same as the phenotypic differences, the hybrid individuals between P+ and P- are viable (the biomass is even larger than both P+ and P- parental species), but they are largely sterile, such as they hardly produce seeds and pollen do not seem to fertilize female flowers very well.”

The key to the isolation between the species appears to be the process that created them in the first place. Dr Ma said: “When a plant becomes polyploid, within a few generations, the polyploid species may go through accelerated rate of genome reorganization and other mutational processes that follow hybridization and genome duplication.

“It is not straightforward to characterize such processes in long-established polyploid species, but analysis of the immediate descendants of synthetic polyploids has revealed that they can be dramatic. For instance, Song et al. (1995) observed changes in restriction fragment patterns in each of the first few generations after synthesizing polyploids from several Brassica species, attributing these changes to chromosomal re-arrangements, point mutations, gene conversion and DNA methylation.

Dr Ma sees this a step that could take researchers down many paths while studying polyploidization and the evolution of sexual systems. “Many further directions can be taken, for example, using a large number of genome-wide markers and further sampling, we could establish with more confidence the evolutionary paths that led to the origin of the two hexaploidy lineages, we could distinguish between incomplete lineage sorting and genome introgression; We should reinvestigate the taxonomy and systematics of the genus Mercurialis.”

Dr Ma concluded: “This paper is relevant to people working on speciation, polyploidization, hybridization, evolution of plant sexual system and evolution of plant reproduction. Our research shows that the distinct evolutionary histories of two hexaploid lineages of M. annua have contributed to the remarkable reproductive diversity of the species complex. It seems likely that reproductive interference between them will eventually lead to the displacement of one lineage by the other via pollen swamping. So, while polyploidization can contribute to speciation, diversification might also be compromised by reproductive interference.”

Further reading

Buggs, R. J. A., & Pannell, J. R. (2006). Rapid Displacement of a Monoecious Plant Lineage Is Due to Pollen Swamping by a Dioecious Relative. Current Biology, 16(10), 996–1000. https://doi.org/10.1016/j.cub.2006.03.093

Ma, W.-J., Santos del Blanco, L., & Pannell, J. R. (2019). A new biological species in the Mercurialis annua polyploid complex: functional divergence in inflorescence morphology and hybrid sterility. Annals of Botany. https://doi.org/10.1093/aob/mcz058

Russell, J. R. W., & Pannell, J. R. (2014). Sex determination in dioecious Mercurialis annua and its close diploid and polyploid relatives. Heredity, 114(3), 262–271. https://doi.org/10.1038/hdy.2014.95

Santos del Blanco, L., Tudor, E., & Pannell, J. R. (2019). Low siring success of females with an acquired male function illustrates the legacy of sexual dimorphism in constraining the breakdown of dioecy. Ecology Letters, 22(3), 486–497. https://doi.org/10.1111/ele.13207

Song, K., Lu, P., Tang, K., & Osborn, T. C. (1995). Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proceedings of the National Academy of Sciences, 92(17), 7719–7723. https://doi.org/10.1073/pnas.92.17.7719