Taxonomy & Evolution

Temporal patterns of Brassicaceae diversification

Huang et al. propose that whole genome duplication events serve as a constant pump for continuous and high species diversification.

Periodically, plants can undergo a Whole Genome Duplication (WGD). This is when the entire genome is copied. In humans, we have a pair of chromosomes in our genome, making us diploid. A diploid plant that undergoes a whole genome duplication becomes tetraploid because it has four chromosomes. Other plants can be hexaploid or even, in the case of some strawberries, octoploid. Anything above one pair of chromosomes is considered polyploid. When these duplication events occur, odd things can happen in a plant, and it can suddenly become much better suited to a niche. But what is the relationship between WGD events and evolution?

Xiao-Chen Huang and colleagues have been looking at mesopolyploidization events in the Brassicaceae. Meso- in the sense of a few million years ago rather than recent (Neo-) or extremely ancient (Palaeo-). In particular, they have been looking at rate shifts in the family. These are the rate of extinction, the rate of speciation and the net rate of both. If this speed of speciation changes, then there has been a ‘rate shift’ and this is what Huang and colleagues investigated.

The Brassicaceae is a familiar family, as a few of the species have been domesticated. This is the family that has turnips, cabbages and mustards in it, but Professor Marcus Koch, of Heidelberg University, and co-author of the paper, explained that there’s a lot more to the Brassicaceae. “The Brassicaceae are known for their occurrence in harsh environments (salt, alpine, arctic, heavy metals, etc.), and various lineages show very high speciation rates, which makes them a great study system to analyse such kinds of evolutionary processes. Furthermore, the family has more than 4000 species, which simply provides the statistical power for any analysis.”

“The Brassicaceae is also known for its many polyploid species and it is was long thought that polyploidization per se might be a driver of subsequent evolutionary diversification and subsequent speciation, Whole Genome Duplication can provide the genetic basis for exploring new environments and developing new traits and characters under changing selection regimes. Yet, to the contrary, there has been some debate that polyploids might be also seen as evolutionary “dead ends”.

“We have shown that in Brassicaceae both factors, past polyploidization and rate shifts (e.g. triggered by environmental change) are not necessarily linked; and both contribute to high speciation rates in Brassicaceae.”

The way they did this was by sequencing the DNA of plastids in the Brassicaceae to elaborate on an evolutionary backbone. The plastids are organelles like chloroplasts or chromoplasts that contain pigments in a cell. They have their own DNA, and so are independent of the polyploidization events in the cell nucleus, but can still provide their own measure of evolutionary time. This revealed that the Brassicaceae started diverging around thirty million years ago, with many of the tribes diverging in the following milliions of years in the Miocene. This backbone has been used to anchor individual phylogenies based on a nuclear encoded DNA sequence data comprising nearly 2000 out of the 4000 species from the Brassicaceae family.

BAMM analyses on tribes in Brassicaceae. Full details in Huang et al. 2020.

While the species underwent whole genome duplications during this period, the authors also found that rate shifts could occur without these duplications. I asked Professor Koch if it was a surprise to see whole genome duplications not driving the rate shifts. “Yes and no: A genome duplication has many severe impacts on the entire genetic system. And also from an evolutionary point of view the genome has to be stabilized (diploidization process), to diversify subsequently. But if this process has been successful, then this system might be positioned to diversify better under new environmental conditions.”

“However, also changing environmental conditions may trigger increased speciation (without preceding genome duplication). And, therefore both process are independent from each other – but we may hypothesize that there are additive effects.”

The Miocene was an epoch that lead to a cooling of the planet, before the Pliocene when there were a series of Ice Ages. These environment shifts had an effect on the species in the Brassicaceae. Can past climate change be used to predict the future? Probably not according to Professor Koch. “The time scales we considered span millions of years. Current (and very fast) climate change is severely influencing extinction rate (in combination with increased nitrogen, landscape changes, etc.), but environmental change most likely may not increase speciation rate accordingly. This means that the net speciation rate will rapidly decrease. However, we cannot measure this process “in real time”, simply because new species evolve over thousands to tens of thousands of years. This is why it is so important and meaningful to reconstruct the past.”

The authors write that they made three key findings in their research:

“(1) Significant rate shifts are seen in 12 out of 52 tribes across Brassicaceae, which are decoupled from mesopolyploid WGDs. Shifts that were detected within tribes were randomly distributed over the time span, indicating no single epoch contributing to a major burst in Brassicaceae diversification. However, the Pliocene–Pleistocene is playing a major role for present-day Brassicaceae diversity and highlights that diversification of Brassicaceae is generally favoured by cooler and drier conditions. Pleistocene glacial/deglaciation cycles may have contributed to the maintenance of the high diversification rate in Brassicaceae.
(2) The combined effect of older crown age and faster net diversification rate is sufficient to explain the high species richness across Brassicaceae tribes.
(3) Brassicaceae species have approx. 43.3 % neopolyploids, suggesting WGD as a constant driving force for species diversification. With the passage of time, neopolyploids turn into mesopolyploids and are the source for future diversification.“

For Professor Koch, it’s the both polyploidization and environmental response that are important factors in the evolutionary history of the Brassicaceae.“I think, among other findings, the take-home message is: ‘Polyploidization contributes continuously and significantly to species diversity over evolutionary times in Brassicaceae. It is not an evolutionary dead-end, rather than an intrinsic property of this important plant family comprising also Arabidopsis and numerous crop plants such as the Brassicas.’”

Update: 6 March 2020 An earlier version muddied the relationship between plastid DNA and nuclear DNA.