Polyploidy. Part 5: Patterns of Autopolyploidy

switchgrass, Panicum virgatum, famous autopolyploid

Polyploidy is whole genome duplication, uncommon in animals, but common in plant evolution, between living plant species and in individuals within plant species. (See previous blogs link). Although it is actually a continuum, botanists recognize allopolyploidy, when the genomes that duplicated come from two different species and autopolyploidy when a single genome doubles. This post is about autopolyploids.

When two species cross and the hybrid doubles its chromosomes, usually a new species forms and it is pretty easy to detect. (For example blanketflowers: Gaillardia pulchella crossed with Gaillardia aristata, each diploid with 24 chromosomes, underwent polyploidy to create the bigger Gaillardia x grandiflora, tetraploid with 48 chromosomes). Autopolyploids are harder to spot. Since they doubled the same chromsomes, they do not look particularly distinctive. It is hard work to figure out that a plant is polyploid, let alone where those chromosomes originated. (See figure 1 in Heslop-Harrison et al. to see how allopolyploids are detected link) Detection has gotten easier with DNA markers, but it still requires gathering and processing a number of plants.  As a result, nobody knows how many species are autopolyploid. 

buffalograss, Bouteloua/Buchloe dactyloides, autopolyploid

Autopolyploid variation often occurs within species and within local populations. Different individuals have different numbers of chromosomes. For example, fireweed (Chamerion angustifolium) has populations which contain individuals with 36 chromosomes, diploids, some triploids with 54 chromosomes and some with 72 chromosomes, tetraploids. This kind of variation occurs in a surprising number of species. Dozens of important North American grasses include individuals of different ploidy levels, for example big bluestem (Andropogon gerardi), switchgrass (Panicum virgatum), blue grama (Bouteloua gracilis) and buffalograss (Buchloe dactyloides). Other species known to have within-population polyploid variation include quaking aspen (Populus tremuloides), species of sagebrush (Artemisia), yarrow (Achillea species), spring beauty (Claytonia ) and many more. Plants all over the world, temperate and tropical, monocots and dicots, herbs, shrubs and trees...

Autopolyploidy confers many genetic changes. Higher polyploids are usually bigger and grow more slowly. All kinds of complex effects follow from having four copies of each gene not just two. So botanists expect different polyploids within a species to differ in their adaptations. They look especially to see if different ploidy levels grow in different habitats. 

fireweed, Chamerion

Several studies have shown some spatial separation between autopolyploids of the same species. Fireweed diploids with 36 chromosomes are generally found at higher elevations than fireweed tetraploids with 72 chromosomes. Yarrow (Achillea borealis) tetraploids (36 chromosomes) and hexaploids (54 chromosomes) are found in different soils and plant communities, the tetraploids in the milder climates along the Pacific Coast, hexaploids in drier locations. In buffalograss, tetraploids (40 chromosomes) dominate populations in the north and west of the species' range and hexaploids (60 chromosomes) dominate in the south and west. And there are other cases, going back decades to the earliest studies. Higher polyploids, which have to have been produced from lower polyploids, are thought to be better adapted to harsh or novel environments.

We have only a handful of studies of the distribution of autopolyploids within a species. Many of the polyploid species are very widespread, so characterizing the distribution of autopolyploid types across their range is a very large project. (See the maps in Hadle et al.'s study of buffalograss, link)

I think we are a long way from a generalization about the benefits of autopolyploidy within a species and within populations. There are too many autopolyploids out there and too few botanists studying them. 

Autopolyploidy makes all kinds of changes to cells, and plants generally. If you compare a diploid to a autotetraploid in the same population, the tetraploid will be different not only in cell size and ratios in the nucleus and between organelle, but in the regulation and dosage of hundreds of genes, because it has four copies not two of both the structural genes and the regulatory genes. And with four copies, the rules of inheritance are different. Researchers are actively trying to understand what we can say that becoming polyploid usually does. 

yarrow, Achillea

Here are viable, different explanations for what benefit autopolyploidy confers:

First, individual plants that are higher autopolyploids can have different tolerances than the lower polyploids they are derived from, especially be more tolerant of drought or other stresses. As noted above, various studies have show geographic- or habitat- based separation of the ploidy levels within a species.

A second possibility is that autopolyploidy is adaptive, but what it adapts the species to depends on the genes that doubled and the particular environment, so patterns of adaptation will be case-specific. (No easy generalizations). 

A third possible explanation is that autopolyploidy adds to genetic variation in the species and that is adaptive in itself. Thus autopolyploid populations with several polyploids present are better able to respond to a changing environment than any population of only one ploidy level. The diversity enhances recombinations so some of the progeny will be very fit and help the species survive and prosper as conditions change. Not any particular gene, but variation itself is the key.

A fourth possible explanation is that autopolyploidy is just an irreversible genetic error. A major mutation. So the chromosomes fail to separate and the seedling carries twice the genome. This explanation requires no benefit to polyploidy, but so long as there is no particular disadvantage, the new autopolyploid may live, reproduce, and pass on autopolyploidy to its offspring. If this genetic error is common, we will often detect autopolyploids. 

Finally, all of those can be true for some autopolyploid species. 

big bluestem, Andropogon gerardi in a recently burned part of Konza Prairie, Manhattan Kansas
both common polyploids are well represented among the plants in the photo 
(old slide, color a bit too blue)

My own experience with autopolyploidy, in the dominant prairie grass big bluestem, had all the above elements. The higher polyploids were slightly bigger, with bigger cells. They tended to be in the west of the range of big bluestem (which was across all the U.S. east of the Rocky Mountains). The higher polyploids produce very little viable seed, especially in comparison with the the lower polyploids. You can put this together as western conditions favor the higher polyploids. But you can also tell it as the higher polyploids are not very fit and will die out. Which means you can also look at the whole continent and see two ploidy levels in some places and by themselves other places and conclude that polyploidy is unimportant to big bluestem. Two research groups have worked on polyploidy in big bluestem since I retired. They have added lots of new information but you can still marshal the existing data to support quite different conclusions. 

There is lots more to be learned about polyploidy in plants.

Comments and corrections welcome.

Previous blogs on polyploidy

Polyploidy, Multiple Copies of the Genome. Part . Basics. link

Polyploidy 2. And Crop Plants link

Polyploidy Part 3. Patterns in Nature: Speciation. link

Polyploidy 4. Distribution of Autopolyploidy link

References

Doyle, J. J. and J. E. Coate. 2020. Autopolyploidy: an epigenetic mutation. American Journal of Botany. 107:  1097-1100.

Hadle, J. J., P. L. Russell and J. B. Beck. 2019. Are buffalograss (Buchloe dactyloides) cytotypes spatially and ecologically differentiated? American Journal of Botany. 106: 1116-1125. link Accessed 7/6/24,

Heslop-Harrison, J.S. P., T. Schwarzacher and Q. Liu. 2023. Polyploidy: its consequences and enabling role in plant diversification and evolution. Annals of Botany. 131: 1-9. link  Accessed 7/6/24.

Husband, B. C. and D. W. Schemske. 1998. Cytotype distribution at a diploid–tetraploid contact zone in Chamerion (Epilobium) angustifolium (Onagraceae). American Journal of Botany. 85:1688-1694.

McArthur, E. D. and S. C. Sanderson. 1999. Cytogeography and chromosome evolution of subgenus Tridentatae of Artemisia (Asteraceae) link Accessed 7/3/24.

McIntyre, P. J. 2012. Cytogeography and genome size variation in the Claytonia perfoliata (Portulacaceae) polyploid complex. Annals of Botany. 110: 1195-1203.

Parisod, C., R. Holderegger, and C. Brochmann. 2010. Evolutionary consequences of autopolyploidy. New Phytologist. 186: 5-17.

Ramsay, J. and D. Futuyma. 2011. Polyploidy and ecological adaptation in wild yarrow. PNAS (Proceedings of the National Academy of Sciences, U.S.A.) 108: 7096-7101.

Time marches on note: Andropogon gerardi is now the correct spelling of big bluestem's scientific name because of an obscure naming rule that allows Gerard in "Gerard's andropogon" to be possessive with one i not two.

Kathy Keeler

A Wandering Botanist

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