Single Independent Autopolyploidization Events From Distinct Diploid Gene Pools and Residual Sexuality Support Range Expansion of Locally Adapted Tetraploid Genotypes in a South American Grass

Abstract

Polyploidy plays a major role in plant evolution. The establishment of new polyploids is often a consequence of a single or few successful polyploidization events occurring within a species’ evolutionary trajectory. New polyploid lineages can play different roles in plant diversification and go through several evolutionary stages influenced by biotic and abiotic constraints and characterized by extensive genetic changes. The study of such changes has been crucial for understanding polyploid evolution. Here, we use the multiploid-species Paspalum intermedium to study population-level genetic and morphological variation and ecological differentiation in polyploids. Using flow cytometry, amplified fragment length polymorphism (AFLP) genetic markers, environmental variables, and morphological data, we assessed variations in ploidy, reproductive modes, and the genetic composition in 35 natural populations of P. intermedium along a latitudinal gradient in South America. Our analyses show that apomictic auto-tetraploids are of multiple independent origin. While overall genetic variation was higher in diploids, both diploids and tetraploids showed significant variation within and among populations. The spatial distribution of genetic variation provides evidence for a primary origin of the contact zone between diploids and tetraploids and further supports the hypothesis of geographic displacement between cytotypes. In addition, a strong link between the ecological differentiation of cytotypes and spatial distribution of genetic variation was observed. Overall, the results indicate that polyploidization in P. intermedium is a recurrent phenomenon associated to a shift in reproductive mode and that multiple polyploid lineages from genetically divergent diploids contributed to the successful establishment of local polyploid populations and dispersal into new environments.

Variation of Residual Sexuality Rates along Reproductive Development in Apomictic Tetraploids of Paspalum

“…This leads to noxious effects caused by the inbreeding depression [69][70][71] which likely affects the normal development of the sexual seeds and leads to a decrease in the observed proportion of these seeds. The observed values of sexual seeds in the facultative apomictic tetraploids of P. cromyorhizon and P. maculosum are similar to those previously registered in others Paspalum species, e.g., [10,13,31,43]. Although there is a decrease in the production of sexual seeds, the observed values show a wide variation reaching up to 45% of total seeds in the M1 population of P. maculosum.…”

“…However, this advantage is not enough to displace the sexual pathway at the seed stage. In facultative apomicts like observed in P. cromyorhizon and P. maculosum, the frequency of sexual and apomictic seeds may also be influenced by environmental conditions and local adaptation in apomictic populations [13]. The final output of this competition will directly shape the genetic contribution of each apomictic genotype to the gene pool of the population, which will consequently alter the allelic frequencies and genotypic diversity in the following generations.…”

“…Nonetheless, apomixis (especially apospory) is not an obligated or irreversible condition, and it can be interrupted by sexual reproduction events that originate new genetic variants in the population e.g., [2,57,88,89], as seen in natural populations of Pilosella officinarum (see [90]) and in P. cromyorhizon and some P. maculosum populations (this work). Therefore, the production of non-clonal progeny by some plants within the population buffers the reduction in genotypic (and genetic) diversity expected within populations of apomicts, which in turn allows greater adaptability under different environmental conditions [13,91,92]. In addition, as few as 5% sexual events in apomictic polyploids prevent deleterious mutations to accumulate, avoiding genomic decay and the extinction of apomictic lineages [12,93].…”

“…Most apomictic plants are facultative, maintaining the ability to reproduce sexually at different-often low-frequencies depending on the taxa, the environmental conditions, and the ploidy level, as well as the mechanism of apomictic embryo formation [7][8][9][10][11]. This residual sexuality benefits from using a very sophisticated combination of reproductive strategies, generating diversity and, concurrently, allowing the best fitted individuals to propagate clonally [8,12,13].…”

Phylogeography of Eriotheca species complex: insights into the origin and range expansion of apomictic and polyploid trees in Neotropical Savannas

“…Polyploidy and whole genome duplication (WGD) events have been recognized as major evolutionary processes in plants and have been studied and discussed for more than a century (Soltis et al ., 2014; Hörandl 2022). WGD events can cause phenotypic, physiological, reproductive, genomic, and ecological changes in polyploids when compared to their diploid ancestors (Soltis et al ., 2014, 2016; Balao et al ., 2016; Husband et al ., 2016; Karbstein et al ., 2021; Karunarathne & Hojsgaard, 2021; Ulum et al ., 2021). For the establishment and evolution of newly formed polyploids, reproductive barriers may be necessary to isolate diploids from polyploids (Husband et al ., 2016; Hörandl, 2022).…”