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.

Piyal Karunarathne,Diego Hojsgaard

doi:10.3389/fgene.2021.736088

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.

Highlights

Polyploidization in plants is a recurring and pivotal evolutionary phenomenon that brings both short- and long-term benefits for plant diversification (Werth et al, 1985; Soltis et al, 2010; Symonds et al, 2010)
The occurrence of new polyploids in natural populations is unequivocally lower than expected from such values (Suda and Herben, 2013), implying that polyploidization events are not always inherently beneficial
In combination with data from species distribution modeling (Karunarathne et al, 2018), the present study sheds light on the evolutionary aspects of P. intermedium life history, suggesting that intraspecific variation is segregated within cytotypes and that recurrent formation of tetraploids allows a range expansion of polyploid cytotypes into new habitats, creating genetically divergent lineages and promoting ecologically differentiation

Summary

Introduction

Polyploidization in plants is a recurring and pivotal evolutionary phenomenon that brings both short- and long-term benefits for plant diversification (Werth et al, 1985; Soltis et al, 2010; Symonds et al, 2010). Comparative genomic studies show that approximately 15% of plant speciation events resulted from polyploidy (Wood et al, 2009) and that polyploidy is substantially associated to higher plant diversity (Symonds et al, 2010; Jiao et al, 2011). Polyploidization can either act as an instantaneous mechanism for divergence and speciation because of reproductive isolation (see Soltis et al, 2009) or as a step toward extinction due to competitive exclusion by the majority cytotype [i.e., minority cytotype disadvantage (Levin, 1975; Parisod et al, 2010)]. Mechanisms that help newly arisen polyploids to overcome competition, survive, and establish themselves devoid of reproductive isolation are key to the success of polyploids

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Discussion

Conclusion