Abstract
Polyploidy is a major driving force in angiosperm evolution, but our understanding of establishment and early diversification processes following allo- vs. auto-polyploidy is limited. An excellent system to address such questions is the monocot plant Prospero autumnale, as it comprises several genomically and chromosomally distinct diploid cytotypes and their auto- and allotetraploid derivatives. To infer origins and evolutionary trajectories of the tetraploids, we use genome size data, in situ hybridization with parental genomic DNAs and specific probes (satDNA, rDNAs), as well as molecular-phylogenetic analyses. Thus, we demonstrate that an astounding range of allotetraploid lineages has been formed recurrently by chromosomal re-patterning, interactions of chromosomally variable parental genomes and nested cycles of extensive hybridization, whereas autotetraploids have originated at least twice and are cytologically stable. During the recurrent formation and establishment across wide geographic areas hybridization in some populations could have inhibited lineage diversification and nascent speciation of such a hybrid swarm. However, cytotypes that became fixed in populations enhanced the potential for species diversification, possibly exploiting the extended allelic base, and fixed heterozygosity that polyploidy confers. The time required for polyploid cytotype fixation may in part reflect the lag phase reported for polyploids between their formation and species diversification.
Highlights
Polyploidy is found in the ancestry of all lineages (Van de Peer et al, 2009), and is important in the diversification and speciation of flowering plants (Wendel, 2000; Soltis et al, 2009; Weiss-Schneeweiss et al, 2013)
Chromosome numbers and karyotypes, including localization of rDNAs and satDNA PaB6 using Fluorescence in Situ Hybridization (FISH), were established for 27 tetraploids (Figures S1–S3), each one representing a different natural population (Table S1), with genome sizes available for 25 of them (Table 1). 11 individuals were analyzed by Genomic in Situ Hybridization (GISH) (Table 1, Figures 1, 2)
While distribution patterns of 5S and 35S rDNA, and of satDNA PaB6 loci in the polyploids were additive compared to the diploid progenitors (Table 1, Figures S2A,B, S3A–C, Supplementary File S1), genome size of polyploids often deviated from the expected additive value, experiencing both upsizing and downsizing (−16%; Type I B7 autotetraploids; Table 1)
Summary
Polyploidy is found in the ancestry of all lineages (Van de Peer et al, 2009), and is important in the diversification and speciation of flowering plants (Wendel, 2000; Soltis et al, 2009; Weiss-Schneeweiss et al, 2013). Evolution of Prospero Tetraploids potential differences with respect to establishment and early diversification between autopolyploids and allopolyploids requires a group of closely related, yet distinct diploid, autopolyploid and allopolyploid lineages that may or may not be recognized taxonomically. The P. autumnale complex is remarkably variable in chromosome number (dysploidy on diploid level, polyploidy, B-chromosomes: Ainsworth et al, 1983; Vaughan et al, 1997; Jang et al, 2013, 2016), chromosome structure (fusions, inversions, translocations, centric shifts, supernumerary chromosomal segments: Taylor, 1997; Jang et al, 2013), genome size (Ebert et al, 1996; Vaughan et al, 1997; Jang et al, 2013) and repetitive DNA distribution and copy number (Emadzade et al, 2014). The P. autumnale complex encompasses four diploid cytotypes with unique combinations of basic chromosome number (x = 7, 6, 5), genome size, locations of pericentric satellite DNA PaB6 and of 5S and 35S rDNA loci (Jang et al, 2013; Emadzade et al, 2014).
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