The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications

Abstract

The duplication of an entire genome is no small affair. Whole genome duplication (WGD) is a dramatic mutation with long-lasting effects, yet it occurs repeatedly in all eukaryotic kingdoms. Plants are particularly rich in documented WGDs, with recent and ancient polyploidization events in all major extant lineages. However, challenges immediately following WGD, such as the maintenance of stable chromosome segregation or detrimental ecological interactions with diploid progenitors, commonly do not permit establishment of nascent polyploids. Despite these immediate issues some lineages nevertheless persist and thrive. In fact, ecological modeling commonly supports patterns of adaptive niche differentiation in polyploids, with young polyploids often invading new niches and leaving their diploid progenitors behind. In line with these observations of polyploid evolutionary success, recent work documents instant physiological consequences of WGD associated with increased dehydration stress tolerance in first-generation autotetraploids. Furthermore, population genetic theory predicts both short-and long-term benefits of polyploidy and new empirical data suggests that established polyploids may act as "sponges" accumulating adaptive allelic diversity. In addition to their increased genetic variability, introgression with other tetraploid lineages, diploid progenitors, or even other species, further increases the available pool of genetic variants to polyploids. Despite this, the evolutionary advantages of polyploidy are still questioned, and the debate over the idea of polyploidy as an evolutionary dead-end carries on. Here we broadly synthesize the newest empirical data moving this debate forward. Altogether, evidence suggests that if early barriers are overcome, WGD can offer instantaneous fitness advantages opening the way to a transformed fitness landscape by sampling a higher diversity of alleles, including some already preadapted to their local environment. This occurs in the context of intragenomic, population genomic, and physiological modifications that can, on occasion, offer an evolutionary edge. Yet in the long run, early advantages can turn into long-term hindrances, and without ecological drivers such as novel ecological niche availability or agricultural propagation, a restabilization of the genome via diploidization will begin the cycle anew.

Polyploidy promotes species diversification of Allium through ecological shifts

“…Polyploidisation is a major mechanism of speciation (Rothfels & Otto, ). A high polyploid frequency is predicted to accelerate speciation, whereas a low polyploid frequency will induce extinction at an early age as a result of MCE (Levin, ; Baduel et al ., ). Our results support this hypothesis by demonstrating a high species diversification rate for Allium lineages with high polyploid frequencies (Fig.…”

A novel allele ofASY3promotes meiotic stability in autotetraploidArabidopsis lyrata

“…In PDS5b, at the 5' end of tetraploid alleles from five A. arenosa plants we observe evidence for a GC of the first two exons to the diploid allele, providing evidence of GC (or CO) between ploidy levels (S8A Fig). In addition, analysis of genome resequencing data [25] revealed a 3' GC from a diploid ASY1 A. lyrata allele to a tetraploid A. arenosa allele in the KAG population (S8B Fig). The widespread presence of such evidence of gene conversion products in these loci exhibiting the most dramatic signatures of selection suggests a mechanism by which the peaks of differentiation generally found in this system are so narrow [3,8,25,32,33], despite a recent origin, and possible bottleneck, of the tetraploids [25].…”

Genes derived from ancient polyploidy have higher genetic diversity and are associated with domestication inBrassica rapa

“…Polyploidy often precedes domestication and crops are nearly twice as likely to be domesticated in lineages with a relatively recent WGD compared to those without 10 . Among the potential explanations for the relationship between polyploidy and domestication, the expanded genetic diversity and plasticity of polyploid plants may be especially advantageous during domestication and crop improvement [11][12][13][14][15] . Analyses in yeast have shown that polyploid lineages not only have higher genetic diversity but also adapt to new environments faster than their lower ploidal level relatives 16 .…”

“…Although nearly 30% of plant species are recent polyploids, all flowering plants are paleopolyploids with varying histories of WGD 18 . Given that the genetic consequences of polyploidy play out over time as genomes diploidize and paralogs fractionate 13,19,20 , we may expect that the effects of polyploidy extend to diploidized species. Here, we sought to test whether past polyploidy is associated with increased diversity and domestication in the crops of Brassica rapa .…”