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 modelling 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 synthesise 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.
Highlights
Whole genome duplication (WGD) is a pervasive event in the evolution of eukaryotes, with an especially strong representation throughout the plant kingdom
Understanding the effect of WGD in isolation from separate yet correlated effects has only recently made major progress. While it was suggested 35 years ago that biochemical and physiological changes resulting from WGD might underlie polyploid adaptability (Levin, 1983), the best evidence of a direct link took three decades to emerge, when Chao et al, 2013) elegantly demonstrated that A. thaliana first generation autotetraploids have instantaneously enhanced salt tolerance compared to isogenic diploids
Excellent recent reviews have discussed the complex mixture of advantages and disadvantages of polyploidy, and here we aimed to extend this with the most recent evidence considered explicitly in the scope of the dynamic temporal nature of shifting costs and benefits
Summary
Whole genome duplication (WGD) is a pervasive event in the evolution of eukaryotes, with an especially strong representation throughout the plant kingdom. This stems from both direct competition between the two cytotypes (Yamauchi et al, 2004) and frequency dependent selection (Levin, 1975), which suggests most autopolyploids are likely to go extinct before establishment (Levin, 1975; Husband, 2000) Despite these challenges, WGD events have occurred repeatedly throughout the evolution of eukaryotes (Gregory and Mable, 2005; Wood et al, 2009; Wendel, 2015), leading to an abundance of established polyploid species in the wild. It has long been recognized that asexual reproduction (vegetative propagation and agamospermy) and WGD are correlated, with polyploids displaying elevated rates of asexual propagation compared to diploid relatives (Manning and Dickson, 1986; Schinkel et al, 2016; Herben et al, 2017) Such a reproductive strategy may even confer short-term benefits. Whatever the mechanism, stabilizing meiosis would seem the best solution given the advantages of sex in the long run
Sign-in/Register to view highlights & summary 
Published Version (
Free)
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call