Convergence and novelty in adaptation to whole genome duplication in three independent polyploids

Abstract

Convergent evolution is observed broadly across the web of life, but the degree of evolutionary constraint during adaptation of core intracellular processes is not known. High constraint has been assumed for conserved processes, such as cell division and DNA repair, but reports of nimble evolutionary shifts in these processes have confounded this expectation. Whole genome duplication (WGD) necessitates the concerted adjustment of a wide range of fundamental intracellular functions but nevertheless has been repeatedly survived in all kingdoms. Given this repeated adaptation to WGD despite obvious intracellular challenges to core processes such as meiosis, we asked: how do lineages not only survive WGD, but sometimes ultimately thrive? Are the solutions employed constrained or diverse? Here we detect genes and processes under selection following WGD in the Cochlearia species complex by performing a scan for selective sweeps following WGD in a large-scale survey of 73 resequenced individuals from 23 populations across Europe. We then contrast our results from two independent WGDs in Arabidopsis arenosa and Cardamine amara. We find that while WGD does require the adaptation of particular functional processes in all three cases, the specific genes recruited to respond are highly flexible. We also observe evidence of varying degrees of convergence between different cases. Our results point to a polygenic basis for the distributed adaptive systems that control meiotic crossover number, ionomic rewiring, cell cycle control, and nuclear regulation. Given the sheer number of loci under selection post-WGD, we surmise that this polygenicity may explain the general lack of convergence between these species that are ~30 million years diverged. Based on our results, we speculate that adaptive processes themselves – such as the rate of generation of structural genomic variants—may be altered by WGD in nascent autopolyploids, contributing to the occasionally spectacular adaptability of autopolyploids observed across kingdoms.

When everything changes at once: finding a new normal after genome duplication

“…Interestingly, several genes involved in maintaining K + /Na + ratios (SOS1/NHX7, HKT1) [97,[167][168][169], and other ion homeostasis regulatory channels implicated in salt and other stress responses (CCC1, KEA2, KEA3) [170,171], as well as a number of other genes that have been associated with salt tolerance, are ploidy-differentiated (and in Ar. arenosa, show additional signatures suggestive of selection) in the genome scans for adaptation to autopolyploidy published to date [26,29,30]. Links to global ion homeostasis are evident, for example, from the observation that a mutant for the trans-Golgi-network-localized NHX5 channel ( ploidydifferentiated in Ar.…”

“…arenosa [ 26 , 28 ], Ca. amara [ 30 ] and Co. officinalis [ 29 ], there is evidence that guard cell responsiveness and patterning may be under selection. Ion fluxes between guard cells and adjacent subsidiary cells, mediated by plasma membrane ion transport, are critical for guard cell turgor changes (e.g.…”

“…In this light, it is interesting that the main guard cell H + -ATPase, AHA1, shows evidence of having been modified by selection in established tetraploids of Ar. arenosa and also shows evidence of ploidy-associated differentiation in Co. officinalis [ 26 , 28 , 29 ]. Although AHA1 has diverse functions throughout the plant (e.g.…”

“…In addition, all three species show evidence of selection having targeted regulators of AHA1: in Ar. arenosa , PPI2 and in Co. officinalis , PPI1 are more differentiated between diploids and tetraploids than the genome average [ 29 , 30 ]. These proteins bind to and stimulate AHA1 [ 75 , 76 ], though their in planta functions are still largely mysterious.…”

“…These are: Arabidopsis arenosa, in which adaptation to genome duplication was studied using genome-wide outlier scans comparing natural diploids and their established autotetraploid derivatives (which have a monophyletic origin about 30 000 generations ago [25]) using several distinct metrics related to genetic diversity, differentiation and the site frequency spectrum [26][27][28]. The genomes of two additional species, Cochlearia officinalis and Cardamine amara, have also been scanned for genome-wide differentiation outliers between ploidies using several differentiation statistics [29,30].…”