Abstract
Whole genome duplications have occurred recurrently throughout the evolutionary history of eukaryotes. The resulting genetic and phenotypic changes can influence physiological and ecological responses to the environment; however, the impact of genome copy number on evolvability has rarely been examined experimentally. Here, we evaluate the effect of genome duplication on the ability to respond to selection for early flowering time in lines drawn from naturally occurring diploid and autotetraploid populations of the plant Chamerion angustifolium (fireweed). We contrast this with the result of four generations of selection on synthesized neoautotetraploids, whose genic variability is similar to diploids but genome copy number is similar to autotetraploids. In addition, we examine correlated responses to selection in all three groups. Diploid and both extant tetraploid and neoautotetraploid lines responded to selection with significant reductions in time to flowering. Evolvability, measured as realized heritability, was significantly lower in extant tetraploids ( = 0.31) than diploids ( = 0.40). Neotetraploids exhibited the highest evolutionary response ( = 0.55). The rapid shift in flowering time in neotetraploids was associated with an increase in phenotypic variability across generations, but not with change in genome size or phenotypic correlations among traits. Our results suggest that whole genome duplications, without hybridization, may initially alter evolutionary rate, and that the dynamic nature of neoautopolyploids may contribute to the prevalence of polyploidy throughout eukaryotes.
Highlights
The evolutionary significance of whole genome duplication, polyploidy, has been debated since it was discovered a century ago [1,2,3,4,5,6,7]
We find that polyploidy has a significant effect on the response to selection for early flowering in Chamerion angustifolium
Autotetraploid lines derived from natural populations had significantly lower realized heritabilities than those from natural diploid populations, suggesting that the potential to respond to a given selection pressure is reduced by genome duplication
Summary
The evolutionary significance of whole genome duplication, polyploidy, has been debated since it was discovered a century ago [1,2,3,4,5,6,7]. Polyploidy is associated with increased genetic diversity (reviewed by [9]) and species richness [10,11,12,13] It is still unclear whether genome duplication typically increases or decreases a species’ ability to respond to selection [14,15]. Evolvability may be diminished after genome duplication if adaptation is limited by the rate of spread of a beneficial allele (i.e. the efficiency of selection) since mutations are more likely to be masked [6,16] The magnitude of these contradictory effects will depend on population size, mutation rate, reproductive system and the level of dominance of beneficial alleles [6]. While the effects of diploidy compared to haploidy have been explored using isogenic lines of yeast [17,18,19], there have been no experimental evaluations of natural diploid and polyploid populations, nor comparisons of extant and newly formed polyploids
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