Abstract

A long-standing hypothesis in evolutionary biology is that polyploid plants have a fitness advantage over diploids in climatically variable or extreme habitats. Here we provide the first empirical evidence that polyploid advantage in these environments is caused by two distinct processes: homeostatic maintenance of reproductive output under elevated abiotic stress, and fixed differences in seed development. In an outdoor climate manipulation experiment using coastal to inland Australian populations of the perennial grass Themeda triandra Forssk., we found that total output of viable seed in drought- and heat-stressed tetraploid plants was over four times higher than in diploids, despite being equal under more favourable growing conditions. Tetraploids also consistently produced heavier seeds with longer hygroscopic awns, traits which increase propagule fitness in extreme environments. These differences add to fitness benefits associated with broader-scale local adaptation of inland T. triandra populations to drought stress. Our study provides evidence that nucleotypic effects of genome size and increased reproductive flexibility can jointly underlie polyploid advantage in plants in stressful environments, and argue that ploidy can be an important criterion for selecting plant populations for use in genetic rescue, restoration and revegetation projects, including in habitats affected by climate change.

Highlights

  • As a driver of reproductive isolation, phenotypic diversity and speciation, polyploidy has had an unparalleled role in generating2017 The Authors

  • Tetraploids from all source regions were more fit than diploids, either across all climate treatments, or only in heat or drought stress treatments

  • Our study provides the first empirical evidence that polyploid advantage in plants in such habitats involves two independent processes: (i) homeostatic maintenance of reproductive output under increasing abiotic stress and (ii) fixed differences in seed size and morphology that increase propagule fitness and mobility

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Summary

Introduction

As a driver of reproductive isolation, phenotypic diversity and speciation, polyploidy has had an unparalleled role in generating2017 The Authors. Changes in gene copy number may increase biochemical flexibility and promote homeostasis in stressful environments by enabling spatial and temporal partitioning of gene expression among homeologues [3,11] or, in the case of autopolyploids, via maintenance of allelic diversity across loci on homologous chromosomes [12]. Genetic consequences such as the occurrence of transgressive phenotypes [6], chromosomal rearrangements, the masking of deleterious alleles and changes to DNA methylation [13] may contribute to polyploid advantage in extreme habitats [2]. These can occur rapidly in allopolyploids, and may become important in autopolyploids over time [2]

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