Empirical evidence of fixed and homeostatic patterns of polyploid advantage in a keystone grass exposed to drought and heat stress

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: homeostati...

Full description

Bibliographic Details
Main Authors: Robert C. Godfree, David J. Marshall, Andrew G. Young, Cathy H. Miller, Sarah Mathews
Format: Article
Language:English
Published: The Royal Society 2017-01-01
Series:Royal Society Open Science
Subjects:
Online Access:https://royalsocietypublishing.org/doi/pdf/10.1098/rsos.170934
_version_ 1818329696347095040
author Robert C. Godfree
David J. Marshall
Andrew G. Young
Cathy H. Miller
Sarah Mathews
author_facet Robert C. Godfree
David J. Marshall
Andrew G. Young
Cathy H. Miller
Sarah Mathews
author_sort Robert C. Godfree
collection DOAJ
description 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.
first_indexed 2024-12-13T12:52:10Z
format Article
id doaj.art-7d1d4c3e3d634fbda9162155be5a49d3
institution Directory Open Access Journal
issn 2054-5703
language English
last_indexed 2024-12-13T12:52:10Z
publishDate 2017-01-01
publisher The Royal Society
record_format Article
series Royal Society Open Science
spelling doaj.art-7d1d4c3e3d634fbda9162155be5a49d32022-12-21T23:45:17ZengThe Royal SocietyRoyal Society Open Science2054-57032017-01-0141110.1098/rsos.170934170934Empirical evidence of fixed and homeostatic patterns of polyploid advantage in a keystone grass exposed to drought and heat stressRobert C. GodfreeDavid J. MarshallAndrew G. YoungCathy H. MillerSarah MathewsA 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.https://royalsocietypublishing.org/doi/pdf/10.1098/rsos.170934polyploidyfitnessrestorationextreme eventhomeostasisclimate adaptation
spellingShingle Robert C. Godfree
David J. Marshall
Andrew G. Young
Cathy H. Miller
Sarah Mathews
Empirical evidence of fixed and homeostatic patterns of polyploid advantage in a keystone grass exposed to drought and heat stress
Royal Society Open Science
polyploidy
fitness
restoration
extreme event
homeostasis
climate adaptation
title Empirical evidence of fixed and homeostatic patterns of polyploid advantage in a keystone grass exposed to drought and heat stress
title_full Empirical evidence of fixed and homeostatic patterns of polyploid advantage in a keystone grass exposed to drought and heat stress
title_fullStr Empirical evidence of fixed and homeostatic patterns of polyploid advantage in a keystone grass exposed to drought and heat stress
title_full_unstemmed Empirical evidence of fixed and homeostatic patterns of polyploid advantage in a keystone grass exposed to drought and heat stress
title_short Empirical evidence of fixed and homeostatic patterns of polyploid advantage in a keystone grass exposed to drought and heat stress
title_sort empirical evidence of fixed and homeostatic patterns of polyploid advantage in a keystone grass exposed to drought and heat stress
topic polyploidy
fitness
restoration
extreme event
homeostasis
climate adaptation
url https://royalsocietypublishing.org/doi/pdf/10.1098/rsos.170934
work_keys_str_mv AT robertcgodfree empiricalevidenceoffixedandhomeostaticpatternsofpolyploidadvantageinakeystonegrassexposedtodroughtandheatstress
AT davidjmarshall empiricalevidenceoffixedandhomeostaticpatternsofpolyploidadvantageinakeystonegrassexposedtodroughtandheatstress
AT andrewgyoung empiricalevidenceoffixedandhomeostaticpatternsofpolyploidadvantageinakeystonegrassexposedtodroughtandheatstress
AT cathyhmiller empiricalevidenceoffixedandhomeostaticpatternsofpolyploidadvantageinakeystonegrassexposedtodroughtandheatstress
AT sarahmathews empiricalevidenceoffixedandhomeostaticpatternsofpolyploidadvantageinakeystonegrassexposedtodroughtandheatstress