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

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.

Genome duplication effects on functional traits and fitness are genetic context and species dependent: studies of synthetic polyploid Fragaria

“…For the Special Issue: Plant-Environment Interactions: Integrating Across Levels and Scales Genome duplication effects on functional traits and fitness are genetic context and species dependent: studies of synthetic polyploid Fragaria Na Wei 1,4 , Zhaokui Du 2 , Aaron Liston 3 , and Tia-Lynn Ashman 1,4 one third of extant angiosperms (Wood et al, 2009), and globally widespread along the latitudinal gradient with an increased frequency from the tropics (~30%) to the poles (~50%) (Rice et al, 2019). While the potential adaptive mechanisms of polyploid prevalence in plant evolution and ecology have long been discussed (Levin, 1983;Ramsey and Ramsey, 2014;Soltis et al, 2016;Van de Peer et al, 2017), only recently have investigators begun to experimentally evaluate the hypotheses for polyploid advantage and disentangle underlying mechanisms in ecologically relevant contexts (e.g., Maherali et al, 2009;Ramsey, 2011;Chao et al, 2013;Godfree et al, 2017;Wei et al, 2019a). Polyploid biogeography (Rice et al, 2019) points to the association between polyploid prevalence and environmental stress (Van De Peer et al, 2017).…”

“…Polyploid biogeography (Rice et al, 2019) points to the association between polyploid prevalence and environmental stress (Van De Peer et al, 2017). Not only can polyploidy improve stress tolerance (e.g., to drought, salinity, or temperature extremes; Maherali et al, 2009;Zhang et al, 2010;Liu et al, 2011;Chao et al, 2013;Yang et al, 2014), but polyploids can have a fitness advantage over diploids across a broad range of environments, from stressful to favorable conditions (e.g., Hahn et al, 2012;Godfree et al, 2017;Wei et al, 2019a), highlighting the potential of polyploid advantage under a changing environment where stresses that have not previously been encountered are possible. Such ecological advantage of polyploid plants in the wild has been attributed to divergence in functional traits and stronger positive effects of trait plasticity relative to diploids (Wei et al, 2019a).…”

“…Polyploid plants are common, accounting for approximately one third of extant angiosperms (Wood et al., ), and globally widespread along the latitudinal gradient with an increased frequency from the tropics (~30%) to the poles (~50%) (Rice et al., ). While the potential adaptive mechanisms of polyploid prevalence in plant evolution and ecology have long been discussed (Levin, ; Ramsey and Ramsey, ; Soltis et al., ; Van de Peer et al., ), only recently have investigators begun to experimentally evaluate the hypotheses for polyploid advantage and disentangle underlying mechanisms in ecologically relevant contexts (e.g., Maherali et al., ; Ramsey, ; Chao et al., ; Godfree et al., ; Wei et al., 2019a).…”

Polyploidy promotes species diversification of Allium through ecological shifts

“…Habitat shifts are thought to be an important factor for driving polyploid evolution. This idea is founded on studies using simulated data (Rodriguez, 1996;Marchant et al, 2016) and on empirical observations (Godfree et al, 2017), both for deep time (Estep et al, 2014;Cai et al, 2019) and more recent time (Abbott & Lowe, 2004;Chao et al, 2013). Modelling studies have shown that niche separation or intermediate states between polyploidy and diploidy can counteract MCE-related interference (Levin, 1975;Parisod & Broennimann, 2016) and promote polyploid expansion (Rodriguez, 1996;Marchant et al, 2016).…”

“…Modelling studies have shown that niche separation or intermediate states between polyploidy and diploidy can counteract MCE-related interference (Levin, 1975;Parisod & Broennimann, 2016) and promote polyploid expansion (Rodriguez, 1996;Marchant et al, 2016). Moreover, robust transformative effects of polyploids make them more responsive to stress (Chao et al, 2013;Godfree et al, 2017;Certner et al, 2019), which consequently improves their survival and long-term persistence. Therefore, habitat shifts may contribute to polyploid speciation through ecological radiations.…”