Early consequences of allopolyploidy alter floral evolution in Nicotiana (Solanaceae)

Elizabeth W Mccarthy,Andrew R Leitch,Amy Litt,Amelda Kurti,Sandra Knapp,Jacob B Landis,Amber J Lawhorn,Steven C Le Comber,Mark W Chase

doi:10.1186/s12870-019-1771-5

Abstract

BackgroundPolyploidy has played a major role in angiosperm evolution. Previous studies have examined polyploid phenotypes in comparison to their extant progenitors, but not in context of predicted progenitor phenotypes at allopolyploid origin. In addition, differences in the trends of polyploid versus diploid evolution have not been investigated. We use ancestral character-state reconstructions to estimate progenitor phenotype at allopolyploid origin to determine patterns of polyploid evolution leading to morphology of the extant species. We also compare trends in diploid versus allopolyploid evolution to determine if polyploidy modifies floral evolutionary patterns.ResultsPredicting the ancestral phenotype of a nascent allopolyploid from reconstructions of diploid phenotypes at the time of polyploid formation generates different phenotype predictions than when extant diploid phenotypes are used, the outcome of which can alter conclusions about polyploid evolution; however, most analyses yield the same results. Using ancestral reconstructions of diploid floral phenotypes indicate that young polyploids evolve shorter, wider corolla tubes, but older polyploids and diploids do not show any detectable evolutionary trends. Lability of the traits examined (floral shape, corolla tube length, and corolla tube width) differs across young and older polyploids and diploids. Corolla length is more evolutionarily labile in older polyploids and diploids. Polyploids do not display unique suites of floral characters based on both morphological and color traits, but some suites of characters may be evolving together and seem to have arisen multiple times within Nicotiana, perhaps due to the influence of pollinators.ConclusionsYoung polyploids display different trends in floral evolution (shorter, wider corolla tubes, which may result in more generalist pollination) than older polyploids and diploids, suggesting that patterns of divergence are impacted by the early consequences of allopolyploidy, perhaps arising from genomic shock and/or subsequent genome stabilization associated with diploidization. Convergent evolution in floral morphology and color in Nicotiana can be consistent with pollinator preferences, suggesting that pollinators may have shaped floral evolution in Nicotiana.

Highlights

Polyploidy has played a major role in angiosperm evolution
Our results show that using reconstructed progenitor phenotypes from the point of allopolyploid origin can potentially alter the interpretation of the progression of allopolyploid evolution, especially in older allopolyploids
We show that young allopolyploids display different trends in floral evolution than older allopolyploids or diploids, suggesting that the early consequences of allopolyploidy can alter floral evolution, at least in Nicotiana allopolyploids

Summary

Introduction

Polyploidy has played a major role in angiosperm evolution. Previous studies have examined polyploid phenotypes in comparison to their extant progenitors, but not in context of predicted progenitor phenotypes at allopolyploid origin. Polyploidy may increase adaptability to new environments [4], but newly established polyploids are rare and are at a disadvantage because they are much more likely to receive pollen from diploids, which may be incompatible due to the difference in ploidy [5], or may self-fertilize, leading to inbreeding depression Many crop species, such as wheat, oilseed rape, coffee, and cotton, are allopolyploid, involving both whole genome duplication and interspecific hybridization [6]. Growth in yeast and the evolution of complex traits in angiosperms may be on a different scale, they are both controlled by regulatory networks and biochemical pathways These yeast results suggest that tetraploids may be at a fitness disadvantage in the short-term, but may be more adaptable in the long-term, especially in harsh and stressful conditions [22,23,24,25]. The ability of polyploids to adapt to harsh environments has been proposed as one hypothesis for the persistence and increased diversification of polyploids after major ecological events such as the mass extinction event at the Cretaceous-Paleogene boundary [25,26,27]

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