Time-calibrated phylogenetic trees establish a lag between polyploidisation and diversification in Nicotiana (Solanaceae)

James J Clarkson,Mark W Chase,Steven Dodsworth

doi:10.1007/s00606-017-1416-9

James J Clarkson, Mark W Chase + Show 1 more

Open Access

https://doi.org/10.1007/s00606-017-1416-9

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Abstract

We investigate the timing of diversification in allopolyploids of Nicotiana (Solanaceae) utilising sequence data of maternal and paternal origin to look for evidence of a lag phase during which diploidisation took place. Bayesian relaxed clock phylogenetic methods show recent allopolyploids are a result of several unique polyploidisation events, and older allopolyploid sections have undergone subsequent speciation at the polyploid level (i.e. a number of these polyploid species share a singular origin). The independently formed recent polyploid species in the genus all have mean age estimates below 1 million years ago (Ma). Nicotiana section Polydicliae (two species) evolved 1.5 Ma, N. section Repandae (four species) formed 4 Ma, and N. section Suaveolentes (~35 species) is about 6 million years old. A general trend of higher speciation rates in older polyploids is evident, but diversification dramatically increases at approximately 6 Ma (in section Suaveolentes). Nicotiana sect. Suaveolentes has spectacularly radiated to form 35 species in Australia and some Pacific islands following a lag phase of almost 6 million years. Species have filled new ecological niches and undergone extensive diploidisation (e.g. chromosome fusions bringing the ancestral allotetraploid number, n = 24, down to n = 15 and ribosomal loci numbers back to diploid condition). Considering the progenitors of Suaveolentes inhabit South America, this represents the colonisation of Australia by polyploids that have subsequently undergone a recent radiation into new environments. To our knowledge, this study is the first report of a substantial lag phase being investigated below the family level.

Highlights

Polyploidy in angiospermsNumerous whole-genome duplication (WGD) or polyploidisation events have been identified in the evolutionary history of flowering plants, leading to the wellestablished concept that all angiosperms are paleopolyploids [recently reviewed in Soltis et al (2016) and Wendel (2015)]
We investigate the timing of diversification in allopolyploids of Nicotiana (Solanaceae) utilising sequence data of maternal and paternal origin to look for evidence of a lag phase during which diploidisation took place
The phylogenetic trees resulting from BEAST2 analyses of both the plastid and nuclear datasets were consistent with previous studies in the genus

Summary

Introduction

Numerous whole-genome duplication (WGD) or polyploidisation events have been identified in the evolutionary history of flowering plants, leading to the wellestablished concept that all angiosperms are paleopolyploids [recently reviewed in Soltis et al (2016) and Wendel (2015)]. For example, Brassica species have only 8–10 pairs of chromosomes and appear to be functionally ‘diploid’ in terms of the numbers of structural (housekeeping) genes despite their paleopolyploid ancestry (they have an estimated ploidy level of 288x; Wendel 2015). Mounting evidence suggests species radiations do not immediately follow polyploid events, but rather appear after a fairly substantial time lag. Increases in net diversification rates tend to follow a lag phase post-polyploidisation, adding support to the previously proposed model (Schranz et al 2012; Tank et al 2015). It seems probable that at the genomic level the progression of events associated with diploidisation is an important factor in understanding the lag phase (Dodsworth et al 2016a)

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