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

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.

Reconstructing Phylogenetic Relationships Based on Repeat Sequence Similarities

“…The branches of the network showed no conflicting splits, indicating overall consistency in the topology of the individual trees employed to infer the phylogeny. The phylogenetic hypothesis we obtained was equivalent to previous ones based on nrITS, plastid markers, low-copy nuclear genes or repeat abundances (Chase et al 2003;Clarkson et al 2004;Kelly et al 2013;Renny-Byfield et al 2013;Dodsworth et al 2017).…”

“…Repandae is a group of four allotetraploid species originating from a single allopolyploidisation event -between N. obtusifolia and N. sylvestris -approximately 4-5 million years ago (Clarkson et al 2005;Clarkson et al 2017). The phylogenetic relationships among the species of this group have been thoroughly analysed based on nuclear and plastid DNA sequences, as well as using the abundance of repeats as systematic markers (Dodsworth et al 2017), each time resulting in consistent results. Therefore, it constitutes a perfect study case to test the novel phylogenetic approach presented in the current work.…”

“…Therefore, it constitutes a perfect study case to test the novel phylogenetic approach presented in the current work. Plant materials and Illumina sequencing details can be found in Dodsworth et al (2017). The reads can be downloaded from NCBI Short Read Archive [SRA] using the following accession numbers: N. repanda-SRR453021; N. nudicaulis-SRR452996]; N. sylvestris-SRR343066; N. obtusifolia-SRR452993; N. nesophila-SRR4046065; N. stocktonii-SRR4046066.…”

UNEXPECTED DIVERSITY OF AUSTRALIAN TOBACCO SPECIES (NICOTIANA SECTION SUAVEOLENTES, SOLANACEAE)

“…Suaveolentes in Australia indicated an early Miocene arrival, pre-dating the onset of aridification at ∼15 Ma, with vicariance then largely driving cyclical arid zone speciation. This contrasts with the six million-year origin calculated by Clarkson et al (2017), but the precise origins of the section may never be known with certainty, due to the long timelines involved, and the great likelihood of local extinction events.…”

“…About six million years ago, the allotetraploid N . section Suaveolentes was formed in South America (Clarkson et al, 2017), from where its ancestor dispersed to Africa (Namibia; one species), Australia (c. 40 species) and the Pacific islands (three species), including New Caledonia and the Marquesas Islands in French Polynesia (Marks, 2010). Today, no allotetraploid species of N .…”