Species radiations, despite immense phenotypic variation, can be difficult to resolve phylogenetically when genetic change poorly matches the rapidity of diversification. Genomic potential furnished by palaeopolyploidy, and relative roles for adaptation, random drift and hybridisation in the apportionment of genetic variation, remain poorly understood factors. Here, we study these aspects in a model radiation, Syzygium, the most species-rich tree genus worldwide. Genomes of 182 distinct species and 58 unidentified taxa are compared against a chromosome-level reference genome of the sea apple, Syzygium grande. We show that while Syzygium shares an ancient genome doubling event with other Myrtales, little evidence exists for recent polyploidy events. Phylogenomics confirms that Syzygium originated in Australia-New Guinea and diversified in multiple migrations, eastward to the Pacific and westward to India and Africa, in bursts of speciation visible as poorly resolved branches on phylogenies. Furthermore, some sublineages demonstrate genomic clines that recapitulate cladogenetic events, suggesting that stepwise geographic speciation, a neutral process, has been important in Syzygium diversification.

BackgroundSatellite DNA is a rapidly diverging, largely repetitive DNA component of many eukaryotic genomes. Here we analyse the evolutionary dynamics of a satellite DNA repeat in the genomes of a group of Asian subtropical lady slipper orchids (Paphiopedilum subgenus Parvisepalum and representative species in the other subgenera/sections across the genus). A new satellite repeat in Paphiopedilum subgenus Parvisepalum, SatA, was identified and characterized using the RepeatExplorer pipeline in HiSeq Illumina reads from P. armeniacum (2n = 26). Reconstructed monomers were used to design a satellite-specific fluorescent in situ hybridization (FISH) probe. The data were also analysed within a phylogenetic framework built using the internal transcribed spacer (ITS) sequences of 45S nuclear ribosomal DNA.ResultsSatA comprises c. 14.5% of the P. armeniacum genome and is specific to subgenus Parvisepalum. It is composed of four primary monomers that range from 230 to 359 bp and contains multiple inverted repeat regions with hairpin-loop motifs. A new karyotype of P. vietnamense (2n = 28) is presented and shows that the chromosome number in subgenus Parvisepalum is not conserved at 2n = 26, as previously reported. The physical locations of SatA sequences were visualised on the chromosomes of all seven Paphiopedilum species of subgenus Parvisepalum (2n = 26–28), together with the 5S and 45S rDNA loci using FISH. The SatA repeats were predominantly localisedin the centromeric, peri-centromeric and sub-telocentric chromosome regions, but the exact distribution pattern was species-specific.ConclusionsWe conclude that the newly discovered, highly abundant and rapidly evolving satellite sequence SatA is specific to Paphiopedilum subgenus Parvisepalum. SatA and rDNA chromosomal distributions are characteristic of species, and comparisons between species reveal that the distribution patterns generate a strong phylogenetic signal. We also conclude that the ancestral chromosome number of subgenus Parvisepalum and indeed of all Paphiopedilum could be either 2n = 26 or 28, if P. vietnamense is sister to all species in the subgenus as suggested by the ITS data.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4956-7) contains supplementary material, which is available to authorized users.

Species radiations have long fascinated biologists, but the contribution of adaptation to observed diversity and speciation is still an open question. Here, we explore this question using the clove genus, Syzygium, the world’s largest genus of tree species comprising approximately 1200 species. We dissect Syzygium diversity through shotgun sequencing of 182 distinct species and 58 additional as-yet unidentified taxa, and assess their genetic diversity against a chromosome-level reference genome of the sea apple, Syzygium grande. We show that Syzygium grande shares a whole genome duplication (WGD) event with other Myrtales. Genomic analyses confirm that Syzygium originated in Sahul (Australia-New Guinea), and later diversified eastward to the Hawaiian Islands and westward in multiple independent migration events. The migrations were associated with bursts of speciation events, visible by poorly resolved branches on phylogenies and networks, some of which were likely confounded by incomplete lineage sorting. Clinal genomic variation in some sublineages follows phylogenetic progression, which coupled with sympatric occurrences of distantly related species suggests that both geographic and ecological speciation have been important in the diversification of Syzygium. Together, these results point to a mixture of both neutral and adaptive drivers having contributed to the radiation of the genus.