Abstract: Polyploidy is a major factor in the evolution of plants, yet we know little about the origin and evolution of polyploidy in intertidal species. This study aimed to identify the evolutionary transitions in three true-mangrove species of the genus Acanthus distributed in the Indo–West Pacific region. For this purpose, we took an integrative approach that combined data on morphology, cytology, climatic niche, phylogeny, and biogeography of 493 samples from 42 geographic sites. Our results show that the Acanthus ilicifolius lineage distributed east of the Thai–Malay Peninsula possesses a tetraploid karyotype, which is morphologically distinct from that of the lineage on the west side. The haplotype networks and phylogenetic trees for the chloroplast genome and eight nuclear genes reveal that the tetraploid species has two sub-genomes, one each from A. ilicifolius and A. ebracteatus, the paternal and maternal parents, respectively. Population structure analysis also supports the hybrid speciation history of the new tetraploid species. The two sub-genomes of the tetraploid species diverged from their diploid progenitors during the Pleistocene. Environmental niche models revealed that the tetraploid species not only occupied the near-entire niche space of the diploids, but also expanded into novel environments. Our findings suggest that A. ilicifolius species distributed on the east side of the Thai–Malay Peninsula should be regarded as a new species, A. tetraploideus, which originated from hybridization between A. ilicifolius and A. ebracteatus, followed by chromosome doubling. This is the first report of a true-mangrove allopolyploid species that can reproduce sexually and clonally reproduction, which explains the long-term adaptive potential of the species.

Key words: Acanthus, Allopolyploid, Biogeography, Evolution, Hybridization, Polyploidy