Mangroves invade some very marginal habitats for woody plants—at the interface between land and sea. Since mangroves anchor tropical coastal communities globally, their origin, diversification and adaptation are of scientific significance, particularly at a time of global climate change. In this study, a combination of single-molecule long reads and the more conventional short reads are generated from Rhizophora apiculata for the de novo assembly of its genome to a near chromosome level. The longest scaffold, N50 and N90 for the R. apiculata genome, are 13.3 Mb, 5.4 Mb and 1.0 Mb, respectively. Short reads for the genomes and transcriptomes of eight related species are also generated. We find that the ancestor of Rhizophoreae experienced a whole-genome duplication ~70 Myrs ago, which is followed rather quickly by colonization and species diversification. Mangroves exhibit pan-exome modifications of amino acid (AA) usage as well as unusual AA substitutions among closely related species. The usage and substitution of AAs, unique among plants surveyed, is correlated with the rapid evolution of proteins in mangroves. A small subset of these substitutions is associated with mangroves’ highly specialized traits (vivipary and red bark) thought to be adaptive in the intertidal habitats. Despite the many adaptive features, mangroves are among the least genetically diverse plants, likely the result of continual habitat turnovers caused by repeated rises and falls of sea level in the geologically recent past. Mangrove genomes thus inform about their past evolutionary success as well as portend a possibly difficult future.

When living organisms independently invade a new environment, the evolution of similar phenotypic traits is often observed. An interesting but contentious issue is whether the underlying molecular biology also converges in the new habitat. Independent invasions of tropical intertidal zones by woody plants, collectively referred to as mangrove trees, represent some dramatic examples. The high salinity, hypoxia, and other stressors in the new habitat might have affected both genomic features and protein structures. Here, we developed a new method for detecting convergence at conservative Sites (CCS) and applied it to the genomic sequences of mangroves. In simulations, the CCS method drastically reduces random convergence at rapidly evolving sites as well as falsely inferred convergence caused by the misinferences of the ancestral character. In mangrove genomes, we estimated ∼400 genes that have experienced convergence over the background level of convergence in the nonmangrove relatives. The convergent genes are enriched in pathways related to stress response and embryo development, which could be important for mangroves' adaptation to the new habitat.

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Convergent evolution is especially common in plants that have independently adapted to the same extreme environments (i.e., extremophile plants). The recent burst of omics data has alleviated many limitations that have hampered molecular convergence studies of non-model extremophile plants. In this review, we summarize cases of genomic convergence in these taxa to examine the extent and type of genomic convergence during the process of adaptation to extreme environments. Despite being well studied by candidate gene approaches, convergent evolution at individual sites is rare and often has a high false-positive rate when assessed in whole genomes. By contrast, genomic convergence at higher genetic levels has been detected during adaptation to the same extreme environments. Examples include the convergence of biological pathways and changes in gene expression, gene copy number, amino acid usage, and GC content. Higher convergence levels play important roles in the adaptive evolution of extremophiles and may be more frequent and involve more genes. In several cases, multiple types of convergence events have been found to co-occur. However, empirical and theoretical studies of this higher level convergent evolution are still limited. In conclusion, both the development of powerful approaches and the detection of convergence at various genetic levels are needed to further reveal the genetic mechanisms of plant adaptation to extreme environments.

Aim Population genomics data were used to determine the genetic diversity, genetic divergence and genetic structure of the mangrove, Rhizophora apiculata, across its distributional range and to re-assess the evolutionary processes that shaped its current distribution.Location The Indo-Malesian region section of the Indo-West Pacific region.Methods Next-generation sequencing technology was used to sequence 81 nuclear loci from a pooled DNA sample of 31-44 individuals of Rhizophora apiculata from 11 populations. Five nuclear loci from six to eight individuals from 18 populations were sequenced using conventional Sanger sequencing technology to validate the results.Results Genetic diversity at the population level was low (p and h were < 1.0 9 10 À3 in most of the populations), but relatively high at the species level (p = 2.419 9 10 À3 and h = 1.362 9 10 À3 ). The populations of R. apiculata in the Indo-Malesian region were genetically differentiated and grouped into three clusters: east Indian Ocean (EIO), South China Sea (SCS) and Australasia (AUA). Based on the genetic distance matrices, two genetic discontinuities were observed, and they correspond to the Malay Peninsula land barrier and the Wallacea zone. The admixture observed in populations from the Malacca Strait was attributed to asymmetric gene flow through the strait, which was simulated by the isolation-with-migration (IM) model.Main conclusion Both the Sunda shelf barrier and ocean currents in Wallacea contributed to the observed genetic discontinuity, which separated R. apiculata into three clusters (SCS, EIO and AUA). The cycle between extinction and recolonization in the SCS in response to Pleistocene sea level fluctuations reduced the genetic diversity within populations. The repeated opening and closing of the gene flow corridors, such as the Malacca Strait, may have blurred the genetic discontinuities to an extent and introduced an admixture into populations in boundary areas.