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.
Allopatric speciation requiring an unbroken period of geographical isolation has been the standard model of neo-Darwinism. While doubts have been repeatedly raised, strict allopatry without any gene flow remains a plausible mechanism in most cases. To rigorously reject strict allopatry, genomic sequences superimposed on the geological records of a well-delineated geographical barrier are necessary. The Strait of Malacca, narrowly connecting the Pacific and Indian Ocean coasts, serves at different times either as a geographical barrier or a conduit of gene flow for coastal/marine species. We surveyed 1700 plants from 29 populations of 5 common mangrove species by large-scale DNA sequencing and added several whole-genome assemblies. Speciation between the two oceans is driven by cycles of isolation and gene flow due to the fluctuations in sea level leading to the opening/closing of the Strait to ocean currents. Because the time required for speciation in mangroves is longer than the isolation phases, speciation in these mangroves has proceeded through many cycles of mixing-isolation-mixing, or MIM, cycles. the MIM mechanism, by relaxing the condition of no gene flow, can promote speciation in many more geographical features than strict allopatry can. Finally, the MIM mechanism of speciation is also efficient, potentially yielding mn (m > 1) species ather n cycles. SIGNIFICANCE STATEMENT Mechanisms of species formation have always been a conundrum. Speciation between populations that are fully geographically isolated, or allopatric speciation, has been the standard solution in the last 50 years. Complete geographical isolation with no possibility of gene flow, however, is often untenable and is inefficient in generating the enormous biodiversity. By studying mangroves on the Indo-Malayan coasts, a global hotspot of coastal biodiversity, we were able to combine genomic data with geographical records on the Indo-Pacific Barrier that separates Pacific and Indian Ocean coasts. We discovered a novel mechanism of speciation that we call mixingisolation-mixing (MIM) cycles. By permitting intermittent gene flow during speciation,MIMcycles can potentially generate species at an exponential rate, thus combining speciation and biodiversity in a unified framework.
Sequencing multiple species that share the same ecological niche may be a new frontier for genomic studies. While such studies should shed light on molecular convergence, genomic-level analyses have been unsuccessful, due mainly to the absence of empirical controls. Woody plant species that colonized the global tropical coasts, collectively referred to as mangroves, are ideal for convergence studies. Here, we sequenced the genomes/transcriptomes of 16 species belonging in three major mangrove clades. To detect convergence in a large phylogeny, a CCS+ model is implemented, extending the more limited CCS method (convergence at conservative sites). Using the empirical control for reference, the CCS+ model reduces the noises drastically, thus permitting the identification of 73 convergent genes with Ptrue (probability of true convergence) > 0.9. Products of the convergent genes tend to be on the plasma membrane associated with salinity tolerance. Importantly, convergence is more often manifested at a higher level than at amino-acid (AA) sites. Relative to >50 plant species, mangroves strongly prefer 4 AAs and avoid 5 others across the genome. AA substitutions between mangrove species strongly reflect these tendencies. In conclusion, the selection of taxa, the number of species and, in particular, the empirical control are all crucial for detecting genome-wide convergence. We believe this large study of mangroves is the first successful attempt at detecting genome-wide site convergence.
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.
Significance statementMechanisms of species formation have always been a conundrum. Speciation between populations that are fully geographically isolated, or allopatric speciation, has been the standard solution in the last 50 years. Complete geographical isolation with no possibility of gene flow, however, is often untenable and is inefficient in generating the enormous biodiversity. By studying mangroves on the Indo-Malayan coasts, a global hotspot of coastal biodiversity, we were able to combine genomic data with geographical records on the Indo-Pacific barrier that separates Pacific and Indian Ocean coasts. We discovered a novel mechanism of speciation, that we call mixingisolation-mixing (MIM) cycles. By permitting intermittent gene flow during speciation, MIM can potentially generate species at an exponential rate, thus combining speciation and biodiversity in a unified framework. AbstractAllopatric speciation requiring an unbroken period of geographical isolation has been the standard model of neoDarwinism. While doubts have been repeatedly raised, strict allopatry without any gene flow remains a plausible mechanism in most cases. To rigorously reject strict allopatry, genomic sequences superimposed on the geological records of a well-delineated geographical barrier will be necessary. The Strait of Malacca, narrowly connecting the Pacific and Indian Ocean coasts, serves at different times either as a geographical barrier or a conduit of gene flow for coastal/marine species. We surveyed 1,700 plants from 29 populations of five common mangrove species by large scale DNA sequencing and added several whole-genome assemblies. Speciation between the two oceans is driven by cycles of isolation and gene flow due to the fluctuations in sea level leading to the opening/closing of the Strait to ocean currents. Because the time required for speciation in mangroves is longer than the isolation phases, speciation in these mangroves has proceeded through many cycles of mixing-isolation-mixing, or MIM cycles. The MIM mechanism, by relaxing the condition of no gene flow, can promote speciation in many more geographical features than strict allopatry can. Finally, the MIM mechanism of speciation is also efficient, potentially yielding m n (m>1) species after n cycles.
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