Ancient geograpical barriers drive differentiation among Sonneratia caseolaris populations and recent divergence from S. Ianceolata

Glacial vicariance is thought to influence population dynamics and speciation of many marine organisms. Mangroves, a plant group inhabiting intertidal zones, were also profoundly influenced by Pleistocene glaciations. In this study, we investigated phylogeographic patterns of a widespread mangrove species Sonneratia caseolaris and a narrowly distributed, closely related species S. lanceolata to infer their divergence histories and related it to historical geological events. We sequenced two chloroplast fragments and five nuclear genes for one population of S. lanceolata and 12 populations of S. caseolaris across the Indo-West Pacific (IWP) region to evaluate genetic differentiation and divergence time among them. Phylogenetic analysis based on sequences of nuclear ribosomal internal transcribed spacer and a nuclear gene rpl9 for all Sonneratia species indicate that S. lanceolata individuals are nested within S. caseolaris. We found strong genetic structure among geographic regions (South China Sea, the Indian Ocean, and eastern Australia) inhabited by S. caseolaris. We estimated that divergence between the Indo-Malesia and Australasia populations occurred 4.035 million years ago (MYA), prior to the onset of Pleistocene. BARRIERS analysis suggested that complex geographic features in the IWP region had largely shaped the phylogeographic patterns of S. caseolaris. Furthermore, haplotype analyses provided convincing evidence for secondary contact of the South China Sea and the Indian Ocean lineages at the Indo-Pacific boundary. Demographic history inference under isolation and migration (IM) model detected substantial gene flow from the Sri Lanka populations to the populations in the Java Island. Moreover, multi-locus sequence analysis indicated that S. lanceolata was most closely related to the Indian Ocean populations of S. caseolaris and the divergence time between them was 2.057 MYA, coinciding with the onset of the Pleistocene glaciation. Our results suggest that geographic isolation driven by the Pleistocene ice age resulted in the recent origin of S. lanceolata

Speciation with gene flow via cycles of isolation and migration: insights from multiple mangrove taxa

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 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 mn (m>1) species after n cycles

Extensive gene flow in secondary sympatry after allopatric speciation

In the conventional view, species are separate gene pools delineated by reproductive isolation (RI). In an alternative view, species may also be delineated by a small set of ‘speciation genes’ without full RI, a view that has gained broad acceptance. A recent survey, however, suggested that the extensive literature on ‘speciation with gene flow’ is mostly (if not all) about exchanges in the early stages of speciation. There is no definitive evidence that the observed gene flow actually happened after speciation is completed. Here, we wish to know whether ‘good species’ (defined by the ‘secondary sympatry’ test) do continue to exchange genes and, importantly, under what conditions such exchanges can be observed. De novo whole-genome assembly and re-sequencing of individuals across the range of two closely related mangrove species (Rhizophora mucronata and R. stylosa) reveal the genomes to be well delineated in allopatry. They became sympatric in northeastern Australia but remain distinct species. Nevertheless, their genomes harbor ∼4000–10 000 introgression blocks averaging only about 3–4 Kb. These fine-grained introgressions indicate continual gene flow long after speciation as non-introgressable ‘genomic islets,’ ∼1.4 Kb in size, often harbor diverging genes of flower or gamete development. The fine-grained introgression in secondary sympatry may help settle the debate about sympatric vs. micro-allopatric speciation. In conclusion, true ‘good species’ may often continue to exchange genes but the opportunity for detection is highly constrained

Convergent adaptation of the genomes of woody plants at the land-sea interface

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 P-true (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

Transcriptional Homeostasis of a Mangrove Species, Ceriops tagal, in Saline Environments, as Revealed by Microarray Analysis

<div><h3>Background</h3><p>Differential responses to the environmental stresses at the level of transcription play a critical role in adaptation. Mangrove species compose a dominant community in intertidal zones and form dense forests at the sea-land interface, and although the anatomical and physiological features associated with their salt-tolerant lifestyles have been well characterized, little is known about the impact of transcriptional phenotypes on their adaptation to these saline environments.</p> <h3>Methodology and Principal findings</h3><p>We report the time-course transcript profiles in the roots of a true mangrove species, <em>Ceriops tagal</em>, as revealed by a series of microarray experiments. The expression of a total of 432 transcripts changed significantly in the roots of <em>C. tagal</em> under salt shock, of which 83 had a more than 2-fold change and were further assembled into 59 unigenes. Global transcription was stable at the early stage of salt stress and then was gradually dysregulated with the increased duration of the stress. Importantly, a pair-wise comparison of predicted homologous gene pairs revealed that the transcriptional regulations of most of the differentially expressed genes were highly divergent in <em>C. tagal</em> from that in salt-sensitive species, <em>Arabidopsis thaliana</em>.</p> <h3>Conclusions/Significance</h3><p>This work suggests that transcriptional homeostasis and specific transcriptional regulation are major events in the roots of <em>C. tagal</em> when subjected to salt shock, which could contribute to the establishment of adaptation to saline environments and, thus, facilitate the salt-tolerant lifestyle of this mangrove species. Furthermore, the candidate genes underlying the adaptation were identified through comparative analyses. This study provides a foundation for dissecting the genetic basis of the adaptation of mangroves to intertidal environments.</p> </div

Description of a new natural Sonneratia hybrid from Hainan Island, China

Here, we describe, illustrate and compare a new natural hybrid, Sonneratia × zhongcairongii Y. S. Wang & S. H. Shi (Sonneratiaceae), with its possible parent species. Based on its morphological characteristics and habitat conditions, this taxon is considered to represent a sterile hybrid between S. alba and S. apetala. In China, the new hybrid is only reported in the mangrove forest in Dongzhai Harbour, Hainan Island. It has intermediate characteristics with its parents by elliptical leaf blades, peltate stigma, terminal or axillary inflorescence with 1–3 flower dichasia, cup – shaped calyx (4–6 calyx lobes) and no petals. We also provide a key for the identification of Sonneratia species

DNA barcoding reveals insect diversity in the mangrove ecosystems of the Hainan Island, China

Insect diversity is an indicator of environmental conditions. Frequent outbreaks of mangrove pests have threatened the fragile mangrove ecosystem in China and the sustainable utilization of mangrove resources. The understanding of mangrove pests as well as a fundamental knowledge of insect diversity in mangrove forests in China has been hindered by the difficulty of morphological species delimitation because captured insect specimens are either larvae or incompletely-preserved adults. DNA barcoding technology uses only a small amount of DNA to conduct species identification. Taking advantage of this, we investigated the entomofauna of mangrove forests in Hainan island by using a barcode combining cytochrome c oxidase subunit I (COI) and cytochrome-b (Cytb). We collected 627 specimens at six localities around the island, which were identified as 219 insect species belonging to 11 orders and 72 families. Lepidoptera, Coleoptera, and Hymenoptera are the most species-rich and abundant taxa. We also identified 13 mangrove pests, five parasitoids, and 12 species of predators.The accepted manuscript in pdf format is listed with the files at the bottom of this page. The presentation of the authors' names and (or) special characters in the title of the manuscript may differ slightly between what is listed on this page and what is listed in the pdf file of the accepted manuscript; that in the pdf file of the accepted manuscript is what was submitted by the author

Genetic discontinuities in a dominant mangrove Rhizophora apiculata (Rhizophoraceae) in the Indo-Malesian region

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 (π and θ were < 1.0 × 10−3 in most of the populations), but relatively high at the species level (π = 2.419 × 10−3 and θ = 1.362 × 10−3). 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

Population subdivision promoted by a sea-level-change-driven bottleneck: A glimpse from the evolutionary history of the mangrove plant Aegiceras corniculatum

Historic climate changes drive geographical populations of coastal plants to contract and recover dynamically, even die out completely. Species suffering from such bottlenecks usually lose intraspecific genetic diversity, but how do these events influence population subdivision patterns of coastal plants? Here, we investigated this question in the typical coastal plant: mangrove species Aegiceras corniculatum. Inhabiting the intertidal zone of the tropical and subtropical coast of the Indo-West Pacific oceans, its populations are deemed to be greatly shaped by historic sea-level fluctuations. Using dual methods of Sanger and Illumina sequencing, we found that the 18 sampled populations were structured into two groups, namely, the "Indo-Malayan" group, comprising three subgroups (the northern South China Sea, Gulf of Bengal, and Bali), and the "Pan-Australasia" group, comprising the subgroups of the southern South China Sea and Australasia. Based on the approximate Bayesian computations and Stairway Plot, we inferred that the southern South China Sea subgroup, which penetrates the interior of the "Indo-Malayan" group, originated from the Australasia subgroup, accompanied by a severe bottleneck event, with a spot of gene flow from both the Australasia and "Indo-Malayan" groups. Geographical barriers such as the Sundaland underlie the genetic break between Indian and Pacific Oceans, but the discontinuity between southern and northern South China Sea was originated from genetic drift in the bottleneck event. Hence, we revealed a case evidencing that the bottleneck event promoted population subdivision. This conclusion may be applicable in other taxa beyond coastal plants

Distribution of Mangrove Species Kandelia obovata in China Using Time-series Sentinel-2 Imagery for Sustainable Mangrove Management

Mangrove management in China is converting from emphasis on occupied area to intrinsical quality. Mangrove species have varied ecological values, e.g., those having well-developed prop roots are more beneficial for coastal stabilization. The detailed distribution of mangrove species on a national scale remains a challenge, impeding species-specific applications in the ecology and management of mangroves, as well as evaluations of related Sustainable Development Goals. Although local-scale studies have explored various data sources, the variability of plant phenology is the key factor preventing their generalization from local areas to large latitudinal spans (e.g., the coast of China). The separability time period, defined by a separability metric for each scene of the image time series, provides a potential way to tackle the aforementioned problem. We conducted a case study on mapping Kandelia obovata in China based on Sentinel-2 time-series imagery, as it is a representative native mangrove species with the largest latitudinal span and tolerance to low temperatures. The proposed approach considered the separability between K. obovata and its typical co-occurring mangrove species, as well as that between K. obovata and salt marshes. The overall accuracy of the generated K. obovata map in China for 2020 reached 88.5% based on independently collected samples. The proposed approach is transferable to diverse mangrove species that inhabit a vast latitudinal span. The implications for sustainable mangrove management were discussed to reveal the benefits to precise management of mangroves, accurate biomass and carbon estimations accounting for species differences, and effective evaluation of mangrove ecosystem services