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Recent origin and semi-permeable species boundaries in the scleractinian coral genus Stylophora from the Red Sea.

ABSTRACT: Reticulate evolution, introgressive hybridisation, and phenotypic plasticity have been documented in scleractinian corals and have challenged our ability to interpret speciation processes. Stylophora is a key model system in coral biology and physiology, but genetic analyses have revealed that cryptic lineages concealed by morphological stasis exist in the Stylophora pistillata species complex. The Red Sea represents a hotspot for Stylophora biodiversity with six morphospecies described, two of which are regionally endemic. We investigated Stylophora species boundaries from the Red Sea and the associated Symbiodinium by sequencing seven DNA loci. Stylophora morphospecies from the Red Sea were not resolved based on mitochondrial phylogenies and showed nuclear allele sharing. Low genetic differentiation, weak isolation, and strong gene flow were found among morphospecies although no signals of genetic recombination were evident among them. Stylophora mamillata harboured Symbiodinium clade C whereas the other two Stylophora morphospecies hosted either Symbiodinium clade A or C. These evolutionary patterns suggest that either gene exchange occurs through reticulate evolution or that multiple ecomorphs of a phenotypically plastic species occur in the Red Sea. The recent origin of the lineage leading to the Red Sea Stylophora may indicate an ongoing speciation driven by environmental changes and incomplete lineage sorting.

SUBMITTER: Arrigoni R

PROVIDER: S-EPMC5054360 | biostudies-literature | 2016 Oct

REPOSITORIES: biostudies-literature

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Recent origin and semi-permeable species boundaries in the scleractinian coral genus Stylophora from the Red Sea.

Arrigoni Roberto R Benzoni Francesca F Terraneo Tullia I TI Caragnano Annalisa A Berumen Michael L ML

Scientific reports 20161007

Reticulate evolution, introgressive hybridisation, and phenotypic plasticity have been documented in scleractinian corals and have challenged our ability to interpret speciation processes. Stylophora is a key model system in coral biology and physiology, but genetic analyses have revealed that cryptic lineages concealed by morphological stasis exist in the Stylophora pistillata species complex. The Red Sea represents a hotspot for Stylophora biodiversity with six morphospecies described, two of ...[more]

PMID: 27713475

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Project description:Over the past several decades, corals worldwide have been affected by global warming, experiencing severe bleaching events that have often lead to coral death. The symbiotic Red Sea coral Stylophora pistillata is considered an opportunistic ‘r’ strategist, thriving in relatively unstable and unpredictable environments, and it is considered a stress-tolerant species. This study aimed to examine S. pistillata gene expression and to clarify the cellular pathways that are active during short-term heat stress caused by an increase from 24°C to 34°C over a 10-day period. Total RNA was extracted from heat-stressed coral fragments, labeled and hybridized against a designated S. pistillata custom microarray containing approximately 12,000 genes. Our results show that the heat stress reaction was sighted from 32°C and intensified significantly after 34°C treatment. Protein interaction networks of up- and down-regulated genes were constructed. The main clustering groups of up-regulated genes were ER stress and ER protein folding, cell cycle, ubiquitin-mediated proteolysis, cell death and cell death regulation and cellular stress response genes. These genes were enriched in cellular pathways related to the unfolded protein response (UPR) in the ER, ER-associated degradation (ERAD) and ubiquitin-mediated proteolysis. An analysis of the down-regulated genes yielded different clusters of genes related to extracellular matrix and actin organization, collagen, negative regulation of cell death and the Notch and Wnt signaling pathways. Genes encoding redox regulation proteins and molecular chaperones may be considered accurate “early warning genes”, while genes related to sensing and repairing DNA damage are severe heat-related genes. Here, we suggest that during short-term heat stress, S. pistillata might divert cellular energy into mechanisms such as UPR and ERAD at the expense of growth and biomineralization processes in an effort to recover from the stress.

Project description:BackgroundThe evolution of species boundaries and the relative impact of selection and gene flow on genomic divergence are best studied in populations and species pairs exhibiting various levels of divergence along the speciation continuum. We studied species boundaries in Iberian barbels, Barbus and Luciobarbus, a system of populations and species spanning a wide degree of genetic relatedness, as well as geographic distribution and range overlap. We jointly analyze multiple types of molecular markers and morphological traits to gain a comprehensive perspective on the nature of species boundaries in these cyprinid fishes.ResultsIntraspecific molecular and morphological differentiation is visible among many populations. Genomes of all sympatric species studied are porous to gene flow, even if they are not sister species. Compared to their allopatric counterparts, sympatric representatives of different species share alleles and show an increase in all measures of nucleotide polymorphism (S, Hd, K, π and θ). High molecular diversity is particularly striking in L. steindachneri from the Tejo and Guadiana rivers, which co-varies with other sympatric species. Interestingly, different nuclear markers introgress across species boundaries at various levels, with distinct impacts on population trees. As such, some loci exhibit limited introgression and population trees resemble the presumed species tree, while alleles at other loci introgress more freely and population trees reflect geographic affinities and interspecific gene flow. Additionally, extent of introgression decreases with increasing genetic divergence in hybridizing species pairs.ConclusionsWe show that reproductive isolation in Iberian Barbus and Luciobarbus is not complete and species boundaries are semi-permeable to (some) gene flow, as different species (including non-sister) are exchanging genes in areas of sympatry. Our results support a speciation-with-gene-flow scenario with heterogeneous barriers to gene flow across the genome, strengthening with genetic divergence. This is consistent with observations coming from other systems and supports the notion that speciation is not instantaneous but a gradual process, during which different species are still able to exchange some genes, while selection prevents gene flow at other loci. We also provide evidence for a hybrid origin of a barbel ecotype, L. steindachneri, suggesting that ecology plays a key role in species coexistence and hybridization in Iberian barbels. This ecotype with intermediate, yet variable, molecular, morphological, trophic and ecological characteristics is the local product of introgressive hybridization of L. comizo with up to three different species (with L. bocagei in the Tejo, with L. microcephalus and L. sclateri in the Guadiana). In spite of the homogenizing effects of ongoing gene flow, species can still be discriminated using a combination of morphological and molecular markers. Iberian barbels are thus an ideal system for the study of species boundaries, since they span a wide range of genetic divergences, with diverse ecologies and degrees of sympatry.

Dataset Information

Recent origin and semi-permeable species boundaries in the scleractinian coral genus Stylophora from the Red Sea.

Publications

Recent origin and semi-permeable species boundaries in the scleractinian coral genus Stylophora from the Red Sea.

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