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. 2016 Oct 7:6:34612.
doi: 10.1038/srep34612.

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

Roberto Arrigoni  1 , Francesca Benzoni  2   3 , Tullia I Terraneo  1 , Annalisa Caragnano  3 , Michael L Berumen  1
Affiliations

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

Roberto Arrigoni et al. Sci Rep. .

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.

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Figures

Figure 1
Figure 1. Mitochondrial Bayesian phylogenetic tree reconstructions of the genus Stylophora.
(A) cytochrome oxidase I gene, (B) putative control region, (C) open reading frame of unknown function. Values at branches represent posterior Bayesian probabilities (>0.7), ML SH-like support (>70%), and MP bootstrap values (>70%), respectively. Dashes (−) indicate nodes that are statistically unsupported. Sequences obtained in this study are indicated in bold. Colours denote Stylophora morphospecies as indicated by the embedded key. Clade numbers follow designations of.
Figure 2
Figure 2. Haplowebs of Stylophora morphospecies belonging to clade 4 based on nuclear rDNA.
(A) ITS1, (B) ITS2. Each circle represents a haplotype and its size is proportional to its total frequency. Coloured lines connect haplotypes of heterozygotes individuals and colours denote Stylophora morphospecies as indicated by the embedded key. Small grey circles represent missing haplotypes and small orange circles represent a single nucleotide change.
Figure 3
Figure 3. Haplowebs of Stylophora morphospecies belonging to clade 4 based on nuclear HSP70 gene.
Each circle represents a haplotype and its size is proportional to its total frequency. Coloured lines connect haplotypes of heterozygotes individuals and colours denote Stylophora morphospecies as indicated by the embedded key. Small grey circles represent missing haplotypes and small orange circles represent a single nucleotide change.
Figure 4
Figure 4. Distribution of Symbiodinium clades across the analysed S. mamillata, S. wellsi, and “S. pistillata” complex (on the left) and across the Red Sea (on the right) based on psbA.
Circles in the map refer to the sampling sites of Stylophora corals (Data S1) and are proportional to the number of analysed colonies. The circle colours refer to Symbiodinium clade A (light grey) and clade C (dark grey). The map was created using Natural Earth (http://www.naturalearthdata.com) and QuantumGIS 2.12 (Quantum GIS Development Team, www.qgis.org).
Figure 5
Figure 5. Multi-locus time-calibrated phylogeny reconstruction of the genus Stylophora inferred from the concatenated dataset (COI, CR, ORF, ITS1, ITS2, and HSP70) analysed using BEAST.
The orange circle marks the node that was time-constrained with fossil (the first appearance of S. octophyllia in Santonian and Oman) as described in the text. Values above nodes are mean node ages and orange bars display the 95% highest posterior density (HPD) interval of node ages. Values under nodes are posterior probabilities (>0.9). Clade numbers refer to. Colours in the map are the same as used in the time-calibrated phylogeny on the left. The map was created using Natural Earth (http://www.naturalearthdata.com) and QuantumGIS 2.12 (Quantum GIS Development Team, www.qgis.org).
Figure 6
Figure 6. Variability of in-vivo colony appearance and skeleton morphology of Stylophora morphospecies from the Red Sea.
(A–D) S. mamillata SA432 and SA433, (E–H) S. wellsi SA371 and SA731, (I–T) “S. pistillata” complex: (I,J) S. danae SA730, (K,L) S. subseriata SA1500, (M,N) S. pistillata SA1743, (O,P) S. kuehlmanni SA1757, (Q,R) S. pistillata SA1546, showing verrucae typical of Pocillopora, (S,T) S. pistillata “mordax” form SA1241. Colours refer to S. mamillata (green), S. wellsi (blue), and “S. pistillata” complex (black). Scale bars 1 cm.
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