Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change

Edited by Nancy Knowlton, Smithsonian Institution, Washington, DC, and approved March 3, 2016 (received for review February 4, 2016)
April 4, 2016
113 (16) 4416-4421


Reef corals in the Persian/Arabian Gulf (PAG) withstand exceptionally high salinity and regular summer temperatures of ∼35 °C that kill conspecifics elsewhere. These thermotolerant communities established themselves within only ∼6,000 y under the pressure of rapid climate change and can therefore inform how other coral reefs may respond to global warming. One key to the thermotolerance of PAG corals is their symbiosis with Symbiodinium thermophilum. Phylogeographic evidence indicates that this symbiont represents a stress-tolerant subpopulation of an ancestral taxonomic group with surprising genetic diversity that exists at barely detectable levels outside the PAG. Our results highlight the critical importance of present-day biodiversity for future adaptation to climate change for coral reefs and ecosystems in general.


Coral communities in the Persian/Arabian Gulf (PAG) withstand unusually high salinity levels and regular summer temperature maxima of up to ∼35 °C that kill conspecifics elsewhere. Due to the recent formation of the PAG and its subsequent shift to a hot climate, these corals have had only <6,000 y to adapt to these extreme conditions and can therefore inform on how coral reefs may respond to global warming. One key to coral survival in the world’s warmest reefs are symbioses with a newly discovered alga, Symbiodinium thermophilum. Currently, it is unknown whether this symbiont originated elsewhere or emerged from unexpectedly fast evolution catalyzed by the extreme environment. Analyzing genetic diversity of symbiotic algae across >5,000 km of the PAG, the Gulf of Oman, and the Red Sea coastline, we show that S. thermophilum is a member of a highly diverse, ancient group of symbionts cryptically distributed outside the PAG. We argue that the adjustment to temperature extremes by PAG corals was facilitated by the positive selection of preadapted symbionts. Our findings suggest that maintaining the largest possible pool of potentially stress-tolerant genotypes by protecting existing biodiversity is crucial to promote rapid adaptation to present-day climate change, not only for coral reefs, but for ecosystems in general.
Episodes of heat stress cause coral bleaching, the breakdown of the obligate symbiosis between the coral host and its algal partner that contributes to the global decline of coral reefs (1). Despite their capacity to acclimate to rising seawater temperatures (2), corals will suffer from high-frequency bleaching episodes by the end of this century, threatening their survival in the warmer oceans of the future (3). Changing to symbiotic associations with more thermally tolerant types like Symbiodinium trenchii (synonym type D1a/D1–4) may increase the heat stress tolerance of corals rapidly (46). However, due to tradeoffs such as reduced calcification rates that can be associated with hosting alternative symbionts, reef ecosystems may ultimately fail to benefit from the increased thermal tolerance of their most important habitat-forming species (5, 6). Hence, it is unclear at present whether alternative symbiont associations will rescue reefs from their expected demise in response to global warming.
We are using the Persian/Arabian Gulf (PAG), the world’s hottest sea, as a natural laboratory where coral communities endure regular summer temperatures of up to ∼35 °C to address the question of how coral reefs relying on heat-tolerant Symbiodinium may respond to rapid climate change over a prolonged period. Due to rising sea levels associated with the last glacial retreat, the modern PAG started to form ∼12,500 y before present (BP) by ingression of the Indian Ocean into the previously dry basin, extending to present-day shorelines ∼6,000 y BP (7). By this time, the climate in the Middle East began to change from cooler and moister to warmer and more arid, reaching today’s conditions only ∼4,000 y ago (810). Hence, the coral communities of the PAG, composed mostly of a subset of Indian Ocean species (11), have had to adjust rapidly to temperatures not expected to occur in other parts of the world’s oceans before the next century (12). We recently discovered that corals of the southern, hottest region of the PAG form a prevalent, year-round association with a thermally tolerant symbiont species, Symbiodinium thermophilum (13). Although the symbiosis with S. thermophilum might not be the sole cause for the heat tolerance, and others factors including the host physiology (14) and environmental conditions (such as the exceptionally high salinity in the relevant PAG regions) (15) may contribute to the resilience of the holobiont, the striking dominance of this symbiont in the southern PAG strongly suggests that it represents a key component to the success of corals in this extreme environment.
S. thermophilum can be identified by specific intragenomic variants of the nuclear ribosomal second internal transcribed spacer region (ITS2), which carry an 8-bp duplication indel named “S. thermo.-indel” (13). In close to pure S. thermophilum populations, these variants represent an average ∼16% of the total ITS2 sequences, however this proportion can vary considerably (Fig. S1). Additionally, this symbiont can be distinguished by its genetically disparate resolution from other closely related ITS2 C3 types using the noncoding region of the chloroplastic psbA gene (psbAncr) among other markers (13). As yet undetected in other parts of the world, our previous work suggested that symbionts characterized by the S. thermo.-indel and a disparate psbAncr resolution (hereafter S. thermophilum group) may not be endemic to the PAG (15). Because the understanding of heat tolerance in coral–symbiont associations is crucial in gauging the adaptation potential of coral reefs to global warming, we investigated the origin of S. thermophilum to assess whether this thermotolerant symbiont emerged as the result of an unexpectedly rapid evolution under the pressure of the extreme environmental conditions in the PAG or whether this species originated elsewhere.
Fig. S1.
Proportion of S. thermo.-indel–containing variants in total ITS2 sequences from C3 predominated cnidarians (n = 116) from the PAG. Cnidarians included in the analysis contained >50% clade C Symbiodinium, of which >95% were C3 or closely related variants. Average % S. thermo.-indel–containing amplicons: 16.6%.

Results and Discussion

We screened for S. thermophilum at 23 sites across >5,000 km of coastline from the northwestern PAG to the Gulf of Eilat/Aqaba in the Red Sea (Fig. 1A). The symbiont was detected by the presence of the S. thermo.-indel in libraries containing 2.8 × 106 ITS2 amplicons obtained by 454 and MiSeq sequencing (except Eilat; see Methods) of >900 symbiotic hexa- and octocorallians from 46 genera (Tables S1 and S2). The results for the 10 most sampled taxa are presented in Fig. 1A, with details being given for all samples in Fig. 2 and Tables S1 and S2.
Fig. 1.
Identification and phylogenetic resolution of the S. thermophilum group. Colors denote sampling locations according to map coloration with yellow denoting non-S. thermophilum group clade C symbionts. (A) Sampling sites (three letter abbreviations; e.g., JAN) are detailed in Table S1. The presence of S. thermophilum group symbionts within the 10 most sampled genera are presented categorically (undetected, <1% and >1% S. thermo.-indel). Regional summaries (*)/(*) represent the proportion of samples in which S. thermophilum group symbionts were detected (Tables S1 and S2). The map was created as detailed in Hume et al., 2015 (13). (B) PsbAncr estimated phylogeny of S. thermophilum group samples created through the addition of samples collected in the Gulf of Oman and the Red Sea (sequenced as part of this study) to psbAncr alignments previously constructed (15). Symbionts within the gray branches are ITS2 type C3 and closely related ITS2 types from the Atlantic and Indo-Pacific (17). Wedges and circles represent collapsed groups and individual samples, respectively. Lengths of collapsed branches are drawn to scale with number of contained sequences indicated. (C) Supermatrix Bayesian estimation of phylogeny using six additional genetic markers (Fig. S3 and Table S5) on a selection of cnidarian-harbored Symbiodinium samples collected in the PAG, the Gulf of Oman, the Red Sea, as well as several reference locations (see Methods for further details). The full collapsed tree with clade C subtree is expanded below. Numbers in parentheses represent multiple sequences resolving at the same position and are colored according to collection site and sequence type (Gulf of Oman, blue; PAG, green; Red Sea, red; reference sequences, yellow). Gray groupings contain reference Symbiodinium from clades A–I as well as two outgroups (G. simplex and P. glacialis) (Table S5). Nodes supported with posterior probability (PP) above 0.8 are not displayed. Nodes with supports below 0.8 are marked with an asterisk (*).
Fig. 2.
Identification of clade C sequences containing the S. thermo.-indel as a proxy for the presence of S. thermophilum and classification of the symbiont complements in all sampled individuals. Each vertical bar represents a single sample. The contribution of sequences representing different clades/species to the sequence complement of each sample is color-coded as defined in the legend. Sample origins are shown below the chart (Table S1). Numbers of samples containing the S. thermo.-indel as a proportion of the total samples are shown in white in the format (*)/(*) (Tables S1 and S2).
Table S1.
Detection of S. thermophilum symbionts in the PAG, the Gulf of Oman, and the Red Sea through screening for the rDNA ITS2 S. thermo.-indel
Water bodyRegion (abbreviation)ReefNumber of samples% hosts with S. thermo.-indelHosts >1%* S. thermo.-indelHosts <1%* S. thermo.-indelGenera with S. thermo.-indel
PAGJana (JAN)Subri3129635 of 13
 Subri (Jana)41278310 of 18
 Chandelier23741347 of 9
Yassat (YAS)Al Yassat331003307 of 7
Saadiyat (SAD)Saadiyat429840111 of 12
  Ras Ghanada26962237 of 7
Gulf of OmanFujairah (FUJ)Al Aqah3415144 of 14
 Dibba Rock370000 of 14
Muscat (MUS)Bandar Khayran Islet900000 of 21
 Damanyat 3 sisters350000 of 17
 Damanyat legends360000 of 16
 Damanyat Noodle580000 of 15
 Fahal Island Site I346112 of 14
 Fahal Island Site II287112 of 12
 Saifat Ash Shiekh871101 of 23
Red SeaEilat (EIL)Eilat270000 of 1
Yanbu (YAN)Yanbu 23313103 of 13
 Yanbu Ayona360000 of 17
KAUST (KAU)KAUST Al Fahal420000 of 16
 KAUST Inner Fsar313102 of 13
 KAUST Shib Nazaar430000 of 16
Al Lith (LIT)Al Lith Abu Lath4015337 of 17
 Al Lith South Reef330000 of 18
This is representative of total ITS2 amplicons detected (all clades).
Table S2.
Proportion of taxa in which S. thermophilum symbionts were detected through screening for the ribosomal DNA ITS2 S. thermo.-indel
Alcyonacea  Unidentified0/4
Nephtheidae  Nephthea0/1
Xeniidae  Xenia0/23
Diploastreidae  Diploastrea0/5
Caryophylliidae  Cladocora0/1
Fungiidae  Fungia0/7
Montastraeidae  Montastraea0/1
Pectiniidae  Mycedium0/1
Members of the S. thermophilum group were found in 10 out of the 11 sampled genera in the southern PAG but were less frequent in the western PAG and could only be detected at low levels in ∼4% of samples in the Gulf of Oman and the Red Sea (Figs. 1 and 2 and Tables S1 and S2). Additionally, when screening public databases for ITS2 sequences containing the S. thermo.-indel, we retrieved a close match with a sequence originating from Kaneohe Bay, Hawaii, which was recently entered in GenBank (accession no. EF428343). This hit may indicate the presence of a S. thermophilum group member in the Indo-Pacific, implying an even wider, cryptic distribution.
PsbAncr sequences of samples containing the S. thermo.-indel from the Gulf of Oman and Red Sea are resolved within the strongly supported (PP = 1) monophyletic S. thermophilum group (Fig. 1B and Table S3) but as genetically separate from the majority of PAG sequences and with larger average within-group genetic distances (0.065 vs. 0.039; Table S4). The average genetic distance of the five most divergent sequence pairs within the S. thermophilum group was larger than that between the considerably divergent C27 and C40 ITS2 types (0.163 vs. 0.154; Fig. S2 and Table S4), demonstrating a genetic diversity in the group greater than that found among considerably divergent clade C lineages. This highlights the existence of a wide range of previously unidentified and possibly stress-tolerant genotypes within the group.
Table S3.
Accession numbers for the seven genetic markers (amplicons) used in this study
ADD036*Al AqahFUJC39KR996268KR996350KR996309KR996391KR996432KR996473KT156647
ALB028*Al LithLITC41KR996270KR996352KR996311KR996393KR996434KR996475KT156649
ALB012*Al LithLITC41KR996271KR996353KR996312KR996394KR996435KR996476KT156650
ADD3*Al AqahFUJGroupKR996275KR996357KR996316KR996398KR996439KR996480KT156654
ALB4*Al LithLITGroupKR996276KR996358KR996317KR996399KR996440KR996481KT156655
ALB20*Al LithLITGroupKR996277KR996359KR996318KR996400KR996441KR996482KT156656
ALB30*Al LithLITGroupKR996281KR996363KR996322KR996404KR996445KR996486KT156660
OMA71*Fahal Isl.MUSGroupKR996282KR996364KR996323KR996405KR996446KR996487KT156661
ADD014*Al AqahFUJGroupN/AN/AN/AN/AN/AN/AKT156662
B334§Al AqahN/AGroupKR996296KR996378KR996337KR996419KR996460KR996501KP280310
B21561§Al AqahN/AGroupKR996299KR996381KR996340KR996422KR996463KR996504KP280307
B21560§Al AqahN/AGroupKR996302KR996384KR996343KR996425KR996466KR996507KP280309 
BH1550§Al AqahN/AGroupKR996303KR996385KR996344KR996426KR996467KR996508KP280308 
Samples were collected as part of this study.
Locations were as follows: MP, Musandam Peninsular; UAQ, Umm Al Quwain; SAS, Saifat Ash Shiekh.
The group is S. thermophilum.
Samples were collected and psbAncr sequences were amplified as part of D’Angelo et al., 2015 (15).
Table S4.
Pairwise and average between- and within-group genetic distances based on the psbAncr alignment from this study*
Sequence/group 1Sequence/group 2Genetic distance
S. thermophilum Average, 0.163
ALB30 (Al Lith)BH1428 (Umm Al Quwain)0.155
BH1660 (Umm Al Quwain)BH1693 (Dalma)0.156
B335 (Muscat)BH1633 (Ras Ghanada)0.160
B21557 (Musandam)B315 (Saadiyat)0.167
B21561 (Fujairah)BH1642 (Saadiyat)0.178
C40 and C27 Average, 0.154
Between group  
S. thermophilum (PAG) 0.039
S. thermophilum (external) 0.065
Pairwise genetic distances of the five most disparate pairs within the S. thermophilum group and between the ITS2 type C40 and C27 groups are shown under the first two corresponding subheadings. Between-group genetic distance of three ITS2 groups (C40, C7, and C7a) and a monophyletic group of Symbiodinium ITS2 type C3 sequences originating from host S. siderea samples (C3SID) as highlighted in yellow in figure 8A from Thornhill et al., 2014 (17) are shown under the subheading ”Between group.” Finally, average within-group genetic distances of S. thermophilum group samples from the PAG and external to the PAG are shown. A partial graphical representation of the data is shown in Fig. S2. Sampling locations are detailed in parentheses.
Sequences were obtained in this study. All other S. thermophilum group sequences were acquired as part of D’Angelo et al., 2015 (15) or Hume et al., 2015 (13).
Fig. S2.
Estimated age of diversity in the S. thermophilum group. C7-C7a, C3SID-C7, C3SID-C7a, and C3SID-C40 represent between-group genetic distance for associated ITS2 groups, with C3SID being defined as the grouping of Symbiodinium ITS2 type C3 sequences originating from host Siderastrea siderea samples as highlighted in yellow in figure 8A from Thornhill et al., 2014 (17). Numbers above genetic distances represent corresponding lineage diversification ages (Mya) extracted from figure 8A of Thornhill et al., 2014 (17). C27–C40 and S. thermophilum group represent average pairwise genetic distances between the five most divergent pairs between ITS2 groups C27 and C40 and within the S. thermophilum group. Error bars represent 1 SD above and below the average (comparisons of five most divergent pairs only). Values for all genetic distances as well as details of the five most divergent pairs are given in Table S4.
To establish the age and taxonomic position of the S. thermophilum group within clade C, we estimated molecular phylogenies of this group with representatives from Symbiodinium clades A–I, including subclade C representatives, using a suite of single gene markers (Tables S3 and S5) through Bayesian analysis. These markers varied in their ability to resolve between clade C types (Fig. S3 and Table S6). Nine of the 31 S. thermophilum group samples showed identical resolutions across all markers and resolved on the ancestral node in a supermatrix phylogeny (Fig. 1C). All non-S. thermophilum group samples resolved as a strongly supported monophyletic group derived from this ancestral node, whereas those S. thermophilum group samples not resolved on the ancestral node separated as sister groups or individual samples. Given the molecular dating of the radiation of clade C placed in the mid-Miocene, these results provide strong evidence that the S. thermophilum group represents one of the oldest (∼13 Mya) and most genetically diverse groups of extant clade C symbionts (16). Furthermore, estimation of divergences between lineages within the ITS2 type C3 and closely related ITS2 variants according to the psbAncr as being between 2 and 12 My old (17), would suggest that within-group genetic distances of the S. thermophilum group represent evolutionary divergences occurring over at least several million years, a span considerably longer than the age of the PAG (Fig. S2).
Table S5.
Reference sequences used in the single-gene and supermatrix estimations of phylogeny
G. simplexJN558103JN558033JN557890JN557867JN557914JN557966
P. glacialisJN558108JN558036N/AJN557868JN557916JN557968
Fig. S3.
Rooted single-gene and supermatrix estimated phylogenies for Symbiodinium spp. Shown are single-gene and supermatrix estimated phylogenies (Bayesian analysis with nodes support assessed through posterior probabilities) for a suite of A–I clade sequences (gray), including subcladal C sequences (C3, C1, C41, and C39; yellow) and S. thermophilum sequences from the PAG (green), Gulf of Oman (blue), and Red Sea (red). For each phylogeny, a full tree is illustrated on the left, in which the clade C subtree is collapsed. The resolution of this collapsed subtree is shown in detail to the right. Numbers in parentheses represent multiple sequences resolving at the same position and are color coded according to collection site and sequence type (Gulf of Oman, blue; PAG, green; Red Sea, red; reference sequence, yellow). Nodes supported with PPs above 0.8 are not displayed. Nodes with supports below 0.8 are marked with an asterisk.
Table S6.
Phylogenetic differentiation of taxa from the clade C ancestral nodes in single-gene phylogenies
SampleITS2 typenr28Self2coipsbAcdscobcp23SSupermatrixTotal
B334S. thermophilum10010012
BH1418S. thermophilum01000011
BH1630S. thermophilum01000011
BH1641S. thermophilum00010011
ADD003S. thermophilum00010011
ALB004S. thermophilum10000011
ALB020S. thermophilum10000011
KAB047S. thermophilum10000011
OMA071S. thermophilum10000011
BH1659S. thermophilum10000011
B335S. thermophilum10000011
B21561S. thermophilum10000011
B21560S. thermophilum10000011
BH1550S. thermophilum10000011
BH1615S. thermophilum10000011
BH1656S. thermophilum10000011
B21551S. thermophilum10000011
BH21549S. thermophilum10000011
BH1649S. thermophilum10000011
BH1643S. thermophilum10000011
BH1661S. thermophilum10000011
BH1663S. thermophilum10000011
OMD054S. thermophilum00000000
YBA016S. thermophilum00000000
ALB030S. thermophilum00000000
BH1660S. thermophilum00000000
BH1660S. thermophilum00000000
BH1699S. thermophilum00000000
BH1693S. thermophilum00000000
BH1694S. thermophilum00000000
B359S. thermophilum00000000
For each sample, a “1” in a single-gene column denotes the sample was not resolved on the clade C ancestral node of that phylogeny.
“0” denotes resolution on the ancestral node.
The diversity of S. thermophilumpsbAncr was assessed by analyzing sequences from independent samples (Table S7) representing six sites in the PAG and nine sites in the Gulf of Oman and the Red Sea. The significant difference (two-sample t test, P value < 0.01) obtained for group comparisons between within-group genetic distances of PAG sequences (0.039; 112 samples) and Gulf of Oman/Red Sea sequences (0.065; 22 samples) (Table S4) provides evidence that the genetic diversity of S. thermophilum in the PAG is strongly reduced compared with the sites outside of this water body. Similarly, in the southern PAG, the overall Symbiodinium diversity at the species/clade level is lower compared with the western PAG and the Strait of Hormuz, which connects the PAG with the Gulf of Oman (15, 18) (Figs. 1A and 2).
Table S7.
Sequences included in the calculation of within-group (PAG vs. Gulf of Oman/Red Sea) genetic distance
IDCollection siteAccession numberHost taxonIDCollection site*Accession numberHost taxon
Persian/Arabian Gulf sequencesPersian/Arabian Gulf sequences
BH1415DalmaKM458276Porites harrisoniBH1630Umm Al QuwainKP280257P. lutea
BH1686DalmaKP280207P. harrisoniBH1668Umm Al QuwainKP280258P. lutea
BH1448DalmaKM458286P. harrisoniBH1456Umm Al QuwainKM458291P. lutea
BH1413DalmaKM458274P. harrisoniBH1626Umm Al QuwainKP280259P. lutea
BH1684DalmaKP280208P. harrisoniBH1669Umm Al QuwainKP280260P. lutea
BH1414DalmaKM458275P. harrisoniBH1457Umm Al QuwainKP280261P. lutea
BH1685DalmaKP280209P. harrisoniBH1660Umm Al QuwainKP280262P. lutea
BH1450DalmaKM458288Porites luteaBH1392Umm Al QuwainKM458294P. lutea
BH1449DalmaKM458287P. luteaBH1661Umm Al QuwainKP280263P. lutea
BH1689DalmaKP280210P. luteaBH1458Umm Al QuwainKM458292P. lutea
BH1692DalmaKP280211P. luteaBH1427Umm Al QuwainKM458284P. lutea
BH1690DalmaKP280212P. harrisoniBH1663Umm Al QuwainKP280264P. lutea
BH1643DalmaKP280213P. harrisoniBH1679Umm Al QuwainKP280265P. lutea
BH1411DalmaKM458273P. harrisoniBH1688Umm Al QuwainKP280266P. lutea
BH1647DalmaKP280215P. harrisoniBH1675Ras Al KaimahKP280267Porites sp.
BH1691DalmaKP280216P. harrisoniBH1621Ras Al KaimahKP280268Porites sp.
BH1447DalmaKP280217P. harrisoniBH1671Ras Al KaimahKP280269Porites sp.
BH1693DalmaKP280218P. luteaBH1672Ras Al KaimahKP280270Porites sp.
BH1416DalmaKP280219P. harrisoniBH1676Ras Al KaimahKP280271Porites sp.
BH1702SaadiyatKP280220Porites lobataBH1623Ras Al KaimahKP280272Porites sp.
BH1704SaadiyatKP280221P. lobataBH1620Ras Al KaimahKP280273Porites sp.
BH1708SaadiyatKP280222P. lobataBH1624Ras Al KaimahKP280275Porites sp.
BH1356SaadiyatKM458293P. luteaBH1670Ras Al KaimahKP280276Porites sp.
B359SaadiyatKP280223P. luteaBH1673Ras Al KaimahKP280277Porites sp.
BH1422SaadiyatKM458279P. luteaBH1678Ras Al KaimahKP280278Porites sp.
BH1694SaadiyatKP280224P. luteaBH1680Ras Al KaimahKP280279Porites sp.
BH1451SaadiyatKM458289P. lobataBH1677Ras Al KaimahKP280280Porites sp.
BH1695SaadiyatKP280225P. lobataBH1683Ras Al KaimahKP280281Porites sp.
BH1417SaadiyatKM458277P. luteaBH1497Ras Al KaimahKP280282Porites sp.
BH1419SaadiyatKM458278P. luteaBH1625Ras Al KaimahKP280283Porites sp.
BH1640SaadiyatKP280226P. lobataBH1682Ras Al KaimahKP280284Porites sp.
BH1699SaadiyatKP280227P. luteaBH1681Ras Al KaimahKP280285Porites sp.
BH1701SaadiyatKP280228P. luteaBH1674Ras Al KaimahKP280286Porites sp.
BH1705SaadiyatKP280229P. luteaB21549MusandamKP280287P. lobata
BH1706SaadiyatKP280230P. luteaB21550MusandamKP280288P. lobata
B315SaadiyatKP280231P. harrisoniBH1652MusandamKP280289P. lobata
BH1696SaadiyatKP280232P. harrisoniBH1616MusandamKP280290P. lutea
BH1641SaadiyatKP280233P. lobataBH1617MusandamKP280291P. lobata
BH1703SaadiyatKP280234P. harrisoniB21551MusandamKP280292P. lutea
BH1642SaadiyatKP280235P. harrisoniB21552MusandamKP280293P. lutea
BH1698SaadiyatKP280236P. luteaB21553MusandamKP280294P. lutea
BH1487SaadiyatKP280237P. lobataB21554MusandamKP280295P. lutea
BH1418SaadiyatKP280238P. luteaBH1649MusandamKP280296P. lobata
BH1639SaadiyatKP280239P. luteaBH1653MusandamKP280297P. lutea
BH1700SaadiyatKP280240P. harrisoniBH1655MusandamKP280298P. lutea
BH1453SaadiyatKM458290P. lobata 
BH1697SaadiyatKP280241P. lobataGulf of Oman and Red Sea sequences
BH1636Ras GhanadaKP280242P. luteaB341Musandam§KP280299P. lutea
BH1547Ras GhanadaKP280243P. lobataBH1659Musandam§KP280300P. lutea
BH1632Ras GhanadaKP280244P. lobataB21556Musandam§KP280301P. lobata
BH1634Ras GhanadaKP280245P. harrisoniBH1658Musandam§KP280302P. lobata
BH1635Ras GhanadaKP280246P. harrisoniB21557Musandam§KP280303P. lobata
BH1548Ras GhanadaKP280247P. luteaBH1656Musandam§KP280304P. lobata
BH1631Ras GhanadaKP280248P. harrisoniBH1614Musandam§KP280305P. lobata
BH1633Ras GhanadaKP280249P. harrisoniBH1615Musandam§KP280306P. lobata
BH1664Umm Al QuwainKP280250P. luteaB21561FujairahKP280307P. lobata
BH1425Umm Al QuwainKM458282P. luteaBH1550FujairahKP280308P. lobata
BH1665Umm Al QuwainKP280251P. luteaB21560FujairahKP280309P. lobata
BH1662Umm Al QuwainKP280252P. luteaB334FujairahKP280310P. lobata
BH1428Umm Al QuwainKM458285P. luteaB335MuscatKP280311Porites sp.
BH1627Umm Al QuwainKP280253P. luteaADd014Fujairah AAKT156662Galxea
BH1424Umm Al QuwainKM458281P. luteaADd003Fujairah AAKT156654Leptastrea
BH1666Umm Al QuwainKP280254P. luteaALb020Al Lith ALSKT156656Montipora.
BH1628Umm Al QuwainKP280255P. luteaALb030Al Lith ALSKT156660Montipora
BH1426Umm Al QuwainKM458283P. luteaALb004Al Lith ALSKT156655Montipora
BH1629Umm Al QuwainKP280256P. luteaKAb047KAUST KIFKT156657Montipora
BH142Umm Al QuwainKM458280P. luteaOMa071Muscat FIS2KT156661Palythoa
    OMd054Muscat SASKT156658Goniastrea
    YBa016Yanbu Y23KT156659Montipora
Collection site abbreviations are as follows: AA, Al Aqah; ALS, Abu lath Shallow Reef; FIS2, Fahal Island Site 2; KIF, KAUST Inner Fasr; SAS, Saifat Ash Shiekh; Y23, Yanbu 23.
Sequence accessions beginning with KM are from Hume et al., 2015 (13), beginning with KP are from D’Angelo et al., 2015 (15), and beginning with KT are from this study.
From samples collected on the PAG side of the Musandam peninsula.
From samples collected on the Gulf of Oman side of the Musandam peninsula.
The low genetic diversity of the S. thermophilum population in the southern PAG could be indicative of a recent bottleneck event or a founder effect. However, the PAG is well connected to the Gulf of Oman via the dominant inflow of surface water through the Strait of Hormuz (18), and various symbiont types including S. trenchii (synonym type D1a/D1-4), some of which are known to be heat stress-tolerant and to associate with many different coral species (19), are already established in other regions of the PAG and the Strait of Hormuz (15). Together with the fact that Symbiodinium can disperse rapidly over long distances (6, 19, 20), these conditions should promote a rapid homogenization of the symbiont distribution. Hence, the distinct distribution patterns presented in this study render founder or bottleneck effects rather unlikely causes of the low genetic diversity of S. thermophilum in the southern PAG. More plausibly, the genetic uniformity of this symbiont in the hottest coral reef ecosystem in the world may have resulted from a strong positive selection of a few of the most thermally tolerant genotypes from an old lineage with a more widespread but cryptic distribution. This selection pressure may not have resulted only from temperature extremes in the southern PAG, but might also have been influenced by the exceptionally high salinity of this habitat (15). Moreover, it cannot be ruled out that characteristics of today’s S. thermophilum populations were recently influenced by evolutionary processes despite the relatively short time (∼thousands of years) that this symbiont has been exposed to the pressures of the PAG environment.
A contrasting scenario was recently presented for the Caribbean, where the lack of genetic diversity among thermotolerant S. trenchii was interpreted as an indicator of a recent, long-range introduction of coral symbiont species (6). There, the opportunistic/invasive nature of a small founder population promoted its rapid spread to coral communities across the Greater Caribbean.
Although productive coral ecosystems exist in the southern PAG, the diversity of its habitat-forming scleractinian corals (34 species) (21) is substantially lower compared with the adjacent Gulf of Oman (68 species) (11) and the central and northern Red Sea (289 species) (22). Furthermore, in contrast to many other parts of the world, where corals construct reefs by forming vertically growing platforms through calcium carbonate accretion, corals in the southern PAG form only a living veneer over suitable substrates (8). Applying the findings from the PAG to the future of coral reefs elsewhere, it appears that coral–dinoflagellate symbioses may respond rapidly to increasing water temperature by the spread of tolerant symbiont associations, which are normally ecologically rare. Nonetheless, the PAG ecosystem has had millennia to adapt, whereas the adaptation to global warming will need to take place over decades to centuries. As exemplified by the coral communities of the PAG and changes in their composition in response to short-term temperature anomalies, not all species will survive beyond certain changes in the environment (21, 23). Inevitably, the shift toward more extreme environmental conditions on the global scale will be accompanied by a substantial loss of diversity both at the species and within-species level.
Although the failure of corals to build reefs in the PAG has been previously attributed to high-frequency disturbances, high-level bioerosion, and the constant exposure of corals to temperature and salinity extremes (8, 15, 24), the dominance of thermally tolerant coral–dinoflagellate combinations might also contribute to reduced reef accretion as recently exemplified for coral communities elsewhere (46). Because modeling predicts that reef accretion will not easily keep up with projected rates of sea-level rise at present day’s growth rates (25), the question arises whether the thermal adaptation of reef corals might come at the cost of an increased risk of reefs drowning in the rising oceans of the future.
Despite the potential tradeoffs that might be associated with the thermal adaptation of coral communities, the example of the PAG suggests that protecting present-day biodiversity is of upmost importance to provide the largest possible genepool from which more stress-tolerant species and genotypes may emerge and become more common under severe natural selection (26, 27). For coral reef ecosystems, this implies that any loss of biodiversity by causes other than heat stress including habitat destruction, pollution, and eutrophication (2831) will reduce their likelihood of adapting to climate change.


Collection and DNA Extraction of Samples.

Cnidarian samples from 46 genera were collected at 23 reefs in the PAG, the Gulf of Oman, and the Red Sea. Sampling locations were categorized as follows: water bodies (the PAG, the Gulf of Oman, and the Red Sea), sampling regions (made up of one or more reef), and reefs. A detailed list of the sampling locations and number of cnidarians collected at each site can be found in Table S1. All samples were collected by SCUBA (self-contained underwater breathing apparatus) diving with ∼1 cm2 of tissue sampled from the surface of each cnidarian. Samples collected at Eilat were placed into 5 mL of RNAlater, whereas all other samples were flash-frozen in liquid nitrogen before storage at –20 °C.
Genomic DNA (gDNA) was extracted as described for environmental samples in Arif et al., 2014 (32), except for samples collected at Eilat. For Eilat samples, host and symbiont gDNA was extracted using a cetyl trimethylammonium bromide (CTAB) extraction. Before extraction, each of the samples was washed with 96% (vol/vol) ethanol to remove the majority of RNAlater storage buffer to minimize coprecipitation of salts during the DNA precipitation step of the extraction. Samples were then frozen in liquid nitrogen before being added to 1 mL of CTAB extraction buffer [2% (wt/vol) CTAB; 1.4 M NaCl; 0.5% 2-β-mercaptoethanol; 2% (wt/vol) polyvinylpyrrolidone (PVP); 20 mM EDTA; 100 mM Tris⋅HCl, pH 8.0] and beaten using a 5-mm stainless steel ball in a Tissue Lyser II (Qiagen) at maximum speed until the sample was completely homogenized. Samples were incubated at 60 °C for 30 min before three extractions in 1 mL of chloroform:isoamyl alcohol (IAA) (24:1), phenol:chloroform:IAA (25:24:1), and chloroform:IAA (24:1) with centrifugation after each extraction. The supernatant was added to an equal volume of isopropanol before incubation at –20 °C for 2 h. The DNA was pelleted through centrifugation before being washed in 750 µL of 96% ethanol and centrifuged. Supernatant was removed and pellets were dried before suspension in 50 µL of ddH2O. All centrifugation steps were carried out at 20,000 × g for 5 min at 4 °C.

ITS2 Genotyping of Symbiodinium spp. Harbored by Coral Samples.

The Symbiodinium nuclear ribosomal ITS2 region of all samples except those collected at Eilat was sequenced by 454 and MiSeq sequencing as detailed (32). The Symbiodinium ITS2 region of the Eilat-collected samples was sequenced by direct PCR sequencing (services provided by Eurofins MWG) using the internal primer SYM_VAR5.8SII (13) on the 18S-ITS1-5.8S-ITS2-28S amplicon amplified by SYM_VAR-FWD and SYM_VAR_REV as detailed (33), with the exception of an annealing temperature of 56 °C. Results of this sequencing revealed a mix of C15-cluster ITS2 sequences. Given that S. thermophilum group symbionts are characterized by an ITS2 type C3, these samples were excluded from further analysis.

Screening of Corals for Associations with S. thermophilum Group.

To identify the presence of S. thermophilum group symbionts, all corals were screened for the characteristic 8-bp indel sequence described in Hume et al., 2015 (13). To incorporate the possibility of PCR error and the existence of possible genetic variants, sequences 1 bp different (substitution only) from the originally described 8-bp sequences were also included in the results (hereafter referred to as the S. thermo.-indel) as indicative of the S. thermophilum group. Symbiont complements identified as having at least one ITS2 amplicon containing the S. thermo.-indel (hereafter referred to as S. thermo.-indel amplicons) were further categorized according to whether such amplicons made up more than or less than 1% of the total Symbiodinium amplicon sequences found in that organism (Fig. 1A). S. thermo.-indel–containing amplicons made up between 2% and 41% of the C3 type ITS2 amplicons in S. thermophilum samples (i.e., a coral sample hosting 100% S. thermophilum would likely have between 2% and 41% ITS2 amplicons containing the S. thermo.-indel; Fig. S1). As such, the 1% cutoff used in this study could potentially represent a 50% complement of S. thermophilum group symbionts, whereas symbionts containing >15% have a high likelihood of containing a close to pure complement of an S. thermophilum group symbiont.

Verification of S. thermophilum Group by PCR Amplification, Sequencing, and Phylogenetic Analysis of the psbAncr.

To validate the successful identification of the S. thermophilum group by the presence of the S. thermo.-indel, samples from the Gulf of Oman and Red Sea that contained more than 25% clade C ITS2 sequences and in which S. thermo.-indel amplicons made up more than 1% of the clade C sequences had the psbAncr analyzed by direct PCR sequencing as detailed in Hume et al., 2015 (13). Chromatograms were checked manually for miscalls. Chromatograms with multiple peaks were first assessed to determine whether the multiple peaks could be explained by a reading frame shift caused by indels by calling secondary peaks using the software Geneious 5.1.7 ( before attempting to resolve indels using Indelligent 1.2 ( If the multiple peaks could be resolved in this way, the majority sequence was associated with that sample. If multiple peaks were not explained by such “indel analysis,” chromatograms were characterized by no more than two peaks at each nucleotide location, and multiple peak locations clearly showed a predominant and lesser abundance of called nucleotide, then these predominant and lesser calls were used to identify a primary and secondary sequence, respectively. In this case, the primary sequence was associated with the sample. In cases where multiple-peaked chromatograms could not be explained by indel analysis or by identifying primary and secondary sequences, the sample genotype was not used in further analysis (1 out of 10 samples).
Nine samples that successfully returned psbAncr sequences were aligned manually with additional sequences from the psbAncr alignment created by Hume et al., 2015 (13) that contained sequences from corals collected within the PAG and C3 radiation sequences (17) collected external to the PAG.
Phylogenetic analysis was conducted by Bayesian inference using Mr. Bayes 3.2.2 ( Phylogenies were estimated using the Jukes–Cantor (JC) model with a gamma-shaped distribution (+G) with invariable sites (I) (according to Akaike Information Criterion using MEGA6; Markov chain Monte Carlo (MCMC) analyses were run for 2.0 × 106 generations (SDs of split frequencies < 0.05), sampling every 1,000 generations. A relative burn-in of 0.25 was used in calculating a 50% majority rule consensus tree.
To compare psbAncr genetic diversity between the S. thermophilum group and the two most divergent ITS2 types (C40 and C27) that resolve within the C3-radiation psbAncr phylogeny, as well as between S. thermophilum group sequences found within and external to the PAG, pairwise genetic distances and within-group genetic distance were calculated in MEGA6 using the JC model +G (Table S4). Variance was determined to be equal (F test) before conducting a two sample Student’s t test to compare the within-group genetic distances of the samples from sites internal and external to the PAG.

Taxonomic Position of S. thermophilum Group Within Symbiodinium Clade C.

To elucidate the taxonomic position of the S. thermophilum group within clade C, a selection of S. thermophilum group, ITS2 type C3, and C41 and C39 (two of the top four numerically common subclades) harboring corals (including some corals under culture at the Coral Reef Laboratory Experimental Mesocosm Facility) (34) had their symbiont complement genotyped with six additional genetic markers (35): the nuclear ribosomal large subunit (nr28S), the nuclear elongation factor 2 (elf2), the chloroplastic ribosomal large subunit (cp23S) domain V, the coding region of the plastid-encoded photosystem II protein D1 (psbAcds), the mitochondrial cytochrome oxidase I (coi), and the mitochondrial cytochrome b (cob). To assess fine-scale taxonomic resolution, the psbAncr was also amplified.
Specifically, the following coral samples underwent this additional genotyping: all samples in the Gulf of Oman and the Red Sea characterized as S. thermophilum by psbAncr genotype and containing >99% clade C ITS2 sequences (eight samples); a selection of 23 samples collected in the PAG as part of studies by Hume et al., 2015 (13) and D’Angelo et al., 2015 (15), representing samples collected over >400 km within the PAG and as resolving in different positions within the psbAncr phylogeny of D’Angelo et al., 2015 (15); samples collected in the Red Sea and Gulf of Oman harboring ITS2 type C3 as their numerically dominant ITS2 amplicon and containing no S. thermo.-indel amplicons (three samples; OMD001, OMD002, and YBA008; Table S3); three ITS2-type C3-harboring Euphyllia spp. corals currently in culture at the Coral Reef Laboratory Experimental Mesocosm Facility (34) but originating from Indo-Pacific waters in proximity to Bali (EU2, EU3, and EU4; Table S3); and finally, four corals containing predominant ITS2 variants for C41 and C39 (representing the first and fourth most common ITS2 variants sampled, respectively) collected in the Red Sea and the Gulf of Oman (Table S3).
All PCR conditions were as for the SYM_VAR_FWD/SYM_VAR_REV primer pair with cycles as detailed in Pochon et al., 2014 (35), except for the psbAncr region that was amplified according to Hume et al., 2015 (13). Sequences were attained through direct PCR sequencing, services provided by Eurofins, using forward (elf2, psbAcds, coi, and cob) and reverse (nr28S and cp23S) primers. Sequences from this study were added to a selection of reference sequences (Table S5) representing members from clades A–I, including subcladal C1, C15, C90, and C91, as well as sequence collections from Gymnodinium simplex and Polarella glacialis as outgroups.
Sequences returned from the six additional genetic markers (i.e., not psbAncr) were aligned in MEGA 6 with the ClustalW algorithm and checked by eye. Hypervariable regions that prevented robust alignment were removed from the cp23S alignment sensu Pochon et al., 2006 (16). Phylogenies were estimated both from individual markers and from a concatenated supermatrix of all six markers. Phylogenies were estimated by Bayesian Inference in Mr. Bayes 3.2.2 using the following nucleotide substitution models: nr28S, Kimura 2-Parameter (K2) +G; Elf2, K2 +G +I; cp23S, Hasegawa Kishino Yano (HKY) +G; psbAcds, Generalized Time Reversible +G; coi, HYK +G; cob, HKY +G. The supermatrix analysis was partitioned with the separate nucleotide models being used for each marker’s region. MCMC analyses were run for 1.0 × 106 generations, sampling every 500 generations. A relative burn-in of 0.25 was used in calculating a 50% majority rule consensus tree. Alignments of the psbAncr sequences returned from the ITS2 type C3 (non-S. thermo.-indel–containing), C41, and C39 samples were not possible between ITS2 types from this study and with previous alignments by Hume et al., 2015 (13) (C3/S. thermophilum radiation) and Thornhill et al., 2014 (17) (C1 radiation) due to the dissimilarity of the sequences.

Data Availability

Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. KR996268–KR996464 and KT156647–KT156665).


We appreciate the help of Cornelia Roder, Sergey Dobretsov, Julia Schnetzer, Todd LaJeunesse, and Drew Wham with sample collection. A. Al-Hemeri (UAE Federal Environment Agency), A. Al-Cibahy (Environment Agency of Abu Dhabi), and the Oman Ministry of Environment & Climate Affairs kindly provided Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) export permits (no. 09FEA555) and collection permits. We acknowledge Tropical Marine Centre (London) and Tropic Marin (Wartenberg) for sponsoring the Coral Reef Laboratory at the University of Southampton. We thank the NYU Abu Dhabi Institute for supporting the 2012/2013 field workshops during which samples for this study were collected and the Interuniversity Institute for Marine Sciences in Eilat for field work support. The study was funded by Natural Environment Research Council Grant NE/K00641X/1 (to J.W.), the European Research Council under the European Union’s Seventh Framework Programme Grant FP7/2007-2013/ERC Grant Agreement 311179 (to J.W.), the King Abdullah University of Science and Technology (C.R.V.), and Israel Science Foundation Grant 341/12, United States Agency for International Development/Middle East Regional Cooperation (USAID/MERC) No. M32-037 (to Y.L.).

Supporting Information

Supporting Information (PDF)
Supporting Information


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Information & Authors


Published in

Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 113 | No. 16
April 19, 2016
PubMed: 27044109


Data Availability

Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. KR996268–KR996464 and KT156647–KT156665).

Submission history

Published online: April 4, 2016
Published in issue: April 19, 2016


  1. Persian/Arabian Gulf
  2. adaptation
  3. coral
  4. Symbiodinium
  5. climate change


We appreciate the help of Cornelia Roder, Sergey Dobretsov, Julia Schnetzer, Todd LaJeunesse, and Drew Wham with sample collection. A. Al-Hemeri (UAE Federal Environment Agency), A. Al-Cibahy (Environment Agency of Abu Dhabi), and the Oman Ministry of Environment & Climate Affairs kindly provided Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) export permits (no. 09FEA555) and collection permits. We acknowledge Tropical Marine Centre (London) and Tropic Marin (Wartenberg) for sponsoring the Coral Reef Laboratory at the University of Southampton. We thank the NYU Abu Dhabi Institute for supporting the 2012/2013 field workshops during which samples for this study were collected and the Interuniversity Institute for Marine Sciences in Eilat for field work support. The study was funded by Natural Environment Research Council Grant NE/K00641X/1 (to J.W.), the European Research Council under the European Union’s Seventh Framework Programme Grant FP7/2007-2013/ERC Grant Agreement 311179 (to J.W.), the King Abdullah University of Science and Technology (C.R.V.), and Israel Science Foundation Grant 341/12, United States Agency for International Development/Middle East Regional Cooperation (USAID/MERC) No. M32-037 (to Y.L.).


This article is a PNAS Direct Submission.



Benjamin C. C. Hume
Coral Reef Laboratory, Ocean and Earth Science, University of Southampton, Southampton SO14 3ZH, United Kingdom;
Christian R. Voolstra
Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Saudi Arabia;
Chatchanit Arif
Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Saudi Arabia;
Cecilia D’Angelo
Coral Reef Laboratory, Ocean and Earth Science, University of Southampton, Southampton SO14 3ZH, United Kingdom;
Institute for Life Sciences, University of Southampton, Southampton SO17 1BJ, United Kingdom;
John A. Burt
Marine Biology Laboratory, Centre for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi 129188, United Arab Emirates;
Gal Eyal
Department of Zoology, Tel Aviv University, Tel Aviv 6997801, Israel;
The Interuniversity Institute for Marine Sciences in Eilat, Eilat 8810369, Israel
Yossi Loya
Department of Zoology, Tel Aviv University, Tel Aviv 6997801, Israel;
Jörg Wiedenmann1 [email protected]
Coral Reef Laboratory, Ocean and Earth Science, University of Southampton, Southampton SO14 3ZH, United Kingdom;
Institute for Life Sciences, University of Southampton, Southampton SO17 1BJ, United Kingdom;


To whom correspondence should be addressed. Email: [email protected].
Author contributions: B.C.C.H., C.R.V., and J.W. designed research; B.C.C.H., C.R.V., and C.A. performed research; B.C.C.H., C.R.V., J.A.B., G.E., Y.L., and J.W. performed field work; B.C.C.H., C.R.V., C.A., C.D., and J.W. analyzed data; and B.C.C.H., C.D., and J.W. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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    Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change
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