The potential role of temperate Japanese regions as refugia for the coral Acropora hyacinthus in the face of climate change

As corals in tropical regions are threatened by increasing water temperatures, poleward range expansion of reef-building corals has been observed, and temperate regions are expected to serve as refugia in the face of climate change. To elucidate the important indicators of the sustainability of coral populations, we examined the genetic diversity and connectivity of the common reef-building coral Acropora hyacinthus along the Kuroshio Current, including recently expanded (<50 years) populations. Among the three cryptic lineages found, only one was distributed in temperate regions, which could indicate the presence of Kuroshio-associated larval dispersal barriers between temperate and subtropical regions, as shown by oceanographic simulations as well as differences in environmental factors. The level of genetic diversity gradually decreased towards the edge of the species distribution. This study provides an example of the reduced genetic diversity in recently expanded marginal populations, thus indicating the possible vulnerability of these populations to environmental changes. This finding underpins the importance of assessing the genetic diversity of newly colonized populations associated with climate change for conservation purposes. In addition, this study highlights the importance of pre-existing temperate regions as coral refugia, which has been rather underappreciated in local coastal management

A phylogeny of the family Poritidae (Cnidaria, Scleractinia) based on molecular and morphological analyses.

The family Poritidae formerly included 6 genera: Alveopora, Goniopora, Machadoporites, Porites, Poritipora, and Stylaraea. Morphologically, the genera can be differentiated based on the number of tentacles, the number of septa and their arrangement, the length of the polyp column, and the diameter of the corallites. However, the phylogenetic relationships within and between the genera are unknown or contentious. On the one hand, Alveopora has been transferred to the Acroporidae recently because it was shown to be more closely related to this family than to the Poritidae by previous molecular studies. On the other hand, Goniopora is morphologically similar to 2 recently described genera, Machadoporites and Poritipora, particularly with regard to the number of septa (approximately 24), but they have not yet been investigated at the molecular level. In this study, we analyzed 93 samples from all 5 poritid genera and Alveopora using 2 genetic markers (the barcoding region of the mitochondrial COI and the ITS region of the nuclear rDNA) to investigate their phylogenetic relationships and to revise their taxonomy. The reconstructed molecular trees confirmed that Alveopora is genetically distant from all poritid genera but closely related to the family Acroporidae, whereas the other genera are genetically closely related. The molecular trees also revealed that Machadoporites and Poritipora were indistinguishable from Goniopora. However, Goniopora stutchburyi was genetically isolated from the other congeneric species and formed a sister group to Goniopora together with Porites and Stylaraea, thus suggesting that 24 septa could be an ancestral feature in the Poritidae. Based on these data, we move G. stutchburyi into a new genus, Bernardpora gen. nov., whereas Machadoporites and Poritipora are merged with Goniopora

Map of sampling locations for this study.

<p>A: Indian and Pacific Ocean, B: southern Red Sea, Gulf of Tadjoura and Gulf of Aden; C–E: main island of Japan and Ryukyu archipelago. AD: Aden, Yemen, AK: Akajima Island, Japan, AM: Amakusa, Japan, AO: Amami-Oshima, Japan, BA: Bir Ali, Yemen, BU: Al Mukallah, Yemen, DJ: Djibouti, IK: Iki Island, Japan, IR: Iriomote Island or Hatoma Island, Japan, IS: Ishigaki Island or Taketomi Island, Japan, KA: Kamaran Islands, Yemen, KK: Kikai Island, Japan KS: Kushimoto, Japan, MI: Miyako Island, Japan, MY: Mayotte Island, France, OT: Ootuki, Japan, OU: Oura bay, Japan, PEN: Song song Island, Malaysia, SO: Suou-Oshima, Japan, SR: Shirahama, Japan, SS: Sesoko Island, Japan, TN: Tanegashima Island, Japan, TR: Nakanoshima Island, Japan</p

Molecular phylogenetic relationships of the family Poritidae and related families based on mitochondrial COI sequences.

<p>Numbers on/below main branches show bootstrap values (>50%) in ML and NJ analyses, and Bayesian posterior probability (>0.8). Stars show specimens collected from western Indian Ocean, and triangles show ones collected from Malacca Strait. Sample codes or accession numbers are shown after species names (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0098406#pone-0098406-t001" target="_blank">Table 1</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0098406#pone.0098406.s006" target="_blank">Table S3</a>). Grey in color for <i>Alveopora</i>, green for <i>Porites</i>, purple for <i>Stylaraea</i>, blue for ‘<i>Poritipora</i>’, and orange for ‘<i>Machadoporites</i>’. <i>Goniopora</i> is shown by bars in black. <i>Bernardpora</i> is shown by bar in red.</p

Comparison of the diagnostic morphological characters between the previous classifications and the classification used in this study in the family Poritidae.

<p>Comparison of the diagnostic morphological characters between the previous classifications and the classification used in this study in the family Poritidae.</p

Polyp and skeleton characters of <i>Stylaraea punctata</i> and <i>Bernardpora stutchburyi</i>.

<p>A–B. <i>Stylaraea punctata</i> AK93, MUFS YFK1244, Akajima Island, Japan. C–D. <i>S. punctata</i> AK92, MUFS YFK1243, Akajima Island, Japan. E–H. <i>Bernardpora stutchburyi</i> SS21G MUFS YFK220, Sesoko, Japan. Living specimen for whole colonies (A, E) and polyps (B, F), corallite structures (C, G), and star-shaped columella (D, H). Arrows show columella. Bars show 1 mm for (C) and (G), and 0.5 mm for (D) and (H).</p

List of samples examined in this study and the accession numbers of DNA sequences.

<p>List of samples examined in this study and the accession numbers of DNA sequences.</p

Molecular phylogenetic relationships of genera of the Poritidae except of <i>Alveopora</i> based on ITS sequences.

<p>Letter (a, b, c, d) after sample code indicates that different alleles were obtained from a single coral sample by cloning. Numbers on/below main branches show bootstrap values (>50%) in ML and NJ analyses, and Bayesian posterior probability (>0.8). Stars show specimens collected from western Indian Ocean, and triangles show ones collected from Malacca Strait. Sample codes or accession numbers are shown after species names (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0098406#pone-0098406-t001" target="_blank">Table 1</a>). Green in color for <i>Porites</i>, purple for <i>Stylaraea</i>, blue for ‘<i>Poritipora</i>’, orange for ‘<i>Machadoporites</i>’, red for <i>Bernardpora,</i> and black for <i>Goniopora</i>.</p

Polyp and skeleton characters of ‘<i>Poritipora</i>’ <i>paliformis</i>, ‘<i>Machadoporites</i>’ <i>tantillus</i> and morphologically related species.

<p>Living specimens and corallite structures for <i>P. paliformis</i> IS48, MUFS YFK959, Taketomi, Japan (A, B) and <i>M. tantillus</i> AD068, UNIMBI AD068, Aden, Yemen (E, F), respectively. Corallite structures of holotypes of <i>P. paliformis</i> MTQ G55857 (C) and <i>Goniopora minor</i> NHMUK 1934.5.14.436 No. 56 (D). Corallites structures of <i>G. burgosi</i> OT6, MUFS YFK286, Otsuki, Japan (G) and <i>G. pendulus</i> TN11, MUFS YFK243, Tanegashima, Japan (H) from Japan water, as examples of corallites with less 24 septa. Bars show 1 mm.</p

Data from: The potential role of temperate Japanese regions as refugia for the coral Acropora hyacinthus in the face of climate change

As corals in tropical regions are threatened by increasing water temperatures, poleward range expansion of reef-building corals has been observed, and temperate regions are expected to serve as refugia in the face of climate change. To elucidate the important indicators of the sustainability of coral populations, we examined the genetic diversity and connectivity of the common reef-building coral Acropora hyacinthus along the Kuroshio Current, including recently expanded (<50 years) populations. Among the three cryptic lineages found, only one was distributed in temperate regions, which could indicate the presence of Kuroshio-associated larval dispersal barriers between temperate and subtropical regions, as shown by oceanographic simulations as well as differences in environmental factors. The level of genetic diversity gradually decreased towards the edge of the species distribution. This study provides an example of the reduced genetic diversity in recently expanded marginal populations, thus indicating the possible vulnerability of these populations to environmental changes. This finding underpins the importance of assessing the genetic diversity of newly colonized populations associated with climate change for conservation purposes. In addition, this study highlights the importance of pre-existing temperate regions as coral refugia, which has been rather underappreciated in local coastal management