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Comparative Study
. 2021 Aug 16;11(1):16568.
doi: 10.1038/s41598-021-95872-0.

Phylogeography, colouration, and cryptic speciation across the Indo-Pacific in the sea urchin genus Echinothrix

Simon E Coppard  1   2 , Holly Jessop  3 , Harilaos A Lessios  3
Affiliations
Comparative Study

Phylogeography, colouration, and cryptic speciation across the Indo-Pacific in the sea urchin genus Echinothrix

Simon E Coppard et al. Sci Rep. .

Abstract

The sea urchins Echinothrix calamaris and Echinothrix diadema have sympatric distributions throughout the Indo-Pacific. Diverse colour variation is reported in both species. To reconstruct the phylogeny of the genus and assess gene flow across the Indo-Pacific we sequenced mitochondrial 16S rDNA, ATPase-6, and ATPase-8, and nuclear 28S rDNA and the Calpain-7 intron. Our analyses revealed that E. diadema formed a single trans-Indo-Pacific clade, but E. calamaris contained three discrete clades. One clade was endemic to the Red Sea and the Gulf of Oman. A second clade occurred from Malaysia in the West to Moorea in the East. A third clade of E. calamaris was distributed across the entire Indo-Pacific biogeographic region. A fossil calibrated phylogeny revealed that the ancestor of E. diadema diverged from the ancestor of E. calamaris ~ 16.8 million years ago (Ma), and that the ancestor of the trans-Indo-Pacific clade and Red Sea and Gulf of Oman clade split from the western and central Pacific clade ~ 9.8 Ma. Time since divergence and genetic distances suggested species level differentiation among clades of E. calamaris. Colour variation was extensive in E. calamaris, but not clade or locality specific. There was little colour polymorphism in E. diadema.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Phylogeny of Echinothrix based on concatenated 16S, ATPase-6, ATPase-8, 28S and Calpain-7 intron sequences reconstructed with RAxML, rooted on Astropyga pulvinata. Clade credibility values > 85% of Bayesian (first number next to node) and > 75% of Maximum Likelihood (second number) reconstruction are shown, –: < 75%. Scale bar reflects number of changes per site, photos show colour morphs present in each molecular clade.
Figure 2
Figure 2
Distribution of clades of Echinothrix. Letter refers to locality, colour to the clade. E.P.B. = Eastern Pacific Barrier. A: Dahab, Egypt, Gulf of Aqaba (28.5236° N, 34.5301° E); B: Muscat, Oman, Gulf of Oman (23.9871° N, 58.1859° E); C: Al Fahal Island, Gulf of Oman (23.6822° N, 58.5020° E); D: Ari Atoll, Maldives (3.8825° N, 72.8340° E); E: Kanyakumari, India (8.0798° N, 77.5276° E); F: Zanzibar Island, Tanzania (6.1374° S, 39.1684° E); G: Amirante Islands, Seychelles (6.1554° S, 52.8513° E); H: Seychelles (4.7178° S, 55.4260° E); I: Réunion Island (21.0271° S, 55.7966° E); J: Tuléar, Madagascar (23.3833° S, 43.6667° E); K: Sodwana Bay, South Africa (27.5187° S, 32.6915° E); L: Sesoko Island, Japan (26.6333° N, 127.8667° E); M: Akajima Island, Japan (26.2042° N, 127.2876° E); N: Kyushu, Japan (31.0553° N, 130.3640° E); O: Ishigaki Island, Japan (24.46307° N, 124.2747° E); P: Kenting, Taiwan (21.9447° N, 120.7750° E); Q: Redang Island, Malaysia (5.7893° N, 103.0184° E); R: Tioman Island, Malaysia (2.8162° N, 104.1543° E); S: Cocos (Keeling) Islands (12.1889° S, 96.8197° E); T: Motupore Island, Papua New Guinea (9.5233° S, 147.2860° E); U: Pago Bay, Guam (13.4207° N, 144.7940° E); V: Noumea, New Caledonia (22.2959° S, 166.4370° E); W: Majuro Atoll, Marshall Islands (7.0915° N, 171.3772° E); X: Suva Lagoon, Fiji (18.1777° S, 178.4875° E); Y: Namatakula, Fiji (18.2372° S, 177.7845° E); Z: Upola Island, Samoa (13.7835° S, 171.8589° W); α: Johnston Atoll (16.7405° N, 169.5074° W); β: Kingman Reef (6.4188° N, 162.3655° W); Ω: Rarotonga, Cook Islands (21.2142° S, 159.7126° W); Δ: Maharepa, Moorea (17.4758° S, 149.7929° W); Γ: Kiritimati Island, Kiribati (Line Islands) (1.9213° N, 157.4442° W); Θ: Oahu, Hawaii (21.2951° N, 157.8830° W); Π: Hawaii Island, Hawaii (19.7308° N, 154.9915° W); Ξ: Maui, Hawaii (20.6267° N, 156.1925° W); Σ: Clipperton Island (10.2862° N, 109.2124° W); Φ: Isla del Coco, Costa Rica (5.5360° N, 87.0244° W). The outline of this map was downloaded from Dmthoth, CC BY-SA 3.0, via Wikimedia Commons and edited in Photoshop Elements 2020.
Figure 3
Figure 3
Bayesian estimates of median molecular divergence times (median dates next to node) based on concatenated ATPase-6 andATPase-8, as derived from analysis using BEAST and calibrated using minimum age of genus and substitution rates from Diadema, a confamilial genus. Bars indicate 95% Highest Posterior Density (HPD) limits. Ages of stages and epoch series based on International Commission on Stratigraphy stratigraphic chart v.2020/01 (Messin. = Messinian, Zancl. = Zanclean, Piac. = Piacenzian, G. = Gelasian, Calabr. = Calabrian, Pleisto. = Pleistocene).
Figure 4
Figure 4
Median joining haplotype network based on mitochondrial ATPase6, ATPase8 and 16S. Constructed in PopART with reticulation tolerance set to zero.
Figure 5
Figure 5
Median joining haplotype network based on 28S rDNA and intron of Calpain-7 nuclear DNA. Constructed in PopART with reticulation tolerance set to zero.
Figure 6
Figure 6
Green median regions of interambulacra in E. calamaris. (a) Close-up of median region, (b) white colour morph with green median regions (haplotype = clade 1, Namatakula, Fiji 13), (c) red colour morph with only red pigmentation in epithelial tissues of interambulacra (haplotype = clade 1, Namatakula, Fiji 22).
Figure 7
Figure 7
Collection localities of Echinothrix used in this study. Letter refers to locality (see Fig. 2 legend), number to the sample size, and colour to species. The outline of this map was downloaded from Dmthoth, CC BY-SA 3.0, via Wikimedia Commons and edited in Photoshop Elements 2020.
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