Bronstein O et al. (2017), Cryptic speciation in pan-tropical sea urchins:...

ECB-ART-45640

Sci Rep 2017 Jul 20;71:5948. doi: 10.1038/s41598-017-06183-2.

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Cryptic speciation in pan-tropical sea urchins: a case study of an edge-of-range population of Tripneustes from the Kermadec Islands.

Bronstein O , Kroh A , Tautscher B , Liggins L , Haring E .

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Tripneustes is one of the most abundant and ecologically significant tropical echinoids. Highly valued for its gonads, wild populations of Tripneustes are commercially exploited and cultivated stocks are a prime target for the fisheries and aquaculture industry. Here we examine Tripneustes from the Kermadec Islands, a remote chain of volcanic islands in the southwest Pacific Ocean that mark the boundary of the genus'' range, by combining morphological and genetic analyses, using two mitochondrial (COI and the Control Region), and one nuclear (bindin) marker. We show that Kermadec Tripneustes is a new species of Tripneustes. We provide a full description of this species and present an updated phylogeny of the genus. This new species, Tripneustes kermadecensis n. sp., is characterized by having ambulacral primary tubercles occurring on every fourth plate ambitally, flattened test with large peristome, one to two occluded plates for every four ambulacral plates, and complete primary series of interambulacral tubercles from peristome to apex. It appears to have split early from the main Tripneustes stock, predating even the split of the Atlantic Tripneustes lineage. Its distinction from the common T. gratilla and potential vulnerability as an isolated endemic species calls for special attention in terms of conservation.

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Species referenced: Echinodermata
Genes referenced: bindin cse1l LOC100887844 LOC115925415 LOC582915

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	Figure 1. Map of the southeastern Indian Ocean and southwestern Pacific showing the location of the Kermadec Islands. Inset shows map of Raoul Island. Stars indicate sample collection localities of Tripneustes kermadecensis n. sp. The map is based on the Wikimedia Commons public domain map file BlankMap-World6.svg (https://commons.wikimedia.org/wiki/File:BlankMap-World6.svg) and edited using the cross-platform geographic information system QGIS v. 2.8.2 (Quantum GIS Development Team (2016). Quantum GIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.osgeo.org).
	Figure 2. External appendages of Tripneustes kermadecensis n. sp. Globiferous (Aâ€“E) and ophicephalous (Fâ€“J) pedicellariae in lateral (B,G), external (C,H), and internal views (D,E,I,J); (Kâ€“M): secondary spine with details of surface sculpture close to base (K) and close to tip (L). All from paratype NHMW-Geo 2017/0016/0001; (A,Eâ€“H,J) derive from the aboral side of the animal, (Bâ€“D,I,Kâ€“M) from the oral side.
	Figure 3. External appearance (A,B) and corona (Câ€“E) of Tripneustes kermadecensis n. sp. Aboral (A,C), oral (B,E), and lateral views (D) of the holotype (AIM MA73563). Images (A and B) were taken from specimens submerged in water for better representation of soft tissue organs and true colours.
	Figure 4. Ambital ambulacral plating of Tripneustes species. (A) Tripneustes gratilla gratilla (TDâ€‰=â€‰90.7â€‰mm; Phatthaya, Thailand; NHMW-Geo 2011/0352/0003); (B) Tripneustes gratilla elatensis (TD ~95â€‰mm; Ras Abusoma, Safaga, Egypt; NHMW-Geo 2008z0004/0012); (C) Tripneustes kermadecensis n. sp. (TDâ€‰=â€‰94.5â€‰mm; Meyer Islands, New Zealand; holotype AIM MA73563); (D) Tripneustes ventricosus (TD ~100â€‰mm; Roatan Island, Honduras; NHMW-Geo 2008z0167/0016). Plates occluded from perradial suture highlighted in red.
	Figure 5. Phylogenetic tree reconstruction of Tripneustes COI sequences. The BI tree is based on 44 haplotypes, 531â€‰bp long, representing all extant species of Tripneustes and is rooted with Lytechinus variegatus (not shown). Supporting values (>0.9 posterior probabilities and >60% ML bootstrap values) are shown above the nodes. The colors of the specimen labels correspond to: Dark green â€“ T. g. gratilla, Red â€“ T. g. elatensis, Light green â€“ T. depressus, Blue â€“ T. ventricosus, and Orange â€“ T. kermadecensis n. sp. Details on the sequences used for this tree are given in the Supplementary TablesÂ S1 and S2.
	Figure 6. Phylogenetic tree reconstruction of Tripneustes control region (CR) sequences. The BI tree is based on 19 unique haplotypes, 446â€‰bp long, representing T. kermadecensis n. sp., T. g. elatensis and T. g. gratilla, and is rooted on Hemicentrotus pulcherrimus and Strongylocentrotus droebachiensis (GenBank accession numbers KC490911, EU054306 and NC009940, respectively). Color code as in Fig.Â 5. Supporting values (>0.9 posterior probabilities and >60% ML bootstrap values) are shown above the nodes. Clades A (comprising T. kermadecensis n. sp.), and B (comprising both T. g. gratilla and T. g. elatensis) are discussed in the text. Details on the sequences used for this tree are given in the Supplementary TablesÂ S1 and S2.
	Figure 7. Tripneustes COI Median-joining haplotype network. The network comprises 339 sequences, 448â€‰bp long, generated during the current study as well as comparable Tripneustes COI sequences available from GenBank (for details see Supplementary TablesÂ S1 and S2). Color code as in Fig.Â 5. Bars indicate the number of substitutions between nodes. The frequency of each haplotype is indicated by size of the circles (see key, top right).
	Figure 8. Phylogenetic tree reconstruction of Tripneustes bindin sequences. (A) Unrooted BI tree of 1256â€‰bp long Tripneustes bindin sequences including exons 1 and 2 (excluding the glycine-rich repeat in exon 1; see main text for details) and parts of the intron (excluding the 169â€‰bp region identified as transposon, respectively inverted repeat; see main text for details). The tree reconstruction is based on 54 unique haplotypes representing all extant species of Tripneustes. Supporting values (>0.9 posterior probabilities and >60% ML bootstrap values) are shown above the nodes. Color code as in Fig.Â 5. T. g. gratilla clades (Aâ€“C) are discussed in the text. Details on the sequences used for this tree are given in the Supplementary TablesÂ S1 and S2. (B) Unique sequence features mapped on the bindin tree topology (position of root inferred from COI tree in Fig.Â 5). Numbers above branches represent number of gylcine rich repeats, names below branches provide information on the nature of insert at the 5â€² end of the bindin intron (see text for details). Note that the transposon DNA-1-2_SP is inserted in normal orientation in T. g. gratilla clades A and B, but as reverse complement in T. ventricosus and T. g. gratilla clade C.
	Figure 9. Phylogenetic tree reconstruction of concatenated Tripneustes sequences. The mid-point rooted BI tree reconstruction is based on 19 unique haplotypes, 2828â€‰bp long, representing T. kermadecensis n. sp., T. g. elatensis and T. g. gratilla. Sequences were concatenated from alignable segments of the mitochondrial markers (COI and CR) as well as the nuclear marker bindin (including exons 1, 2 and the intron). Color code as in Fig.Â 5. Supporting values (>0.9 posterior probabilities and >60% ML bootstrap values) are shown near the nodes. Details on the sequences used for this tree are given in the Supplementary TableÂ S1.
	Figure 10. Peristome (A) and apical disc (B) of Tripneustes kermadecensis n. sp. Paratype (NHMW-Geo 2017/0016/0001).
	Figure 11. Distal compass ends of Tripneustes kermadecensis n. sp. (A) Paratype NHMW-Geo 2017/0016/0001, (B) holotype AIM MA73563, and (C) AIM MA73564.
	Figure 12. Tubefeet spicules of Tripneustes species. (A,D,E,H) Tripneustes kermadecensis n. sp. (Meyer Islands, New Zealand; paratype MA 121530.10); (B,F,I) Tripneustes gratilla gratilla (Philippines; CAS 187193); (C,G,J) Tripneustes gratilla elatensis (Aquaba, Jordan; NHMW NHMW-EV 20454). Top row: terminal disc; middle row: spicules from distal half of tube foot; Bottom row: spicules from base of tube foot. All images are backscatter electron images. 100â€‰Âµm scale bar valid for images A to C; 50â€‰Âµm scale bar for imaged (D) through (J).

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Bowen, The origins of tropical marine biodiversity. 2013, Pubmed