Elucidation of the speciation history of three sister species of crown-of-thorns starfish (Acanthaster spp.) based on genomic analysis

Abstract

The crown-of-thorns starfish (COTS) is a coral predator that is widely distributed in Indo-Pacific Oceans. A previous phylogenetic study using partial mitochondrial sequences suggested that COTS had diverged into four distinct species, but a nuclear genome-based analysis to confirm this was not conducted. To address this, COTS species nuclear genome sequences were analyzed here, sequencing Indian Ocean (NIO) and Red Sea (RS) species genomes for the first time, followed by a comparative analysis with the Pacific Ocean (PO) species. Phylogenetic analysis and ADMIXTURE analysis revealed clear divergences between the three COTS species. Furthermore, within the PO species, the phylogenetic position of the Hawaiian sample was further away from the other Pacific-derived samples than expected based on the mitochondrial data, suggesting that it may be a PO subspecies. The pairwise sequentially Markovian coalescent model showed that the trajectories of the population size diverged by region during the Mid-Pleistocene transition when the sea-level was dramatically decreased, strongly suggesting that the three COTS species experienced allopatric speciation. Analysis of the orthologs indicated that there were remarkable genes with species-specific positive selection in the genomes of the PO and RS species, which suggested that there may be local adaptations in the COTS species.

A new species of crown-of-thorns sea star, Acanthaster benziei sp. nov. (Valvatida: Acanthasteridae), from the Red Sea

“…3). There is full agreement with initial results that proposed species distinction of the Red Sea clade based on COI data alone (Vogler et al 2008), recently corroborated by nuclear genome analyses (Yuasa et al 2021). The molecular-based species distinction of A. benziei sp.…”

“…These four clades were proposed to represent four species, each with a distinct and largely non-overlapping distribution across the Indo-Pacific region: one from the Red Sea (RS), one from the southern Indian Ocean (SIO), one from the northern Indian Ocean (NIO), and one from the Pacific Ocean (PO) (Vogler et al 2008, see also Vogler et al 2012Vogler et al , 2013. This separation of the RS, NIO and PO species has also been confirmed using a nuclear genome-based analysis, however, the SIO could not be included due to sampling difficulties (Yuasa et al 2021). An in-depth review of the original literature and species descriptions, which aimed to allocate species names to these four genetic clades (Haszprunar & Spies 2014), concluded that A. planci is the valid name for the northern Indian Ocean species, Acanthaster mauritiensis (de Loriol 1885) for the southern Indian Ocean species, and Acanthaster cf.…”

“…The original haplotype dataset of Vogler et al (2008) was then supplemented with the new sequences from the type series of A. benziei sp. nov. from Saudi Arabia (Red Sea), as well as five samples from Israel (Red Sea) extracted from full mitochondrial genome sequences from Yuasa et al (2021) (accession numbers LC566218-LC566222). The 632 bp alignment (available in the supplementary material) of 84 sequences was processed in Geneious Prime 2019 (http://www.geneious.com).…”

“…In addition, a neighbour-joining (NJ) clustering of COI sequences with bootstrapping (1000 replicates) was performed in Geneious Prime 2019 using the best-fit Tamura-Nei model. Alignment positions of the partial COI sequences used here refer to positions in the full mitochondrial genome sequences from Yuasa et al (2021). The four newly generated sequences of the A. benziei type series are deposited in the European Nucleotide Archive (Accession Numbers OW970326 -OW970329).…”

Rbm45 Phylogenetics, Protein Domain Conservation, and Gene Architecture in Clade Metazoa

“…The Mean Exon Size versus Exon Number and Age of Taxonomic Lineage versus Exon Number were calculated for the following representative animals across metazoan taxa (common name; exon number; mean exon size in base pairs; approximate lineage age in years): phylum Porifera: Amphimedon queenslandica (sponge; 2; 984; 650,000,000 [57]); phylum Brachiopoda: Lingula anatine (lamp shell; 11; 238; 66,000,000 [58]); phylum Hemichordata: Saccoglossus kowalevskii (acorn worm; 9; 234; 373,000,000 [59]); phylum Echinodermata: Acanthaster planci (crown-of-thorns starfish; 11; 404; 4,000,000 [60]), Strongylocentrotus purpuratus (purple sea urchin; 10; 183; 199,000,000 [61]); phylum Cnidaria: Exaiptasia pallida (pale anemone; 4; 544; 500,000,000 [62]), Hydra vulgaris (freshwater polyp; 3; 420; 540,000,000 [63]), Orbicella faveolata (mountainous star coral; 3; 937; 570,000,000 [64]); phylum Mollusca: Octopus bimaculoides (California two-spot octopus; 10; 219; 155,000,000 [65]), Crassostrea gigas (Pacific oyster; 13; 195; 15,000,000 [66]); phylum Arthropoda: Limulus polyphemus (Atlantic horseshoe crab; 6; 206; 250,000,000 [67]), Drosophila melanogaster (fruit fly; 9; 174; 5,400,000 [68]); phylum Chordata: Branchiostoma floridae (Florida lancelet; 7; 154; 100,000,000 [69]), Latimeria chalumnae (West Indian Ocean coelacanth; 10; 181; 70,000,000 [70]), Orcinus orca (killer whale; 10; 182; 11,000,000 [71]), Lipotes vexillifer (Yangtze River dolphin; 10; 170; 11,000,000 [71]), Alligator mississippiensis (American alligator; 10; 210; 53,000,000 [72]), Xenopus laevis (African clawed frog; 11; 173; 18,000,000 [73]), Danio rerio (Zebrafish; 10; 199; 150,000,000 [74]), Monodelphis domestica (gray short-tailed opossum; 10; 196; 3,000,000 [75]), Rattus norvegicus (Norway rat; 10; 178; 2,000,000 [76]), Mus musculus (house mouse; 10; 190; 6,000,000 [77]), Gallus gallus (chicken; 10; 180; 21,000,000 [78]), Pan troglodytes (common chimpanzee; 10; 181; 8,000,000 [79]), Homo sapiens (human; 10; 149; 300,000 [80]). Scatter plots and regression analysis (R 2 : Coefficient of Determination) were generated in Microsoft Excel.…”