Genomic Single Nucleotide Polymorphism (SNP) markers and mitochondrial haplotypes illuminate the origins of Crown-of-Thorns Starfish (Acanthaster solaris) outbreaks in the South China Sea

Abstract

Background: Outbreaks of the coral predator Crown-of-Thorns Starfish (CoTS) pose a severe threat to coral reefs in the Indo-Pacific Ocean. In 2018, the South China Sea (SCS) experienced significant CoTS outbreaks, leading to extensive coral mortality across the Xisha, Zhongsha, Dongsha, and Nansha Islands, severely impacting the coral reef ecosystem.

Results: To explore the origins of these outbreaks, we conducted a comprehensive genomic analysis using data from genomic single nucleotide polymorphism sites (SNPs) and mitochondrial haplotypes. Our analysis reveals that CoTS populations in the SCS, which exhibit moderate genetic diversity and may have undergone positive selection or population expansion. There was limited genetic differentiation among CoTS populations from XS, ZS, and NS groups. Especially between the XS and ZS groups, there was almost no genetic differentiation. The populations from XS, ZS, and NS groups have strong genetic connections with populations in Vietnam and the Philippines. There was high gene flow from Vietnam to the Xisha Islands and from the Philippines to the Nansha Islands, suggesting that the CoTS populations in these regions primarily originate from these neighboring countries.

Conclusion: The comprehensive analyses of SNP and mitochondrial genomes have provided valuable insights into the population genetics of CoTS. This research has generated significant genomic resources and facilitated important studies on the genetics of the CoTS species. By identifying potential source populations and understanding the genetic basis of their spread, managers can develop more effective conservation strategies to protect vulnerable coral reef ecosystems in the SCS.

Keywords: Crown-of-Thorns Starfish; Gene flow; Population structure; SNPs; The South China Sea.

Fig. 1

The map illustrates the locations of the nine populations of Crown-of-Thorns Starfish for this research. The red dots represent our sampling locations in the South China Sea. The blue dots represent stations cited from Yasuda et al. [22]. It was generated utilizing Ocean Data View v5.5.2 (Schlitzer, Reiner, Ocean Data View, odv.awi.de, 2023)

Fig. 2

Subgroups represented by the ADMIXTURE analysis (k = 2, 3 and 4). Each column represents an individual genome, and the colored segments indicate the proportions of ancestral contributions. K = 2 to 4 indicates the assumed number of ancestral populations. The X-axis displays the group name and its corresponding geographic distribution

Fig. 3

The Maximum likelihood tree constructed from SNPs

Fig. 4

Principal Component Analysis (PCA): The values within brackets indicate the percentage of variance explained by each displayed principal component

Fig. 5

Treemix analysis of gene flow among populations of the Crown-of-Thorns Starfish. Network depicts genetic relationships and drift (branch lengths). Scale bar indicates 100x standard error of covariance matrix. Arrows indicate putative gene flow events, intensity is represented by color

Fig. 6

Haplotype network of mitogenomes from Crown-of-Thorns Starfish. In this TCS network, each node indicates a haplotype, with nodes colored according to origin