Dataset Information

Phylogeography of the crown-of-thorns starfish in the Indian Ocean.

ABSTRACT:

Background

Understanding the limits and population dynamics of closely related sibling species in the marine realm is particularly relevant in organisms that require management. The crown-of-thorns starfish Acanthaster planci, recently shown to be a species complex of at least four closely related species, is a coral predator infamous for its outbreaks that have devastated reefs throughout much of its Indo-Pacific distribution.

Methodology/principal findings

In this first Indian Ocean-wide genetic study of a marine organism we investigated the genetic structure and inferred the paleohistory of the two Indian Ocean sister-species of Acanthaster planci using mitochondrial DNA sequence analyses. We suggest that the first of two main diversification events led to the formation of a Southern and Northern Indian Ocean sister-species in the late Pliocene-early Pleistocene. The second led to the formation of two internal clades within each species around the onset of the last interglacial. The subsequent demographic history of the two lineages strongly differed, the Southern Indian Ocean sister-species showing a signature of recent population expansion and hardly any regional structure, whereas the Northern Indian Ocean sister-species apparently maintained a constant size with highly differentiated regional groupings that were asymmetrically connected by gene flow.

Conclusions/significance

Past and present surface circulation patterns in conjunction with ocean primary productivity were identified as the processes most likely to have shaped the genetic structure between and within the two Indian Ocean lineages. This knowledge will help to understand the biological or ecological differences of the two sibling species and therefore aid in developing strategies to manage population outbreaks of this coral predator in the Indian Ocean.

SUBMITTER: Vogler C

PROVIDER: S-EPMC3424128 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Publications

Phylogeography of the crown-of-thorns starfish in the Indian Ocean.

Vogler Catherine C Benzie John J Barber Paul H PH Erdmann Mark V MV Ambariyanto Sheppard Charles C Tenggardjaja Kimberly K Gérard Karin K Wörheide Gert G

PloS one 20120821 8

<h4>Background</h4>Understanding the limits and population dynamics of closely related sibling species in the marine realm is particularly relevant in organisms that require management. The crown-of-thorns starfish Acanthaster planci, recently shown to be a species complex of at least four closely related species, is a coral predator infamous for its outbreaks that have devastated reefs throughout much of its Indo-Pacific distribution.<h4>Methodology/principal findings</h4>In this first Indian O ...[more]

PMID: 22927975

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Project description:Sporadic outbreaks of the coral-eating crown-of-thorns starfish are likely to be due, at least in part, to spatial and temporal variation in reproductive and settlement success. For gonochoric and broadcast spawning species such as crown-of-thorns starfish, spawning synchrony is fundamental for achieving high rates of fertilization. Highly synchronized gamete release within and among distinct populations is typically the result of the entrainment of neurohormonal endogenous rhythms by cues from the environment. In this study, we conducted multiple spawning assays to test the effects of temperature change, reduced salinity and nutrient enrichment of seawater, phytoplankton, gametes (sperm and eggs), and the combined effect of sperm and phytoplankton on the likelihood of spawning in male and female crown-of-thorns starfish. We also investigated sex-specific responses to each of these potential spawning cues. We found that (1) abrupt temperature change (an increase of 4°C) induced spawning in males, but less so in females; (2) males often spawned in response to the presence of phytoplankton, but none of the females spawned in response to these cues; (3) the presence of sperm in the water column induced males and females to spawn, although additive and synergistic effects of sperm and phytoplankton were not significant; and (4) males are more sensitive to the spawning cues tested and most likely spawn prior to females. We propose that environmental cues act as spawning 'inducers' by causing the release of hormones (gonad stimulating substance) in sensitive males, while biological cues (pheromones) from released sperm, in turn, act as spawning 'synchronizers' by triggering a hormonal cascade resulting in gamete shedding by conspecifics. Given the immediate temporal linkage between the timing of spawning and fertilization events, variability in the extent and synchronicity of gamete release will significantly influence reproductive success and may account for fluctuations in the abundance of crown-of-thorns starfish.

Project description:BackgroundThe crown-of-thorns starfish, Acanthaster planci (L.), has been blamed for coral mortality in a large number of coral reef systems situated in the Indo-Pacific region. Because of its high fecundity and the long duration of the pelagic larval stage, the mechanism of outbreaks may be related to its meta-population dynamics, which should be examined by larval sampling and population genetic analysis. However, A. planci larvae have undistinguished morphological features compared with other asteroid larvae, hence it has been difficult to discriminate A. planci larvae in plankton samples without species-specific markers. Also, no tools are available to reveal the dispersal pathway of A. planci larvae. Therefore the development of highly polymorphic genetic markers has the potential to overcome these difficulties. To obtain genomic information for these purposes, the complete nucleotide sequences of the mitochondrial genome of A. planci and its putative sibling species, A. brevispinus were determined and their characteristics discussed.ResultsThe complete mtDNA of A. planci and A. brevispinus are 16,234 bp and 16,254 bp in size, respectively. These values fall within the length variation range reported for other metazoan mitochondrial genomes. They contain 13 proteins, 2 rRNA, and 22 tRNA genes and the putative control region in the same order as the asteroid, Asterina pectinifera. The A + T contents of A. planci and A. brevispinus on their L strands that encode the majority of protein-coding genes are 56.3% and 56.4% respectively and are lower than that of A. pectinifera (61.2%). The percent similarity of nucleotide sequences between A. planci and A. brevispinus is found to be highest in the CO2 and CO3 regions (both 90.6%) and lowest in ND2 gene (84.2%) among the 13 protein-coding genes. In the deduced putative amino acid sequences, CO1 is highly conserved (99.2%), and ATP8 apparently evolves faster any of the other protein-coding gene (85.2%).ConclusionThe gene arrangement, base composition, codon usage and tRNA structure of A. planci are similar to those of A. brevispinus. However, there are significant variations between A. planci and A. brevispinus. Complete mtDNA sequences are useful for the study of phylogeny, larval detection and population genetics.

Project description:In marine organisms, and in particular for benthic invertebrates including echinoderms, olfaction is a dominant sense with chemosensation being a critical signalling process. Until recently natural product chemistry was the primary investigative approach to elucidate the nature of chemical signals but advances in genomics and transcriptomics over the last decade have facilitated breakthroughs in understanding not only the chemistry but also the molecular mechanisms underpinning chemosensation in aquatic environments. Integration of these approaches has the potential to reveal the fundamental elements influencing community structure of benthic ecosystems as chemical signalling modulates intra- and inter-species interactions. Such knowledge also offers avenues for potential development of novel biological control methods for pest species such as the predatory Crown-of-Thorns starfish (COTS), Acanthaster planci which are the primary biological cause of coral cover loss in the Indo-Pacific.In this study, we have analysed the COTS sensory organs through histological and electron microscopy. We then investigated key elements of the COTS molecular olfactory toolkit, the putative olfactory rhodopsin-like G protein-protein receptors (GPCRs) within its genome and olfactory organ transcriptomes. Many of the identified Acanthaster planci olfactory receptors (ApORs) genes were found to cluster within the COTS genome, indicating rapid evolution and replication from an ancestral olfactory GPCR sequence. Tube feet and terminal sensory tentacles contain the highest proportion of ApORs. In situ hybridisation confirmed the presence of four ApORs, ApOR15, 18, 25 and 43 within COTS sensory organs, however expression of these genes was not specific to the adhesive epidermis, but also within the nerve plexus of tube feet stems and within the myomesothelium. G alpha subunit proteins were also identified in the sensory organs, and we report the spatial localisation of G?i within the tube foot and sensory tentacle.We have identified putative COTS olfactory receptors that localise to sensory organs. These results provide a basis for future studies that may enable the development of a biological control not only for COTS, but also other native pest or invasive starfish.

Dataset Information

Phylogeography of the crown-of-thorns starfish in the Indian Ocean.

Background

Methodology/principal findings

Conclusions/significance

Publications

Phylogeography of the crown-of-thorns starfish in the Indian Ocean.

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