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An Investigation into the Genetic History of Japanese Populations of Three Starfish, Acanthaster planci, Linckia laevigata, and Asterias amurensis, Based on Complete Mitochondrial DNA Sequences.
Abstract
Crown-of-thorns starfish, Acanthaster planci (COTS), are common in coral reefs of Indo-Pacific Ocean. Since they are highly fecund predators of corals, periodic outbreaks of COTS cause substantial loss of healthy coral reefs. Using complete mitochondrial DNA sequences, we here examined how COTS outbreaks in the Ryukyu Archipelago, Japan are reflected by the profile of their population genetics. Population genetics of the blue starfish, Linckia laevigata, which lives in the Ryukyu Archipelago, but not break out and the northern Pacific sea star, Asterias amurensis, which lives in colder seawater around the main Islands of Japan, were also examined as controls. Our results showed that As. amurensis has at least two local populations that diverged approximately 4.7 million years ago (MYA), and no genetic exchanges have occurred between the populations since then. Linckia laevigata shows two major populations in the Ryukyu Archipelago that likely diverged ∼6.8 MYA. The two populations, each comprised of individuals collected from coast of the Okinawa Island and those from the Ishigaki Island, suggest the presence of two cryptic species in the Ryukyu Archipelago. On the other hand, population genetics of COTS showed a profile quite different from those of Asterias and Linckia At least five lineages of COTS have arisen since their divergence ∼0.7 MYA, and each of the lineages is present at the Okinawa Island, Miyako Island, and Ishigaki Island. These results suggest that COTS have experienced repeated genetic bottlenecks that may be associated with or caused by repeated outbreaks.
Figure 1. Complete mitochondrial genomes for (a) Asterias amurensis, (b) Linckia laevigata, and (c) Acanthaster planci, determined by whole-genome shotgun sequencing. The mitochondrial genome of As. amurensis is identical to that determined using a primer-based, long PCR method (Matsubara et al. 2005). The L. laevigata mitochondrial genome was sequenced in this study. The Ac. planci genome, which was determined using a primer-based, long PCR method (Yasuda et al. 2010), was improved by whole-genome shotgun sequencing in this study. Genome lengths and the order of genes are shown. Names of sequenced specimens are shown. Schematic genome structures were drawn by using MitoAnnotator (http://mitofish.aori.u-tokyo.ac.jp/annotation/input.html).
Figure 2. Divergence time estimation of sea star populations based on the RelTime method. An arrowhead indicates the separation between Luidia (Luidiidae) and Patiria (Asterinidae) used as the calibration point. According to O’Hara et al. (2014), the Paxillosida (Luidia) and Valvatida (Linckia and Acanthaster) separated around 185 MYA. In our time-calibrated tree, Linckia shows the deepest divergence. Asterias was more recent, and Acanthaster represents the newest lineage. The long branch following the diversification of A. planci and A. brevispinus (21 MYA) suggests repeated genetic bottlenecks in A. planci.
Figure 3. Population genetics of Asterias amurensis. (a) An adult. (b) Location of sample collections in the main Islands of Japan. (c) Population genetics showing two different populations that diverged approximately 4.7 MYA. Genetic flow is seen in the Tohoku population while no genetic flow is apparent in the Ushimado population. (d) PCA of the populations, supporting the population genetic profile shown in (c).
Figure 4. Population genetics of Linckia laevigata. (a) An adult. (b) Location of sample collections in the Ryukyu Archipelago, Japan. (c) Population genetics showing two different populations that diverged approximately 6.8 MYA. The two populations each comprise mixtures of individuals from Okinawa and Ishigaki Islands. (d) PCA of the populations, supporting the population genetic profile shown in (c).
Figure 5. Population genetics of Acanthaster planci. (a) Many adults covering corals. (b) Location of collecting sites in the Ryukyu Archipelago, Japan. (c) Population genetics showing five different populations that diverged approximately 0.7 MYA. The five distinct population comprise mixtures of individuals from Okinawa, Miyako, and Iriomote Islands. (d) PCA of the populations, supporting the population genetic profile shown in (c).
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