Reef development and Sea level changes drive Acanthaster Population Expansion in the Indo-Pacific region

Molecular clock calibration is central in population genetics as it provides an accurate inference of demographic history, whereby helping with the identification of driving factors of population changes in an ecosystem. This is particularly important for coral reef species that are seriously threatened globally and in need of conservation. Biogeographic events and fossils are the main source of calibration, but these are known to overestimate timing and parameters at population level, which leads to a disconnection between environmental changes and inferred reconstructions. Here, we propose the Last Glacial Maximum (LGM) calibration that is based on the assumptions that reef species went through a bottleneck during the LGM, which was followed by an early yet marginal increase in population size. We validated the LGM calibration using simulations and genetic inferences based on Extended Bayesian Skyline Plots. Applying it to mitochondrial sequence data of crown-of-thorns starfish Acanthaster spp., we obtained mutation rates that were higher than phylogenetically based calibrations and varied among populations. The timing of the greatest increase in population size differed slightly among populations, but all started between 10 and 20 kya. Using a curve-fitting method, we showed that Acanthaster populations were more influenced by sea-level changes in the Indian Ocean and by reef development in the Pacific Ocean. Our results illustrate that the LGM calibration is robust and can probably provide accurate demographic inferences in many reef species. Application of this calibration has the potential to help identify population drivers that are central for the conservation and management of these threatened ecosystems.