Despite the unique nature of endemic species, their origin and population history remain poorly studied. We investigated the population history of 28 coral reef fish species, close related, from the Gambier and Marquesas Islands, from...
moreDespite the unique nature of endemic species, their origin and population history remain poorly studied. We investigated the population history of 28 coral reef fish species, close related, from the Gambier and Marquesas Islands, from five families, with range size varying from widespread to small-range endemic. We analyzed both mitochondrial and nuclear sequence data using neutrality test and Bayesian analysis (EBSP and ABC). We found evidence for demographic expansions for most species (24 of 28), irrespective of range size, reproduction strategy or archipelago. The timing of the expansions varied greatly among species, from 8,000 to 2,000,000 years ago. The typical hypothesis for reef fish that links population expansions to the Last Glacial Maximum fit for 14 of the 24 demographic expansions. We propose two evolutionary processes that could lead to expansions older than the LGM: (a) we are retrieving the signature of an old colonization process for widespread, large-range endemic and paleoendemic species or (b) speciation; the expansion reflects the birth of the species for neoendemic species. We show for the first time that the demographic histories of endemic and widespread reef fish are not distinctly different and suggest that a number of processes drive endemism. The existence of endemic coral reef fish species is a challenge for evolutionary biologists to explain given tropical waters are widely connected. The highest levels of endemism on coral reefs are observed near islands at the peripheries of the Indo-Malay-Philippines Archipelago (IMPA), global hotspot of reef fish species diversity 1–5. As examples from the Pacific Ocean, the percentage of reef fish that are endemic in the Hawaiian archipelago is 25% 6 , 22% in Easter Island 7 , and 14% in the Marquesas Islands 8. Even if actual patterns of distribution of coral reef fish species are now well depicted, the evolution and processes underlying the establishment and maintenance of endemic species remains unclear. Despite their unique nature and their potentially higher risk of extinction, the origin and population history of endemic species is poorly studied. The Pleistocene era (c. 1.8–0.01 Ma), which affected the distribution and demographic history of both terrestrial and costal marine species 9 , was characterized by glacial cycles and sea level fluctuations up to 150 m below present sea level 10,11. Large parts of continental shelves were exposed during low sea level, altering shallow water habitat and likely reducing coral reef area 12–14. These dramatic changes to the environment influence the demographic history of populations, leaving a footprint in the pattern of genetic diversity 15 that will vary depending on the range extent of the species (i.e., how much of the global species was affected by the event). Population bottlenecks and expansions have often been retrieved in marine populations and shown to coincide with the last major sea level changes impacting population dynamics 9,16–18. Species biology can affect how reef fish species respond in term of population size variation to major sea level changes such as through varying the larval phase or habitat 19–22. However, very few studies have explored how species with different range size respond to major climatic events 23,24. Endemic species have by definition a limited distribution 25 so are widely expected to be highly vulnerable to environmental changes that are locally disrupting 26,27. This is particularly the case for coral reef fishes forming metapopulations where connectivity occurs only during the larval stage, i.e. colonization of new suitable habitats and migrant exchanges among
