The Demographic History of Micro-endemics: Have Rare Species Always Been Rare?

Abstract

Extinction has increased as human activities impact ecosystems. Conservation assessments for the IUCN red list are a fundamental tool in aiding the prevention of further extinction, yet, relatively few species have been thoroughly assessed. To increase the efficiency of assessments, novel approaches are needed to highlight threatened species that are currently data deficient. Many Madagascan plant species currently have extremely narrow ranges, but this may not have always been the case. To assess this, we used high-throughput DNA sequencing for 2-5 individuals of each species - reflecting the paucity of samples available for rare species. We estimated effective population size (Ne) for each species and compared this to census population (Nc) sizes when known. In each case, Ne was an order of magnitude larger than Nc - a signature of rapid, recent population decline. We then estimated the demographic history of each species, tracking changes in Ne over time. Five out of ten species displayed significant population declines towards the present (68-90% decreases). Our results for palm trees indicate that it is possible to predict extinction risk, particularly in the most threatened species. We performed simulations to show that our approach has the power to detect population decline during the Anthropocene, but performs less well when less data is used. Similar declines to those in palms were observed in data deficient species or those assessed as of least concern. These analyses reveal that Madagascars narrow endemics were not always rare, having experienced rapid decline in their recent history. Our approach offers the opportunity to target species in need of conservation assessment with little prior information, particularly in regions where human modification of the environment has been rapid. SummaryCurrent IUCN conservation assessment methods are reliant on observed declines in species population and range sizes over the last one hundred years, but for the majority of species this information is not available. We used a population genetic approach to reveal historical demographic decline in the rare endemic flora of Madagascar. These results show that it is possible to predict extinction risk from demographic patterns inferred from genetic data and that destructive human influence is likely to have resulted in the very high frequency of narrow endemics present on the island. Our approach will act as an important tool for rapidly assessing the threatened status of poorly known species in need of further study and conservation, particularly for tropical flora and fauna.