The burden of anthropogenic changes and mutation load in a critically endangered harrier from the Reunion biodiversity hotspot, Circus maillardi

Anthropogenic impact is causing the decline of a large proportion of species worldwide and reduces their genetic diversity. Island species typically have smaller ranges than continental species. As a consequence, island species are particularly liable to undergo population bottlenecks, giving rise to conservation challenges such as inbreeding and unmasking of deleterious genetic load. Such challenges call for more detailed assessments of the genetic make-up of threatened island populations. The Mascarene islands (Indian Ocean) present many prime examples, being unusual in having been pristine until first human arrival similar to 400 years ago, following which anthropogenic pressure was unusually intense. A threatened harrier (Circus maillardi) endemic to the westernmost island of the archipelago is a good example of the challenges faced by species that have declined to small population size following intense anthropogenic pressure. In this study, we use an extensive set of population genomic tools to quantify variation at near-neutral and coding loci, in order to test the historical impact of human activity on this species, and evaluate the species' (mal)adaptive potential. We observed low but significant genetic differentiation between populations on the West and North-East sides of the island, echoing observations in other endemic species. Inbreeding was significant, with a substantial fraction of samples being first or second-degree relatives. Historical effective population sizes have declined from similar to 3000 to 300 individuals in the past 1000 years, with a more recent drop similar to 100 years ago consistent with human activity. Based on our simulations and comparisons with a close relative (Circus melanoleucos), this demographic history may have allowed purging of the most deleterious variants but is unlikely to have allowed the purging of mildly deleterious variants. Our study shows how using relatively affordable methods can reveal the massive impact that human activity may have on the genetic diversity and adaptive potential of island populations, and calls for urgent action to closely monitor the reproductive success of such endemic populations, in association with genetic studies.