Genomic costs without functional consequences in short-range endemics trapped in evolutionary refugia

Emily Roycroft , Ching Ching Lau, Stephen M Zozaya , Keith Allen Christian , Rhiannon Schembri, Craig Moritz 

Species with small geographic ranges are often concentrated in evolutionary refugia, landscapes that support viable populations through significant climate oscillations. Under long-term stable environments and with small population size, species are predicted to evolve narrow climatic tolerances, lose genetic diversity and accumulate harmful mutations. Together, these predictions suggest that short-range endemic species may be highly vulnerable to extinction. Here, we investigate the genomic and evolutionary consequences of persistence in refugia using a radiation of Australian geckos (Gehyra spp.) as a model system. With 82 genomes from eight species, spanning short-range and widespread pairs, we demonstrate the long-term persistence of short-range endemics at sustained small population size. Short-range endemics have lower genomic diversity and higher inbreeding, but do not show excess fixation of harmful mutations compared to their widespread relatives. We find a relative deficit of high-impact mutations in the most inbred species, consistent with purging of strongly deleterious variation. Despite restricted distributions, the physiological tolerances of short-range endemics are highly plastic, and similar to widespread species. Together, these results suggest that species in evolutionary refugia may be no more intrinsically susceptible to extinction than their widespread counterparts. Despite this, short-range species remain highly vulnerable to extinction via extrinsic factors, including catastrophic environmental events.