Living on a volcano's edge: genetic isolation of an extremophile terrestrial metazoan

Communities of organisms inhabiting extreme terrestrial environments provide a uniqueopportunity to study evolutionary forces that drive population structure and geneticdiversity under the combined challenges posed by multiple geogenic stressors. Highabundance of an invasive pantropical earthworm (and the absence of indigenous lumbricidspecies) in the Furnas geothermal field (Sao Miguel Island, Azores) indicates itsremarkable tolerance to high soil temperature, exceptionally high carbon dioxide and lowoxygen levels, and elevated metal bioavailability, conditions which are lethal for themajority of terrestrial metazoans. Mitochondrial and nuclear markers were used to analyzethe relationship between populations living inside and outside the geothermal field.Results showed that Pontoscolex corethrurus (Annelida, Oligochaeta,Glossoscolecidae) to be a genetically heterogeneous complex within the Sao Miguellandscape and is probably differentiated into cryptic species. The population exposed tothe hostile soil conditions within the volcanic caldera possesses the lowestwithin-population mitochondrial diversity but an unexpectedly high degree of nuclearvariability with several loci evidencing positive selection, parameters indicative of agenetically unique population only distantly related to conspecifics living outside thecaldera. In conclusion, P. corethrurus inhabiting active volcanic soil is adiscrete extremophile population that has evolved by tolerating a mixture ofnon-anthropogenic chemical and physical stressors.