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

Abstract

Communities of organisms inhabiting extreme terrestrial environments provide a unique opportunity to study evolutionary forces that drive population structure and genetic diversity under the combined challenges posed by multiple geogenic stressors. High abundance of an invasive pantropical earthworm (and the absence of indigenous lumbricid species) in the Furnas geothermal field (Sao Miguel Island, Azores) indicates its remarkable tolerance to high soil temperature, exceptionally high carbon dioxide and low oxygen levels, and elevated metal bioavailability, conditions which are lethal for the majority of terrestrial metazoans. Mitochondrial and nuclear markers were used to analyze the 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 Miguel landscape and is probably differentiated into cryptic species. The population exposed to the hostile soil conditions within the volcanic caldera possesses the lowest within-population mitochondrial diversity but an unexpectedly high degree of nuclear variability with several loci evidencing positive selection, parameters indicative of a genetically unique population only distantly related to conspecifics living outside the caldera. In conclusion, P. corethrurus inhabiting active volcanic soil is a discrete extremophile population that has evolved by tolerating a mixture of nonanthropogenic chemical and physical stressors.

Harmful or useful? A case study of the exotic peregrine earthworm morphospecies Pontoscolex corethrurus

“…Although several complexes of cryptic species have been recently described in earthworms, highlighting the difficulties of morphological diagnosis in this taxon (King et al, 2008;Novo et al, 2010;Pérez-Losada et al, 2009;Shekhovtsov et al, 2016), there is not much data available in the literature on the genetic diversity within the P. corethrurus morphospecies (Cunha et al, 2014;Dupont et al, 2012). In three populations of P. corethrurus in the Azores archipelago, Cunha et al (2014) revealed the existence of two genetically divergent lineages which were morphologically indistinguishable. They showed that one of the lineages was able to cope with the extreme conditions found in the caldera of a volcano where it tolerates a mixture of nonanthropogenic chemical and physical stressors.…”

“…), and an average temperature of 17°± 2, where no other tropical species occur. This morphospecies was even recorded in the temperate zone, in the Azores archipelago (Cunha et al, 2014) and the Falkland islands (Reynolds and Jones, 2006). Gates (1972) mentioned that P. corethrurus was present in a greenhouse in the London suburb of Kew (United Kingdom), but there is no record of its expansion in this country.…”

“…Righi (1984) identified the Guyana shield as the original region of the Pontoscolex genus. Recently, Cunha et al (2014), revealed the existence of two highly divergent genetic lineages within P. corethrurus in the island of Sao Miguel (Azores), suggesting the existence of cryptic species (i.e., different species which are not distinguishable morphologically). Thus, we choose to refer to the "morphospecies" P. corethrurus (i.e., a species distinguished from others only by its morphology) in this review.…”

The complete mitochondrial DNA sequence of the pantropical earthworm Pontoscolex corethrurus (Rhinodrilidae, Clitellata): Mitogenome characterization and phylogenetic positioning

“…The complete Pontoscolex corethrurus mitogenome was amplified using seven sets of primers (Table 1) designed based on sequences retrieved from a previous study (Cunha et al 2014). Long PCR targets were amplified using different combinations of the primer sets, and and initially sequenced with the same forward or reverse primers.…”

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“…It is also the most well-known earthworm species in the humid tropics, frequently used in ecological and agronomic studies (Bhattacharjee and Chaudhuri, 2002;Buch et al, 2013;Chapuis-Lardy et al, 2010;Dupont et al, 2012;Hamoui, 1991;Marichal et al, 2010). Being a geophagous endogeic species, P. corethrurus shows high plasticity regarding its tolerance to soil physicochemical characteristics, including variable moisture, high temperatures, exceptionally high carbon dioxide and low oxygen levels, and is capable of inhabiting nutrient-poor soils (Cunha et al, 2014;Hamoui, 1991;Lavelle et al, 1987), as well as rotten logs (Buch et al, 2011).…”