Living on a volcano’s edge: genetic isolation of an extremophile terrestrial metazoan
The study of populations of soil organisms living near active geothermal vents provides an unusual opportunity to understand the aspects of their population structure and genetic diversity. Given the relative ease in the accessibility of such populations it is remarkable that these terrestrial metazoan communities appear to be much less well understood than the charismatic marine invertebrate fauna living adjacent to hydrothermal vents. In fact, terrestrial geothermal biotopes are reducing environments with particular unique features, such as elevated soil, pore-water, and atmospheric elemental composition, together with a constant diffuse degassing and high temperatures. The secondary manifestations of volcanism in the geothermal field include low temperature fumaroles (maximum temperature around 100°C), hot springs, CO2 cold springs and several diffuse degassing areas. Volcanic gases present in the mid-Atlantic geothermal field (Furnas, Sao Miguel Island, Azores, Portugal) subjected to the present study, typically comprised water vapour, carbon dioxide (CO2), hydrogen sulfide (H2S), sulfur dioxide (SO2), hydrogen chloride (HCl), lesser amounts of hydrogen fluoride (HF), and the radioactive gas radon (Rn). The ephemeral nature of the geothermal field is expected to favour the settlement by species with admirable colonization abilities. We have previously collected and identified the endogeic glossoscolecid earthworm Pontoscolex corethrurus (Müller, 1856), from the geothermal field at Furnas. P. corethrurus is a well-known invasive species of most tropical regions and its global distribution seems to be only limited by temperature. The presence and high abundance of this species in the geothermal field – and striking absence of indigenous lumbricid species, common in a wide range of soil types outside the caldera may be indicative of its tolerance to the intense and multifactorial stress extant in the active volcanic soil. In fact, morphometric analyses of the epidermis of Amynthas gracilis (an epigeic earthworm, also an invasive species, and the only other earthworm species found in Furnas soil) is ~50% thinner than the respiratory exchange surface in conspecifics resident on inactive volcanic soils. This large difference implies that the responses of earthworms to the multi-stressor challenges in active volcanic soils comprise integrated modifications ranging from genetic and biochemical, to cellular and physiological levels of organisation. Furthermore, neither the extent of genetic diversity in P. corethrurus populations in the Azores archipelago is known, nor the timing and source(s) of the colonization.
Therefore we consider ourselves fortunate to have the opportunity to exploit this remarkable ‘natural evolutionary laboratory’ where two invasive earthworm species have successfully colonised the hostile soil associated with an otherwise very well characterized geothermal field. Our analyses rely on mitochondrial DNA sequence data complemented with nuclear markers in order to accurately characterize the genetic diversity within these populations and their phylogenetic relationships with populations living under less stressful conditions outside the caldera. Furthermore, we determined whether the population adapted to active volcanism possess reduced levels of genetic variation as a consequence of their demographic history, and whether they have become genetically distinct from other populations on the island. The results showed a Furnas population (i.e. within the caldera) with lower mitochondrial diversity exhibiting a very homogeneous mtDNA haplotype, which plausibly indicates the erosive effect of natural selection on the mitochondrial genome, will intensify in populations successfully inhabiting intensely stressful environmental conditions. In contrast, the unexpected high nuclear variability in the geothermal individuals may reveal an intriguing alternative scenario where chemical contaminants increase genetic diversity by causing somatic and even genomic mutations.
We consider that this study makes a number of profound observations on the genetic aspects of the adaptation of an ecologically-relevant soil-dwelling metazoan to the multiplicity of life-challenging stress factors in an extreme environment associated with active volcanic activity. The following paper is our most recent output about these mysterious and amazing volcanic earthworms.
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