Abstract

BackgroundPopulations of the earthworm, Lumbricus rubellus, are commonly found across highly contaminated former mine sites and are considered to have under-gone selection for mitigating metal toxicity. Comparison of adapted populations with those found on less contaminated soils can provide insights into ecological processes that demonstrate the long-term effects of soil contamination. Contemporary sequencing methods allow for portrayal of demographic inferences and highlight genetic variation indicative of selection at specific genes. Furthermore, the occurrence of L. rubellus lineages across the UK allows for inferences of mechanisms associated with drivers of speciation and local adaptation.ResultsUsing RADseq, we were able to define population structure between the two lineages through the use of draft genomes for each, demonstrating an absence of admixture between lineages and that populations over extensive geographic distances form discrete populations. Between the two British lineages, we were able to provide evidence for selection near to genes associated with epigenetic and morphological functions, as well as near a gene encoding a pheromone. Earthworms inhabiting highly contaminated soils bare close genomic resemblance to those from proximal control soils. We were able to define a number of SNPs that largely segregate populations and are indicative of genes that are likely under selection for managing metal toxicity. This includes calcium and phosphate-handling mechanisms linked to lead and arsenic contaminants, respectively, while we also observed evidence for glutathione-related mechanisms, including metallothionein, across multiple populations. Population genomic end points demonstrate no consistent reduction in nucleotide diversity, or increase in inbreeding coefficient, relative to history of exposure.ConclusionsThough we can clearly define lineage membership using genomic markers, as well as population structure between geographic localities, it is difficult to resolve markers that segregate entirely between populations in response to soil metal concentrations. This may represent a highly variable series of traits in response to the heterogenous nature of the soil environment, but ultimately demonstrates the maintenance of lineage-specific genetic variation among local populations. L. rubellus appears to provide an exemplary system for exploring drivers for speciation, with a continuum of lineages coexisting across continental Europe, while distinct lineages exist in isolation throughout the UK.

Highlights

  • Populations of the earthworm, Lumbricus rubellus, are commonly found across highly contaminated former mine sites and are considered to have under-gone selection for mitigating metal toxicity

  • Identification of regions of the genome under selection is empowered with the availability of high-throughput sequencing methods such as Restriction-site Associated DNA sequencing (RADseq), which allows for identification of markers across the genome [8, 9]

  • Through comparison with proximal populations found on less contaminated soils, we have provided insights into ecological processes derived from segregating patterns of genetic differentiation, while calculation of population genetic statistics will demonstrate the long term effects of environmental contamination upon natural populations

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Summary

Introduction

Populations of the earthworm, Lumbricus rubellus, are commonly found across highly contaminated former mine sites and are considered to have under-gone selection for mitigating metal toxicity. In knowing how classical endpoints vary, e.g. growth, reproduction and survival, researchers can determine the short-term effects of exposure to lab-based cohorts and are able to make inferences as to the effects on natural populations [3,4,5]. While these are useful for recognising the effects of exposure within a single generation, effects over multiple generations, such as changes in genetic diversity associated with selection, can be more subtle. Local adaptation (as reviewed by Savolainen et al [15]) can be used to distinguish adaptive mechanisms in populations and can effectively complement species-level comparisons to define evolutionary commonality, and to provide insight into traits and processes that have driven speciation

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