Abstract
Despite the fundamental role that soil invertebrates (e.g. earthworms) play in soil ecosystems, the magnitude of their spatial genetic variation is still largely unknown and only a few studies have investigated the population genetic structure of these organisms. Here, we investigated the genetic structure of seven populations of a common endogeic earthworm (Aporrectodea icterica) sampled in northern France to explore how historical species range changes, microevolutionary processes and human activities interact in shaping genetic variation at a regional scale. Because combining markers with distinct modes of inheritance can provide extra, complementary information on gene flow, we compared the patterns of genetic structure revealed using nuclear (7 microsatellite loci) and mitochondrial markers (COI). Both types of markers indicated low genetic polymorphism compared to other earthworm species, a result that can be attributed to ancient bottlenecks, for instance due to species isolation in southern refugia during the ice ages with subsequent expansion toward northern Europe. Historical events can also be responsible for the existence of two divergent, but randomly interbreeding mitochondrial lineages within all study populations. In addition, the comparison of observed heterozygosity among microsatellite loci and heterozygosity expected under mutation-drift equilibrium suggested a recent decrease in effective size in some populations that could be due to contemporary events such as habitat fragmentation. The absence of relationship between geographic and genetic distances estimated from microsatellite allele frequency data also suggested that dispersal is haphazard and that human activities favour passive dispersal among geographically distant populations.
Highlights
Earthworms represent one of the largest reservoirs of animal biomass and the main invertebrate group of soil ecosystem engineers in most terrestrial temperate ecosystems [1]
Few studies have simultaneously investigated the influence of historical events, such as glacial periods, and contemporary processes, such habitat fragmentation, on the genetic diversity of these species
In their review on the genetic structure of soil invertebrate populations, Costa et al [14] cite only seven studies of earthworm populations. They conclude that earthworm populations generally show a complicated pattern of gene flow, with a weak relationship between genetic and geographic distances
Summary
Earthworms represent one of the largest reservoirs of animal biomass and the main invertebrate group of soil ecosystem engineers in most terrestrial temperate ecosystems [1] They play a key role in soil functioning: they relocate surface litter or organic matter throughout the soil profile [2,3], affect microbial activity [4], and have a significant effect on organic matter mineralisation and soil biogeochemical cycles [5]. Earthworms influence plant growth [8] and plant community structure [9,10], and can be used as indicators of habitat quality [11,12] and as biomarkers in toxicity tests [13] Despite their fundamental impact on soil ecosystems, the spatial population dynamics of earthworms is poorly understood. More earthworm population genetics studies are needed to determine (i) how earthworms move between patches, (ii) how spatial structure affects the stability and dynamics of spatially structured earthworm populations, and (iii) how the landscape affects genetic diversity
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