Genetic Structure of Earthworm Populations at a Regional Scale: Inferences from Mitochondrial and Microsatellite Molecular Markers in Aporrectodea icterica (Savigny 1826)

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.

Dispersal constraints and fine-scale spatial genetic structure in two earthworm species

“…For instance, the number of alleles was three times higher for A. chlorotica than for A. icterica. This difference is not a particularity of the study because the level of genetic diversity recorded is similar to the results of Dupont et al (2011) for A. chlorotica and of Torres-Leguizamon et al (2012) and Torres-Leguizamon et al (2014) for A. icterica at the landscape/region scale. In our study, A. icterica Table 2.…”

“…For instance, the N all value of earthworm's microsatellite loci typically ranges from five to 17 (review in Torres- Leguizamon et al, 2014), whereas A. icterica loci display a maximal N all of 3.6. Such a low polymorphism of molecular markers decreases the precision in estimates of heterozygote deficiencies (Robertson & Hill, 1984), statistical tests of differentiation (Goudet et al, 1996), and estimates of gene-dispersal distances (Leblois et al, 2003).…”

“…Such a low polymorphism of molecular markers decreases the precision in estimates of heterozygote deficiencies (Robertson & Hill, 1984), statistical tests of differentiation (Goudet et al, 1996), and estimates of gene-dispersal distances (Leblois et al, 2003). The low polymorphism of A. icterica microsatellite loci could be reflecting bottlenecks in the evolutionary history of this species (Torres-Leguizamon et al, 2014). More research is needed in order to understand, more clearly, this particularity of A. icterica simple sequence repeats.…”

“…proportion of variance in allele frequencies that is among populations) and related statistics to measure gene flow. Most authors who have tested the relationship between genetic and geographical distances between earthworm populations using these population-based measures, whereby species are arbitrarily divided into partially isolated populations, have found significant genetic differentiation and no or a weak isolation-by-distance (IBD) pattern (Enckell et al, 1986;Kautenburger, 2006;Cameron, Bayne & Coltman, 2008;Prasankok et al, 2013;Torres-Leguizamon et al, 2014, but see Novo, Almodóvar & Díaz-Cosín, 2009;Novo et al, 2010a). All these studies were carried out at the regional/ landscape scale, except that of Novo et al (2010a), which investigated the genetic structure of a homogastrid earthworm at fine spatial scale using F-statistics (0.064 km 2 ).…”

Initial conditions during Technosol implementation shape earthworms and ants diversity

“…Second, human activities associated with less intensive soil transportation than soil construction such as gardening could have involved passive dispersal. Passive dispersal of eggs or adults is sometimes considered important for long distance dispersal of earthworms (Costa et al, 2013;Eijsackers, 2011;Torres-Leguizamon et al, 2014). Globally, dispersal of earthworms in urban landscapes remains poorly understood.…”