Research Article: Genetic structure and distribution of Parisotoma notabilis (Collembola) in Europe: Cryptic diversity, split of lineages and colonization patterns

Date Published: February 7, 2017

Publisher: Public Library of Science

Author(s): Helge von Saltzwedel, Stefan Scheu, Ina Schaefer, Xiao-Yue Hong.


Climatic and biome changes of the past million years influenced the population structure and genetic diversity of soil-living arthropods in Europe. However, their effects on the genetic structure of widespread and abundant soil animal species such as the Collembola Parisotoma notabilis remain virtually unknown. This generalist and parthenogenetic species is an early colonizer of disturbed habitats and often occurs in human modified environments. To investigate ancient climatic influence and recent distributions on the genetic structure of P. notabilis we analyzed populations on a pan-European scale using three genetic markers differing in substitution rates. The results showed that P. notabilis comprises several genetic lineages with distinct distribution ranges that diverged in the Miocene. Genetic distances of COI between lineages ranged between 15% and 18% and molecular clock estimates suggest Late Miocene divergences considering the standard arthropod rate of 2.3% per my. Compared to other soil-living arthropods like oribatid mites, European lineages of P. notabilis are rather young and genetically uniform. The close association with anthropogenic habitats presumably contributed to rapid spread in Europe.

Partial Text

The ubiquitous soil arthropod species Parisotoma notabilis (Schäffer, 1896) is one of the most successful species among Collembola being locally abundant in virtually any habitat in the temperate and boreal zone. Populations can reach densities of up to 10,000 and 6,000 individuals per square meter in forest soils and meadows, respectively, but also typically are present in arable fields, pastures, urban soils and caves [1–8], and even in extreme habitats such as open glacier forelands at high elevation [9]. P. notabilis is the most abundant Collembola species in Europe [10] and together with Isotomiella minor (Schäffer, 1896) it often represents more than 50% of the total individuals in Collembola communities [2,4]. It is morphologically well defined [11–14], but exhibits inter-population differences in tolerance to low pH, mechanical disturbances and metal pollution [1,6]. According to stable isotope ratios of 15N/14N it feeds as generalist on bacteria, fungi and smaller soil animals including protozoans, nematodes and rotifers [15]. Notably, P. notabilis reproduces via parthenogenesis, no males have been found in natural populations [16] except for a Swedish population where males rarely occur [17]. Wind dispersal [8], the potential to start populations from a single female individual and generalist feeding make this species a fast and successful colonizer of new and disturbed habitats [18–22].

This study analyzed the phylogeographic structure of P. notabilis in Europe, one of the most widespread and abundant species of Collembola. The sampling region covered southern, central and northern Europe from east (Ukraine) to west (Pyrenees). Four of the five genetic lineages of this study corresponded with the lineages of [23] but had a wider distribution range due to the extended sampling area. Combined with our data, the southern European lineage L1 of [23] is also common in the east of Europe (Russia2, Ukraine and Turkey), and lineage L2, assumed to be restricted to the Alpine-Carpathian mountain ranges by [23], in fact is widely distributed in western and northern Europe (France, Denmark, Norway, Greenland, west of Scotland) and the Pyrenees. Interestingly, these two widespread lineages are parapatric, indicating either the importance of northern Spain as refuge area during the Last Ice Age or the existence of a contact zone of two lineages [26,51–57] with otherwise distinct distribution ranges. Lineage L0 likely is the type-species lineage and only occurred in three of our sampling locations. However, in combination with the data of [23], it appears to have a rather continuous distribution range in the vicinity of The Channel, and along the coasts of North- and Baltic Sea. Further, additional to the previously described lineage L3 that only occurred in Paris (France) [23], we identified a lineage distantly related to this population in southern Europe (Greece) and a new lineage from a single location in Croatia. These lineages add to the cryptic genetic diversity of P. notabilis in Europe, in particular in southern Europe.




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