A low-dispersal vertebrate in a fragmented landscape; using an individual-based sampling scheme to highlight gene flow in the common adder Vipera berus

Authors and Affiliations: 

Donatien FRANCOIS1, Alexandre BOISSINOT2, Sylvain URSENBACHER3, Olivier LOURDAIS2 & Frédéric YSNEL1

1EA 7316 Biodiversité et Gestion du Territoire, Université de Rennes 1, Campus de Beaulieu, Rennes (France)
2Centre d’Etudes Biologiques de Chizé, Villiers-en-Bois (France)
3Department of Environmental Sciences, Section of Conservation Biology, University of Basel, Basel (Switzerland)

Corresponding author: 

The impact of habitat fragmentation can strongly vary among species or individuals depending on their dispersal abilities (e.g. ability to move through the matrix1), and poor dispersers suffer the most from a fragmented landscape. The common adder (Vipera berus) is a widespread snake species with a low dispersal ability2-4, important phylopatry5,6 and a significant population decline associated with habitat degradation and loss of connectivity (e.g. road building; lack of shelters7,8). Previous studies demonstrated that V. berus populations are strongly affected genetically (e.g. inbreeding; inviable offspring) when populations are isolated from each other9. Similarly, separated by 20km while other population pairs could show no sign of genetic separation despite being 100km apart10. Therefore, this species provides a good opportunity to study functional connectivity and the impact of habitat structure on dispersion, especially since V. berus is a target species for the French green and blue network11,12.
We addressed the influence of fine scale landscape structure (1-10km) on V. berus genetics. The study site (10 × 7km), located in Brittany (France) is based on an agricultural landscape with a network of secondary roads surrounding a preserved Natura 2000 site (4.4 km² of woods, heathland and a hedgerows network). We hypothesized that gene flow would be lower in the agricultural landscape than in the preserved habitat. Accordingly, we expected to find a unique genetic cluster in the Natura 2000 site, within which only weak Isolation-By-Distance (IBD) would be detectable owing to habitats proximity at a fine spatial scale (< 3km). In contrast, we expected several clusters in the rest of the study area, with a strong genetic structure probably related to Isolation-By-Resistance (IBR) or Barriers (IBB) caused by roads or agricultural areas.
In 2015-2016, we set up a targeted and nested sampling design with replicates according to an Individuals-based Sampling Scheme (ISS). This allowed us to collect DNA samples from swabs for 281 adults V. berus in 81 “aggregates” (i.e. localities with 4 to 5 individuals13 found less than 200m from each other). This sampling method is particularly adapted to detect contemporary effects14 and for its flexibility13, which is effective to sample species with a secretive nature and a continuous distribution15,16.
Our clustering analysis reveals a single cluster in the whole area. We also detected a strong IBD effect, not only in the preserved zone but on the whole study area. Mantel correlograms under IBD revealed a significant difference of spatial autocorrelation between sexes, with males dispersing more. However, IBD is not sufficient to explain genetic variation for some pairs of individuals. We expect therefore that landscape features will provide additional information to understand genetic variation in the study area.


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