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The objective of the study was to establish and refine a method for the genomic characterization of European hedgehogs in Denmark using the second-generation genotyping technique, genotyping by sequencing (GBS). Single nucleotide polymorphisms (SNPs) were filtered with a read coverage between 20 - 100 and a maximum number of missing data of 25 %. Individuals with > 25 % missing data were removed yielding a total of 2.4 million SNPs, and after filtering for Minor allele frequency (MAF) >1 %, 2902 SNPs remained. Approximately half of the individuals analysed contained less than 75% of the selected SNPs, and were removed, resulting in a sample size of 30. We estimated inbreeding coefficients (F), observed (HO), expected (HE) and unbiased expected (uHE) heterozygosity and the percent of polymorphic loci (P%). We tested for deviations from Hardy-Weinberg equilibrium (HWE) and patterns of isolation by distance (IBD). We assessed the genetic structure of the sampled individuals based on a Bayesian clustering method, and tested for recent population expansion or decline. We found a P% = 94.5%, a uHE and HE of mean ± SE; 0.31 ± 0.04 and 0.30 ± 0.02, respectively and an HO of 0.290 ± 0.03. The heterozygosity deficiency was reflected in a positive F-value; 0.1 ± 0.01 and a significant deviation for HWE (p < 0.05). The Mantel test for association between the genetical and geographical distances of populations was not significant (b = 0.007, R = 0.145, p > 0.05). The significant and positive F-value found, was explained by inbreeding, genetic substructure and low effective population size (Ne) which are all consequences of habitat fragmentation. We failed to detect recent signs of a population bottleneck or expansion. Further studies on a larger scale are needed to obtain a general view of the conservation status of the Danish hedgehog population.
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Genetics and Biodiversity Journal
Journal homepage:http://ojs.univ-tlemcen.dz/index.php/GABJ
Original Research Paper
Rasmussen S. L 1, Yashiro E2 , Sverrisdóttir E2 , Nielsen K.L2, Lukassen M.B 2, Nielsen
J. L2 , Asp T 3 , Pertoldi C2,4
1Department of Biology, University of Southern Denmark, Odense M, Denmark;
2Department of Chemistry and Bioscience, Aalborg University, Aalborg, Denmark;
3Department of Molecular Biology and Genetics, Aarhus University, Slagelse,Denmark;
4Aalborg Zoo, Aalborg, Denmark
Corresponding Author: Sophie Lund Rasmussen, University of Southern Denmark, Odense,
Denmark; Email: sophielundrasmussen@gmail.com
Article history; Received: 27 May 2019 ; Revised: 2 June 2019; Accepted: 22 June 2019
Abstract
The objective of the study was to establish and refine a method for the genomic characterization of European
hedgehogs in Denmark using the second-generation genotyping technique, genotyping by sequencing (GBS).
Single nucleotide polymorphisms (SNPs) were filtered with a read coverage between 20 - 100 and a maximum
number of missing data of 25 %. Individuals with > 25 % missing data were removed yielding a total of 2.4 million
SNPs, and after filtering for Minor allele frequency (MAF) >1 %, 2902 SNPs remained. Approximately half of
the individuals analysed contained less than 75% of the selected SNPs, and were removed, resulting in a sample
size of 30. We estimated inbreeding coefficients (F), observed (HO), expected (HE) and unbiased expected (uHE)
heterozygosity and the percent of polymorphic loci (P%). We tested for deviations from Hardy-Weinberg
equilibrium (HWE) and patterns of isolation by distance (IBD). We assessed the genetic structure of the sampled
individuals based on a Bayesian clustering method, and tested for recent population expansion or decline. We
found a P% = 94.5%, a uHE and HE of mean ± SE; 0.31 ± 0.04 and 0.30 ± 0.02, respectively and an HO of 0.290 ±
0.03. The heterozygosity deficiency was reflected in a positive F-value; 0.1 ± 0.01 and a significant deviation for
HWE (p < 0.05). The Mantel test for association between the genetical and geographical distances of populations
was not significant (b = 0.007, R = 0.145, p > 0.05). The significant and positive F-value found, was explained by
inbreeding, genetic substructure and low effective population size (Ne) which are all consequences of habitat
fragmentation. We failed to detect recent signs of a population bottleneck or expansion. Further studies on a larger
scale are needed to obtain a general view of the conservation status of the Danish hedgehog population.
Keywords:Structure; SNPs; Bottleneck;Effective population size; European hedgehog;Erinaceus
europaeus;Habitat fragmentation;
Introduction
The western European hedgehog (Erinaceus europaeus), is a hedgehog species found on the British
Isles and Continental Europe, from Iberia and Italy northwards into Scandinavia, as well as on New
Zealand. It is a generally common and widely distributed species that can survive across a wide range
of habitat types (Morris, 2014; Reeve, 1994). However, previous research on both national and local
scale has documented decline or indicated concerns for decline of the hedgehog populations in several
western European countries (Hof and Bright, 2016; Krange, 2015; Müller, 2018; SoBH, 2011; 2015;
2018; van de Poel et al., 2015; Williamset al., 2018). There is currently no data to indicate the status of
the Danish population of hedgehogs, but nonetheless, the situation may be similar in Denmark, due to
comparable habitat fragmentation, landscape structure, farm management practices and climate in the
western European countries. The suspected reasons for the decline are habitat loss and habitat
Applying the GBS technique for the genomic characterization of
a Danish population of European hedgehogs (Erinaceus
europaeus)
Rasmussen et al., (2019) Gen. Biodiv. J: 3(2), 78-86
79
fragmentation, intensified agricultural practices, road traffic accidents, molluscicide and rodenticide
poisoning and badger predation (Brakes and Smith, 2005; Dowdinget al., 2010a; Dowding et al., 2010b;
Haighet al., 2012; Hof and Bright, 2010; Hubertet al., 2011; Huijser and Bergers, 2000; Pettettet al.,
2017; SoBH, 2011; Younget al., 2006).
Hedgehogs are nocturnal and non-territorial and can travel up to 2-3 km per night. Home ranges of adult
hedgehogs are generally estimated to be 20-30 ha for males and 10 ha for females, expanding
temporarily during the mating season (Morris, 2014). Juvenile hedgehogs do not disperse far from their
natal area when reaching independence (Sæther, 1997), and adult hedgehogs seem to remain in the same
area throughout their lives (Reeve, 1994). Previous studies furthermore indicate that relocated
individuals do not disperse very far even when released into an unfavourable habitat (Doncasteret al.,
2001).
During the past 20-30 years, the rehabilitation of sick, orphaned and injured wild hedgehogs has become
an established practice in many western European countries. Denmark has several working hedgehog
rehabilitation centers, where volunteers care for the hedgehogs and release them back into the wild,
when they have recovered. The extent of hedgehog rehabilitation in Denmark is quite comprehensive,
and there has been a tendency to transport hedgehogs over barriers such as seas for rehabilitation, and
to release individuals in foreign habitats. Only recently have the Danish authorities established legal
frameworks and monitoring programs for the practice of wildlife rehabilitation.
Genetic investigations of European hedgehogs have previously been conducted using microsatellites
(Becher and Griffiths, 1997; 1998; Berggren et al., 2005; Bolfikova and Hulva, 2012; Bolfikova et al.,
2013; Bolfikovaet al., 2017; Braakeret al., 2017; Fraseret al., 2012; Henderson et al., 2000; Moran et
al., 2009; Santucci et al., 1998; Seddon et al., 2001). In this study the use of a genotyping by sequencing
(GBS) (Elshireet al., 2011;Narum et al., 2013; Nørgaard et al., 2017; Pellegrino et al., 2016; Pertoldi
and Randi, 2018) was adapted and optimized for the genetic analysis of European hedgehogs.
The flourishing discipline of citizen science, defined as the involvement of citizens from the non-
scientific community in academic research, has gained increasing importance in the field of conservation
biology. Citizen science provides researchers with an opportunity to obtain information that would
otherwise be impossible to collect due to time and resource constraints, and offers motivated citizens an
opportunity to contribute to scientific understanding and conservation through voluntary biological
monitoring (Chandler et al., 2017; Conrad and Hilchey, 2011; Tulloch et al., 2013).The collection of
genetic samples for the present study was successfully based on a citizen science approach.
The main aims of the experiment were: (1) To provide a set of SNPs, which can be used for investigating
the genetic structure and variability of the European hedgehog on a broader scale (2) to evaluate the
patterns of the genetic diversity distribution in the population of Danish hedgehogs in Jutland south of
the Limfjord (Figure 1) and (3) ascertain the historical changes in their effective population size (Ne)
through genetic signatures.
Materials and methods
The genetic samples were obtained as part of a nationwide citizen science project in Denmark, where
volunteers were encouraged to collect dead hedgehogs, from May to December 2016, record the date
and location of the find, and deliver the hedgehog carcasses to one of 26 collection stations distributed
nationally. A total of 697 dead hedgehogs were collected. The hedgehog carcasses were stored at -20
°C. They were subsequently necropsied, and tissue samples from skin and muscle were extracted for
the present research. Afterwards, the samples were stored at -20°C. The subsample used in this study
was based on tissues from 62 hedgehogs collected on the Jutland Peninsula in southern Denmark.
Sample Preparation
DNA was extracted from 1-2 g of hedgehog tissue using the DNeasy Blood and Tissue kit (QIAGEN,
Germany) following the manufacturer’s instructions. The DNA samples (yield >0.5 mg/g tissue with
Rasmussen et al., (2019) Gen. Biodiv. J: 3(2), 78-86
80
minimal sign of degradation) were digested with Sau96I (NEB) and ligated to adapters following the
GBS protocol developed previously (Elshireet al. 2011). The ligated samples were pooled into 4
different pools and purified with AMPure XP beads (Beckman Coulter, USA). PCR amplification was
performed on the 4 sample pools in 50 µL volumes containing approximately 50 ng pooled DNA using
the Phusion High-Fidelity PCR kit (Thermo Scientific, USA) with the following program: 72 °C in 5
min, 98 °C in 30 sec, followed by 20 cycles of 98 °C in 10 sec, 66 °C in 30 sec and 72 °C in 30 sec,
with a final extension at 72 °C in 5 min. The pools were then purified with AMPure XP beads (Beckman
Coulter, USA) after which the DNA concentration was determined by Qubit (Thermo Scientific, USA)
and visualized on the TapeStation 2200 using a D1000 Screen Tape (Agilent, USA). Paired-end 2x151
bp sequencing was run on the Illumina HiSeq X platform at Admera Health (South Plainfield, NJ, USA).
Filtering Raw Sequence Data, Mapping and SNP Calling
The i7 barcodes of the dual-barcoded sequenced reads were first de multiplexed with bcl2fastq2 version
1.0.0 (Illumina, Inc., San Diego, CA, USA) using zero mismatch allowance. Fastq-multx version
1.02.772 (https://github.com/brwnj/fastq-multx) was then used with one mismatch allowance to de
multiplex the custom i5 barcodes (Elshireet al., 2011) and to remove the barcode sequences from the
sequenced reads. Adaptor contamination and quality trimming was performed using Trim Galore with
default parameters (http://www.bioinformatics.babraham.ac.uk/projects/trim_galore). Burrows-
Wheeler Aligner (http://bio-bwa.sourceforge.net/) (BWA) was used to align the reads against the
European hedgehog (Erinaceus europaeus), EriEur 2.26 reference genome
(http://hgdownload.cse.ucsc.edu/downloads.html). Reads with a mapping quality of at least 30 were
kept. Variants were called using The Genome Analysis Tool Kit’s Haplotype Caller
(https://software.broadinstitute.org/gatk/documentation/tooldocs/3.80/org_broadinstitute_gatk_tools_
walkers_haplotypecaller_HaplotypeCaller.php). Joint genotyping was performed using Genotype
GVCFs(https://software.broadinstitute.org/gatk/documentation/tooldocs/3.80/org_broadinstitute_gatk
_tools_ walkers_variantutils_GenotypeGVCFs.php). Initial filtering was performed using Select
Variants(https://software.broadinstitute.org/gatk/documentation/tooldocs/3.80/org_broadinstitute_gatk
_tools_walkers_variantutils_SelectVariants.php) and filtered for SNPs, bi-allelic sites, and mapping
quality > 30 (DePristoet al., 2011). Minor allele frequency (MAF) was estimated from the read coverage,
and SNPs were filtered on a minimum MAF of 1 % (average variant allele frequency <0.99 and >0.01).
Additionally, SNPs were filtered with a read coverage between 20 and 100 and a maximum number of
missing data of 25 %. Individuals with more than 25 % missing data were removed.
Population Genetic Variability and Structure
Inbreeding coefficient (F) observed (HO), expected (HE), unbiased expected (uHE) heterozygosity and
the percent of polymorphic loci (P%), were estimated using GENALEX v. 6.5 (Peakall and Smouse,
2012). The software GENEPOP 3.4 was used for testing for deviations from Hardy-Weinberg
equilibrium (HWE) (Raymond and Rousset, 1995). GENALEX v.6.5 (Peakall and Smouse, 2012) was
also used for checking if a pattern of isolation by distance could be found within every population
investigated (Mantel, 1967). The geographic distance connecting samples was represented by Euclidean
(linear geographic) distances computed in QGis(QGIS Development Team, 2019). Population genetic
structure of the sampled individuals (N = 30), was assessed based on a Bayesian clustering method,
implemented in the STRUCTURE v. 2.3.; 10 independent runs of K = 1- 10 were carried out on the
populations with 106 Markov chain Monte Carlo (MCMC) iterations and 105 burn-in period on the basis
of independent allele frequencies and admixture ancestry model (Pritchard et al., 2000).
Assessment of the Demographic History
Signature of a recent abrupt decline in the population size was evaluated by the program
BOTTLENECK v. 1.2, after 10.000 iterations under infinite allele model (IAM) according to an excess
of the heterozygosity and deficiency of the rare alleles (Luikart and Cornuet, 1998; Luikart et al., 2010).
Rasmussen et al., (2019) Gen. Biodiv. J: 3(2), 78-86
81
Results
Genotypes
A total of 2.4 million SNPs were found. Following filtering for MAF >1 % estimated from read
coverage, maximum missing data of 25 %, and read coverage between 20 and 100, 2902 SNPs remained.
Approximately half, 32 of the original 62, individuals that contained less than 75 % of the selected SNPs
were removed, resulting in 30 individuals remaining for the further investigation. See Figure 1 for an
illustration of the locations of the subsample 30 individuals used in the study.
Figure 1. Map of Denmark indicating the sampling locations (black dots) of the subsample of 30
hedgehogs collected on the peninsula of Jutland, Denmark and the locations of the twelve hedgehog
collection stations (blue crosses) situated in Jutland, Denmark.
Genetic Variability and Structure
The level of polymorphism found was high; P% = 94.5 %, theuHE and HE estimated were quite similar;
mean ± SE = 0.31 ± 0.04 and 0.30 ± 0.02, respectively, whereas the HO was lower; 0.290 ± 0.03. The
heterozygosity deficiency is reflected in a positive F-value; 0.1 ± 0.01 and a significant deviation for
HWE (p < 0.05).
The Bayesian clustering of the genotyped data assigned the highest posterior probability; Estimated Ln
Prob of Data = -147679.1, Mean value of ln likelihood = -147032.9, Variance of ln likelihood = 810.4,
for K = 1.
Rasmussen et al., (2019) Gen. Biodiv. J: 3(2), 78-86
82
The Mantel test for association between the genetic and geographical distances of populations was not
significant (b = 0.007, R = 0.145), indicating that only about 2.1% (i.e. R2 = 0.1452= 0.021) of the
genetic divergence was explained by geographical distance.
Population Bottlenecks and Expansion
The population investigated failed to show a significant deficiency or excess in heterozygosity, which
could indicate expansions or reduction in population size, respectively (p > 0.05).
Discussion
The level of genetic variability in the present study (HE = 0.30 and HO = 0.29) was considerably low
compared to the mean HE = 0.62 and HO = 0.44 based on 41 European hedgehogs in a study conducted
by Curto et al. (2019) using SNPs markers. The level of genetic variability was also lower than the
variability found using microsatellites markers in the same study: HE=0.51 and HO = 0.35, likely because
their study used individuals representing different countries across the European continent and thereby,
was conducted on a much broader scale. The island structure of Denmark furthermore limits the gene
flow. However, the individual hedgehogs chosen for the present study all derive from the peninsula of
Jutland, which is connected to Germany, which could lead to an increased gene flow compared to the
rest of Denmark, which consists of islands.
The low level of genetic variability and the significant and positive F-value, which indicate a significant
deviation from HWE, are probably explained by inbreeding, genetic substructure and low Ne which can
be due to habitat fragmentation, the limited dispersal behaviour of hedgehogs and relocation of
rehabilitated hedgehogs (Becher and Griffiths, 1998; Bolfikova and Hulva, 2012; Braakeret al., 2017).
Despite the deviation from HWE in the present study, the STRUCTURE analysis failed to find further
substructuring and the Mantel test failed to find an isolation by distance effect. The low R2 value is not
due to low power of the test as the sample size utilised for the regression analysis is large. The reasons
could be due to the low level of genetic variability found in this investigation which have probably
cancelled out the Wahlund effect which produce a heterozygosity deficiency due to the lack of panmixia.
The relatively low number of individual hedgehogs included in the analysis (30 individuals after
filtering) could also account for the lack of statistical power (and thereby lack of significance) in our
analyses, especially given the low level of genetic variability among the sampled Danish population.
The software BOTTLENECK 1.2. failed to detect signs of population bottlenecks or expansions.
However, the software is only able to detect recent decreases or increases in population size, within 0.2
Ne to 0.4 Ne generations. We therefore cannot reject the hypothesis that the Danish hedgehog population
has declined before the scope of 0.2 to 0.4 Ne generations.
Conclusion
We developed a successful and effective method for the genomic characterization of European
hedgehogs in Denmark using the GBS technique with 2.4 million detected SNPs. The low level of
genetic variability and the significant and positive F-value found in the subsample of Danish hedgehogs
may be explained by inbreeding, genetic substructure and extremely low Ne, which could be due to
habitat fragmentation, relocation of rehabilitated hedgehogs, the limited dispersal behaviour of
hedgehogs and the general island structure of Denmark. We failed to detect recent signs of a population
bottleneck or expansion (within 0.2 Ne to 0.4 Ne generations). However, this does not rule out the
possibility that the hedgehog population of Jutland has previously undergone a decline.
By integrating population genetics and conservation biology, further studies with a larger sample size,
representative of the general hedgehog population of Denmark, would enable a conclusion on the
conservation status of the Danish hedgehog population. A relevant future focus of research would be to
compare individual heterozygosity with measures of health e.g. parasite load, dental health, toxicology
and presence/absence of cancer, to understand how the low genetic variability detected in the present
study affects hedgehogs at an individual level.
Rasmussen et al., (2019) Gen. Biodiv. J: 3(2), 78-86
83
Acknowledgements
We thank Dr Rien van Wijk and research assistant Camilla Birch for helping with the hedgehog
necropsies and the Natural History Museum of Denmark for offering to share their facilities for the
necropsies. We furthermore thank DrRien van Wijk for preparing the map for Figure 1. Finally, we
thank two anonymous Reviewers for invaluable suggestions and help.
Funding Information
The research was funded by the Aalborg Zoo Conservation Foundation (AZCF; grant number: 5-2017),
Naturama, 15. Juni Fonden, Beckett Fonden, Svalens Fond, Fonden til Værn for Værgeløse Dyr, Iwan
Kliem Larsens Mindelegat, Ingeniør K. A. Rohde og hustrus legat and Bodil Pedersen Fonden.
Authors Contributions
Sophie Lund Rasmussen: Original idea, managing and gathering the collection of samples, extraction
of samples, data analyses, writing of the manuscript as first author and corresponding author.
Erika Yashiro and Jeppe Lund Nielsen: Designing the molecular analysis and editing of the manuscript.
Elsa Sverrisdóttir, Kåre Lehmann Nielsen, Mie Bech Lukassen and Torben Asp: Bioinformatics.
Cino Pertoldi: Supervising laboratory work, bioinformatics, data analyses, writing of manuscript,
responsibility for supervision of the writing of the first author in the role as last author.
Ethics
No ethical issues to declare.
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... In Germany, only two long-term monitoring studies on a very local scale exist, showing similar decreases to those in the UK [6,7], and concerns about the decline in hedgehogs have also been expressed in other European countries [1, 8,9]. The underlying mechanisms causing these declines are certainly complex and multifactorial, including habitat loss, interspecific competition, road collisions, and the intensification of agriculture [4,[10][11][12][13][14]. Due to increasing fragmentation and decreasing density of hedgehog populations, the danger of the formation of island populations and inbreeding is already being discussed [15][16][17][18]. ...
... Hedgehogs could therefore be led around dangerous areas such as roads by building dark corridors using vegetation and reduced illumination through streetlights. Apart from the threat of being killed in traffic, hedgehog populations in urban areas might face genetic isolation [16][17][18]. Bridging parks with dark corridors could help to safely connect isolated populations from different parks and thus increase genetic diversity. In this regard, empirical studies examining the sensory capabilities of hedgehogs using streetlights of different wavelengths and intensities would be helpful. ...
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With urban areas growing worldwide comes an increase in artificial light at night (ALAN), causing a significant impact on wildlife behaviour and its ecological relationships. The effects of ALAN on nocturnal and protected European hedgehogs (Erinaceus europaeus) are unknown but their identification is important for sustainable species conservation and management. In a pilot study, we investigated the influence of ALAN on the natural movement behaviour of 22 hedgehogs (nine females, 13 males) in urban environments. Over the course of four years, we equipped hedgehogs at three different study locations in Berlin with biologgers to record their behaviour for several weeks. We used Global Positioning System (GPS) tags to monitor their spatial behaviour, very high-frequency (VHF) loggers to locate their nests during daytime, and accelerometers to distinguish between active and passive behaviours. We compared the mean light intensity of the locations recorded when the hedgehogs were active with the mean light intensity of simulated locations randomly distributed in the individual’s home range. We were able to show that the ALAN intensity of the hedgehogs’ habitations was significantly lower compared to the simulated values, regardless of the animal’s sex. This ALAN-related avoidance in the movement behaviour can be used for applied hedgehog conservation.
... Microsatellite genotyping has also been used to study the biological invasion process of E. europaeus as an allochthonous species in New Zealand (Bolfíková et al. 2013) and Pianosa Island, Italy (Iannucci et al. 2019). In Denmark, using single nucleotide polymorphisms (SNPs) genotyping, Rasmussen et al. (2019b; found low genetic diversity values (H S = 0.13-0.32) and high population differentiation (F ST = 0.03-0.32) ...
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Anthropogenic habitat fragmentation and roadkill mortality are considered important threats to European hedgehogs. Habitat fragmentation isolates hedgehog populations and, as a consequence, reduces their genetic diversity and leads the populations to vulnerable situations. The hedgehog populations in the Iberian Peninsula represent the southern limit of the species. We used microsatellite markers to estimate the genetic diversity and population structure of Erinaceus europaeus on the Iberian Peninsula. The obtained results indicated the presence of two differentiated groups, north-western and north-eastern, which coincided with the distribution of the two phylogeographic mitochondrial lineages described in the Peninsula. Moreover, in the north-eastern group, three genetically different clusters (Girona, Central Catalonia and Zoo) were identified. The highest genetic diversity ( Hs = 0.696) was detected in the north-western region. Significant genetic differentiation ( F ST range = 0.072–0.224) was found among the clusters, indicating that these groups are well differentiated and present low gene flow. We concluded that the north-western group is genetically stable, whereas in the north-eastern region, despite some contact among groups, some populations are isolated and vulnerable.
... It is widely distributed and can survive across a wide range of habitat types [1,2]. However, investigations on both national and local scales have documented declines, or expressed concerns about decline, of the hedgehog populations in several western European countries [3][4][5][6][7][8][9][10]. The suspected reasons for the decline include habitat loss and fragmentation, intensified agricultural practices, inbreeding, road traffic accidents, lack of biodiversity and suitable nest sites in residential gardens, molluscicide and rodenticide poisoning, and badger predation [4,[11][12][13][14][15][16][17][18][19][20][21][22][23]. In Denmark, where this study occurred, hedgehogs become active after hibernation in mid-April to mid-May [22,24,25]. ...
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Background The European population of hedgehogs ( Erinaceus europaeus ) is declining. It is therefore essential to optimise conservation initiatives such as the rehabilitation of sick, injured and orphaned hedgehogs. Wild animals placed in captivity may be prone to chronic stress, potentially causing negative health effects. Therefore, the effects of these rehabilitation efforts should consequently be evaluated. Furthermore, hand-raising orphaned hedgehogs is a laborious and costly task, and it is therefore relevant to document whether they have equal post release survival rates compared to their wild conspecifics. The objectives of this research were therefore to conduct an exploratory study of glucocorticoid levels in hedgehogs from different backgrounds and compare the post release survival of translocated, rehabilitated and wild, juvenile hedgehogs as well as the possible effect on survival of differences in shy or bold behaviour (personality) exhibited by individuals. Results We measured glucocorticoid levels in 43 wild-caught (n = 18) and rehabilitated (n = 25) hedgehogs and compared the post release survival and spatial behaviour of 18 translocated juvenile hedgehogs (eight hand-raised and ten wild) until hibernation. The possible effect on survival of differences in shy or bold behaviour (personality) exhibited by 17 juvenile individuals (seven hand-raised and ten wild) was also examined. Rehabilitated individuals and females had higher levels of faecal corticosterone metabolites compared to wild individuals and males, respectively. Rehabilitated individuals showed higher levels of saliva corticosterone than wild. The personality tests labelled 13 individuals as shy and 11 as bold. Post release survival was 57% for rehabilitated and 50% for wild individuals. Neither background nor personality affected post release survival. Home range measures were 3.54 and 4.85 ha. Mean dispersal length from the release sites was 217 ± 100 m. Conclusion The higher levels of corticosterone observed in rehabilitated compared to wild hedgehogs calls for consideration of the duration of admission to wildlife rehabilitation centres to reduce stress levels in the patients. Hand-raised juveniles appear to have the same prospects as wild, and personality does not seem to affect post release survival in hedgehogs, indicating that hand-raising of orphaned juvenile hedgehogs is a relevant contribution to the conservation of this species.
... Long-term monitoring studies found that the overall hedgehog population in several countries is declining, sometimes dramatically so [21][22][23][24]. The underlying mechanisms responsible for these declines are likely to be complex and multifactorial, including habitat loss, interspecific competition, traffic accidents and intensification of agriculture [21,[25][26][27][28]. Increasing fragmentation and decreasing hedgehog densities may cause negative genetic effects associated with isolated populations [29][30][31][32]. Usually, urban green spaces such as public parks are favourable environments for urban hedgehogs, providing easily accessible food and resting (nest) sites. ...
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Anthropogenic activities can result in both transient and permanent changes in the environment. We studied spatial and temporal behavioural responses of European hedgehogs (Erinaceus europaeus) to a transient (open-air music festival) and a permanent (highly fragmented area) disturbance in the city of Berlin, Germany. Activity, foraging and movement patterns were observed in two distinct areas in 2016 and 2017 using a “Before & After“ and “Control & Impact“ study design. Confronted with a music festival, hedgehogs substantially changed their movement behaviour and nesting patterns and decreased the rhythmic synchronization (DFC) of their activity patterns with the environment. These findings suggest that a music festival is a substantial stressor influencing the trade-off between foraging and risk avoidance. Hedgehogs in a highly fragmented area used larger home ranges and moved faster than in low-fragmented and low-disturbed areas. They also showed behaviours and high DFCs similar to individuals in low-fragmented, low disturbed environment, suggesting that fragmentation posed a moderate challenge which they could accommodate. The acute but transient disturbance of a music festival, therefore, had more substantial and severe behavioural effects than the permanent disturbance through fragmentation. Our results are relevant for the welfare and conservation measure of urban wildlife and highlight the importance of allowing wildlife to avoid urban music festivals by facilitating avoidance behaviours.
... Paired-end (2x151 bp) sequencing was performed on an Illumina HiSeq X platform by Admera Health (USA). The described method was previously tested in a pilot study using a few individuals from South Jutland by [63]. ...
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Objectives Low genetic diversity can lead to reduced average fitness in a population or even extinction. Preserving genetic connectivity across fragmented landscapes is therefore vital to counteract the negative consequences of genetic drift and inbreeding. This study aimed to assess the genetic composition and consequently the conservation status of a nationwide sample of European hedgehogs (Erinaceus europaeus) in Denmark. Methods We applied an adaptation of the genotyping by sequencing (GBS) technique to 178 individuals from six geographically distinct populations. We used a Bayesian clustering method to subdivide individuals into genetically distinct populations. We estimated individual observed (iH O), observed (H O), and unbiased expected (uH E) heterozygosity, inbreeding coefficient (F IS), percentage of polymorphic loci (P%) and tested for deviations from Hardy-Weinberg equilibrium (HWE). We used linear models to test for potential anthropogenic effects on the genetic variability of hedgehogs with iH O , uH E, P% and F IS as response variables, and assessed the demographic history of the population. Results The Danish hedgehog population is composed of three genetic clusters. We found a mean P% of 54.44-94.71, a mean uH E of 0.126-0.318 and a mean H O of 0.124-0.293 in the six populations. The F IS was found to be significantly positive for three of the six populations. We detected a large heterogeneity of iH O values within populations, which can be due to inbreeding and/or fragmentation. F IS values decreased with increasing farmland density, but there was no significant association with human population or road density.
... Paired-end (2x151 bp) sequencing was performed on an Illumina HiSeq X platform by Admera Health (USA). The described method was previously tested in a pilot study using a few individuals from South Jutland by [63]. ...
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Objectives Low genetic diversity can lead to reduced average fitness in a population or even extinction. Preserving genetic connectivity across fragmented landscapes is therefore vital to counteract the negative consequences of genetic drift and inbreeding. This study aimed to assess the genetic composition and consequently the conservation status of a nationwide sample of European hedgehogs (Erinaceus europaeus) in Denmark. Methods We applied an adaptation of the genotyping by sequencing (GBS) technique to 178 individuals from six geographically distinct populations. We used a Bayesian clustering method to subdivide individuals into genetically distinct populations. We estimated individual observed (iHO), observed (HO), and unbiased expected (uHE) heterozygosity, inbreeding coefficient (FIS), percentage of polymorphic loci (P%) and tested for deviations from Hardy-Weinberg equilibrium (HWE). We used linear models to test for potential anthropogenic effects on the genetic variability of hedgehogs with iHO, uHE, P% and FIS as response variables, and assessed the demographic history of the population. Results The Danish hedgehog population is composed of three genetic clusters. We found a mean P% of 54.44–94.71, a mean uHE of 0.126–0.318 and a mean HO of 0.124–0.293 in the six populations. The FIS was found to be significantly positive for three of the six populations. We detected a large heterogeneity of iHO values within populations, which can be due to inbreeding and/or fragmentation. FIS values decreased with increasing farmland density, but there was no significant association with human population or road density. Conclusions We found a low level of genetic variability and evidence for genetic substructure and low effective population size, which are all consequences of habitat fragmentation. We failed to detect signs of a recent population bottleneck or population increase or decline. However, because the test only identifies recent changes in population size, we cannot reject the possibility of a longer-term decline in the Danish hedgehog population.
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The European hedgehog population is declining in Europe. It is therefore important to investigate the causes for the decline and monitor the general health of the species. We investigated the endoparasite occurrence in 299 dead European hedgehogs. Of these, endoparasites were detected in 69% of the individuals tested. We identified Crenosoma striatum, Capillaria aerophila (syn. Eucoleus aerophilus), Capillaria spp., coccidia, Cryptosporidium spp., Brachylaemus spp. and Capillaria hepatica. We also examined the hedgehogs for Giardia spp. and Echinococcus multilocularis but all were negative. Coccidia (n = 7, 2.5%) and Cryptosporidium spp. (n = 14, 5.2%) were only detected in individuals from Zealand, Lolland and Jutland south of the Limfjord. Single cases of Brachylaemus spp. (n = 1, 0.4%) and Capillaria hepatica (n = 1, 1.1%) were exclusively discovered in Jutland south and north of the Limfjord, respectively. These results indicate a regional difference in endoparasite species carried by European hedgehogs in Denmark. This stresses the need for hedgehogs to be cared for locally when admitted to wildlife rehabilitation centres, and to be released within their area of origin, to prevent spread of endoparasite infections among hedgehogs. Additionally, we explored the following possible determinants of parasite infection in the hedgehogs: sex, age, mortality category (in-care, natural and roadkill), infection with MRSA, genetic heterozygosity, month of death, geographical location and habitat type, and found that only age had a statistically significant effect on endoparasite prevalence, as we detected a lower occurrence of endoparasites in juvenile hedgehogs (
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By applying second‐generation sequencing technologies to microsatellite genotyping, sequence information is produced which can result in high‐resolution population genetics analysis populations and increased replicability between runs and laboratories. In the present study, we establish an approach to study the genetic structure patterns of two European hedgehog species Erinaceaus europaeus and E. roumanicus. These species are usually associated with human settlements and are good models to study anthropogenic impacts on the genetic diversity of wild populations. The short sequence repeats genotyping by sequence (SSR‐GBS) method presented uses amplicon sequences to determine genotypes for which allelic variants can be defined according to both length and single nucleotide polymorphisms (SNPs). To evaluate whether complete sequence information improved genetic structure definition, we compared this information with datasets based solely on length information. We identified a total of 42 markers which were successfully amplified in both species. Overall, genotyping based on complete sequence information resulted in a higher number of alleles, as well as greater genetic diversity and differentiation between species. Additionally, the structure patterns were slightly clearer with a division between both species and some potential hybrids. There was some degree of genetic structure within species, although only in E. roumanicus was this related to geographical distance. The statistically significant results obtained by SSR‐GBS demonstrate that it is superior to electrophoresis‐based methods for SSR genotyping. Moreover, the greater reproducibility and throughput with lower effort which can be obtained with SSR‐GBS and the possibility to include degraded DNA into the analysis, allow for continued relevance of SSR markers during the genomic era.
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Agricultural landscapes have become increasingly intensively managed resulting in population declines across a broad range of taxa, including insectivores such as the hedgehog (Erinaceus europaeus). Hedgehog declines have also been attributed to an increase in the abundance of badgers (Meles meles), an intra-guild predator. The status of hedgehogs across the rural landscape at large spatial scales is, however, unknown. In this study, we used footprint tracking tunnels to conduct the first national survey of rural hedgehog populations in England and Wales. Single and two-species occupancy modelling was used to quantify hedgehog occupancy in relation to habitat and predator covariates. Hedgehog occupancy was low (22% nationally), and significantly negatively related to badger sett density and positively related to the built environment. Hedgehogs were also absent from 71% of sites that had no badger setts, indicating that large areas of the rural landscape are not occupied by hedgehogs. Our results provide the first field based national survey of hedgehogs, providing a robust baseline for future monitoring. Furthermore, the combined effects of increasing badger abundance and intensive agriculture may have provided a perfect storm for hedgehogs in rural Britain, leading to worryingly low levels of occupancy over large spatial scales.
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Conservation genetic disciplines have greatly progressed during the last thirty years, mainly thanks to the continuous development of molecular biological knowledge and the implementation of molecular tools used to describe diversity at the DNA level. The ongoing transition from Conservation genetics to Conservation genomics is showing to increase at an exponential speed as the integrated use of various kinds of molecular genetic data and bioinformatic approaches may improve our theoretical knowledge and practical approaches in the conservation and wise use of biodiversity. Aim of this mini-review is to push forward the ongoing transition, bearing in mind that most of the applied conservation programs would not need entire genomic data set, which are still expensive and time consuming.
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Although hedgehogs are well-known examples of postglacial recolonisation, the specific processes that shape their population structures have not been examined by detailed sampling and fast-evolving genetic markers in combination with model based clustering methods. This study aims to analyse the impacts of isolation within glacial refugia and of postglacial expansion on the population structure of the Northern White-breasted hedgehog (Erinaceus roumanicus). It also discusses the role of the processes at edges of species distribution in its evolutionary history. The maternally inherited mitochondrial control region and the bi-parentally inherited nuclear microsatellites were used to examine samples within the Central Europe, Balkan Peninsula and adjacent islands. Bayesian coalescent inference and neutrality tests proposed a recent increase in the population size. The most pronounced pattern of population structure involved differentiation of the insular populations in the Mediterranean Sea and the population within the contact zone with E. europaeus in Central Europe. An interspecies hybrid was detected for the first time in Central Europe. A low genetic diversity was observed in Crete, while the highest genetic distances among individuals were found in Romania. The recent population in the post-refugial area related to the Balkan Peninsula shows a complex pattern with pronounced subpopulations located mainly in the Pannonian Basin and at the Adriatic and Pontic coasts. Detailed analyses indicate that parapatry and peripatry may not be the only factors that limit range expansion, but also strong microevolutionary forces that may change the genetic structure of the species. Here we present evidence showing that population differentiation may occur not only during the glacial restriction of the range into the refugia, but also during the interglacial range expansion. Population differentiation at the Balkan Peninsula and adjacent regions could be ascribed to diversification in steppe/forest biomes and complicated geomorphology, including pronounced geographic barriers as Carpathians. How to cite this article Černa Bolfíková et al. (2017), Glacial allopatry vs. postglacial parapatry and peripatry: the case of hedgehogs.
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The raccoon dog (Nyctereutes procyonoides) has a wide distribution in Europe and is a prominent example of a highly adaptable alien species. It has been recorded sporadically in Denmark since 1980 but observations since 2008 suggested that the species had established a free-ranging, self-sustaining population. To elucidate the origin and genetic patterns of Danish raccoon dogs, we studied the population genomics of 190 individuals collected in Denmark (n = 141) together with reference captive individuals from Poland (n = 21) and feral individuals from different European localities (Germany, Poland, Estonia and Finland, n = 28). We used a novel genotyping-by-sequencing approach simultaneously identifying and genotyping a large panel of single nucleotide polymorphisms (n = 4526). Overall, there was significant indication for contemporary genetic structuring of the analysed raccoon dog populations, into at least four different clusters, in spite of the existence of long distance gene flow and secondary admixture from different population sources. The Danish population was characterized by a high level of genetic admixture with neighbouring feral European ancestries and the presence of private clusters, non-retrieved in any other feral or captive populations sampled. These results suggested that the raccoon dog population in Denmark was founded by escapees from genetically unidentified Danish captive stocks, followed by a recent admixture with individuals migrating from neighbouring Germany.
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Badgers Meles meles are intraguild predators of hedgehogs Erinaceus europaeus and have been shown to have a major effect on their abundance and behaviour at a localized scale. Previous studies have predicted the exclusion of hedgehogs from rural habitats in areas where badgers are abundant. The two species coexist at the landscape scale, however, as hedgehogs use suburban habitats, which are thought to provide a refuge from the effects of badger predation. We carried out surveys of hedgehog abundance and studied the use of spatial refugia by hedgehogs in relation to badger density and distribution in 10 study sites in the Midlands and south-west regions of England. Surveys confirmed that hedgehogs were almost absent from pasture fields in rural habitats, with their distribution concentrated in amenity grassland fields in suburban areas. However, although suburban habitats are less frequently used by badgers than rural areas, and therefore represented spatial refugia for hedgehogs, the probability of occurrence and abundance of hedgehogs varied in relation to the density of badger setts in the surrounding area. As sett density increased, both the probability of occurrence of hedgehogs and their abundance decreased. A generalized linear model predicted that the probability of hedgehog occurrence in suburban habitats declined towards zero in areas of high badger density. The most probable explanation is the negative effect of high badger abundance on the ability of hedgehogs to move between patches of suburban habitat. The present study concords with results from previous surveys and experimental studies, which found a strong negative spatial relationship between hedgehogs and badgers. It also provides correlative evidence that intraguild predation can exclude intraguild prey from productive habitats.
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We describe a model-based clustering method for using multilocus genotype data to infer population structure and assign individuals to populations. We assume a model in which there are K populations (where K may be unknown), each of which is characterized by a set of allele frequencies at each locus. Individuals in the sample are assigned (probabilistically) to populations, or jointly to two or more populations if their genotypes indicate that they are admixed. Our model does not assume a particular mutation process, and it can be applied to most of the commonly used genetic markers, provided that they are not closely linked. Applications of our method include demonstrating the presence of population structure, assigning individuals to populations, studying hybrid zones, and identifying migrants and admixed individuals. We show that the method can produce highly accurate assignments using modest numbers of loci—e.g., seven microsatellite loci in an example using genotype data from an endangered bird species. The software used for this article is available from http://www.stats.ox.ac.uk/~pritch/home.html.