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Consequences for genetic diversity and population performance of introducing continental red deer into the northern distribution range
Abstract
For several centuries, game management has involved translocations of non-native individuals of many species to reinforce
local native populations. However, there are few quantitative studies of potentially negative effects on population viability
as expected when taxa with different local adaptations hybridise. The European red deer has been subject to particularly many
translocations. Around 1900, a total of 17 red deer of Hungarian (Cervus elaphus hippelaphus) and German (C. e. germanicus) origin were introduced onto the island of Otterøya in Norway where few native red deer (C. e. atlanticus) remained (n~13). To assess interbreeding, the present stock on Otterøya and the indigenous Norwegian and Hungarian populations
were characterised in 14 microsatellite loci and in the control region of mtDNA. An intermediate level of genetic variation
in the Otterøya population and the presence of population specific alleles from both the indigenous Norwegian and the Hungarian
population demonstrate that the introduced red deer interbred with the native. Even distributions of one indigenous and one
non-indigenous mtDNA haplotype in the Otterøya population and two point estimates of admixture indicate similar genetic contributions
from the two parental populations into the hybrid stock. Low numbers of migrants identified with Bayesian assignment tests
demonstrate low recent gene flow from Otterøya into the Norwegian mainland population. The Otterøya hybrid stock has grown
vastly in numbers during recent decades, suggesting a high population viability. We observed that the body mass of red deer
on Otterøya was similar or greater than in adjacent indigenous Norwegian stocks, indicating that population performance has
not been reduced in the hybrid stock and that gene flow probably has not had any negative effects.
KeywordsTranslocation-Hybrid stock-Introgression-Admixture-Dispersal
Supplementary resource (1)
Data
October 2010
... The genetic structure of large mammal species is affected by natural and anthropogenic factors. Anthropogenic impacts like selective hunting, translocations, and habitat destruction/fragmentation can blur natural patterns of genetic diversity and relationships (Frantz et al. 2006;Haanes et al. 2010;Dellicour et al. 2011;Carden et al. 2012;Stanton et al. 2016;Zachos et al. 2016;Galarza et al. 2017;Queirós et al. 2020). Such impacts, particularly in game species, can cause the disintegration of populations into several subpopulations with a more or less pronounced genetic exchange Willems et al. 2016;Iacolina et al. 2019;Mihalik et al. 2020). ...
... The red deer (Cervus elaphus L. 1758) is one of the most widespread and valuable European game species (Ludt et al. 2004;Milner et al. 2006). Consequently, its populations have been extensively managed, introduced, restocked, and selectively hunted for centuries or even millennia (Martínez et al. 2002;Haanes et al. 2010;Carden et al. 2012;Rivrud et al. 2013;Queirós et al. 2014;Hoffmann et al. 2016;Stanton et al. 2016;Frantz et al. 2017;Galarza et al. 2017). Furthermore, during the last decades, the keeping of deer in enclosures has spread all over the world, and the species is farmed for venison and antler products (Milner et al. 2006;Wada et al. 2010;Zachos and Hartl 2011;Bana et al. 2018). ...
... Studies on the genetic structure of European mammals, including red deer, based on mitochondrial DNA (mtDNA) sequences (Ludt et al. 2004;Skog et al. 2009;Niedziałkowska et al. 2011;Meiri et al. 2013;Frank et al. 2017;Rey-Iglesia et al. 2017;Queirós et al. 2019) as well as on microsatellites (Zachos et al. 2016;Frantz et al. 2017;Queirós et al. 2019) have shown the large-scale genetic pattern shaped by the Late Pleistocene and Holocene glacial-interglacial cycles. Local or regional red deer populations have also been extensively studied from a population genetic point of view, often taking into account anthropogenic influences (Kuehn et al. 2003;Zachos et al. 2003;Frantz et al. 2006;Hajji et al. 2008;Haanes et al. 2010;Dellicour et al. 2011;Radko et al. 2014;Krojerová-Prokešová et al. 2015;Borowski et al. 2016;Carranza et al. 2016;Hoffmann et al. 2016;Willems et al. 2016;Galarza et al. 2017). ...
After the last glacial, the Carpathian Basin was repopulated from either eastward or northward colonisation routes for various species; one of these was the emblematic member of the European megafauna, the red deer, Cervus elaphus. We analysed 303 red deer individuals from the middle of the region, in seven Hungarian game reserves, at ten microsatellite loci (C01, C229, T26, T108, T123, T156, T172, T193, T501, T507), to investigate the genetic diversity of these subpopulations. We discovered high levels of genetic diversity of red deer subpopulations; allelic richness values ranging 4.99-7.01, observed heterozygosity 0.729-0.800, polymorphic information content 0.722-0.806, and Shannon's information index 1.668-2.064. Multi-locus analyses indicated population admixtures of various degrees that corresponded to geographical location, and complex genetic structures were shown by clustering. Populations in the southwestern and the northeastern parts of the region formed two highly separated groups, and the red deer from populations in between them were highly admixed (in western Pannonia/Transdanubia, where the Danube flows into the Carpathian Basin). This pattern corresponds to the distribution of mitochondrial as well as Y-chromosome lineages. Assignment tests showed that a large fraction of individuals (29.4%) are found outside of their population of origin, indicating that the dispersal of red deer is rather common, which could be expected considering the life course of the species.
... Maraloid admixture, most likely artificially introduced from the Voronezh population, and the unexpected Tyrrhenian lineage, contribute a significant portion of the population's genetic diversity but serve to remove it further away from the characteristics of the autochthonous deer population that inhabited Belarus before the XVIII century . The exact extent of hybridization remains to be measured, and its effects on the fitness of the Belarusian red deer population are unpredictable (Haanes et al. 2010;Queiros et al. 2020). Additional research into the genetics of ancient deer in the region can serve to steer management of the contemporary population closer toward the optimal path of reconstruction and sustainable conservation of autochthonous deer varieties in natural conditions (Apollonio et al. 2017), as the contemporary population in Belarus experiences growth stabilization after reintroduction and faces the threat of habitat fragmentation under increasing anthropogenic pressure. ...
Here we report the first thorough genetic characterization of the long-understudied red deer population of Belarus in regards to its ancestry according to mtDNA sequence analysis. Employing a 346 base pair segment of the mitochondrial control region (d-loop) from 36 deer specimens of either sex recently harvested across the country, we have discovered 10 haplotypes belonging to 3 of the widely described European red deer lineages, or haplogroups: Iberian (A), Tyrrhenian (B), and Maraloid (E), clarifying the range limits of those lineages in the region. Combining this data with a comparative analysis of genetic diversity and historical records, we conclude that the Belarusian population of red deer has an artificially mixed origin, though it remains unclear how desirable such a state is, in terms of sustainable management, use, and conservation. Inquiries into ancient DNA are required to recognize the lineages closest to the autochthonous deer population of Belarus.
... Gene flow between populations from distinct habitats could subsequently limit the ability to adapt locally and reduce the short-term "fitness" of autochthonous populations. On the other hand, the increasing level of genetic variability caused by translocation could also positively affect population viability through heterosis or reduction of inbreeding depression depending on the genetic distance of the species (taxon) under hybridisation [13][14][15]. In European red deer populations, such migration events were relatively common, predominantly to restore or strengthen local autochthonous populations to avoid local extinction or transport of trophy animals [11,[16][17][18]. ...
Simple Summary
Human activities have left indelible traces in the gene pool of livestock as well as recently domesticated wild animal species which are manifested by changes in their genome structure, often accompanied by the significant loss of biodiversity, especially in the case of small local populations. Despite the benefits of deer farming, intensive artificial selection associated with domestication can lead to several negative effects, including founder effects, inbreeding depression, or rapid decline in effective population size, which are also often present in traditional livestock. This study investigates the effect of human-mediated selection on the diversity of seven farmed red deer populations compared to two wild populations through the quantification of the level of genomic heterozygosity, inbreeding, admixture, and gene flow. These results will help to improve traditional breeding schemes and assist in a more sustainable utilisation of available animal genetic resources.
Abstract
In this study, we analysed the effect of human-mediated selection on the gene pool of wild and farmed red deer populations based on genotyping-by-sequencing data. The farmed red deer sample covered populations spread across seven countries and two continents (France, Germany, Hungary, Latvia, New Zealand, Poland, and Slovakia). The Slovak and Spain wild red deer populations (the latter one in a large game estate) were used as control outgroups. The gene flow intensity, relationship and admixture among populations were tested by the Bayesian approach and discriminant analysis of principal components (DAPC). The highest gene diversity (He = 0.19) and the lowest genomic inbreeding (FHOM = 0.04) found in Slovak wild population confirmed our hypothesis that artificial selection accompanied by bottlenecks has led to the increase in overall genomic homozygosity. The Bayesian approach and DAPC consistently identified three separate genetic groups. As expected, the farmed populations were clustered together, while the Slovak and Spanish populations formed two separate clusters. Identified traces of genetic admixture in the gene pool of farmed populations reflected a strong contemporary migration rate between them. This study suggests that even if the history of deer farming has been shorter than traditional livestock species, it may leave significant traces in the genome structure.
... We detected migrant individuals and inferred hybrids mainly in the northeast population. On the other hand, hybridization between different subspecies and lineages of red deer has been confirmed across Europe (Haanes et al. 2010(Haanes et al. , 2013Fernández-García et al. 2014;Krojerová-Prokešová et al. 2015;Frantz et al. 2017). Consequently, the dispersal and selection balance for red deer in the Pyrenees should be biased to the hybridization process and an increase of the width of the hybrid zone can be expected Hewitt 1985, 1989). ...
Natural events over time, and human interventions, influence the genetic structure of species. The red deer ( Cervus elaphus ) is widely distributed in Europe, with a large‐scale genetic structure largely determined by Pleistocene climatic oscillations. The Iberian Peninsula acted as one of the main glacial refuges for many species; a particular red deer lineage remains on the peninsula and is subjected to special conservation policies. The mountain range of the Pyrenees might be a contact zone where Iberian red deer ( Cervus elaphus hispanicus ) could hybridize with other central European genetic lineages. In the late twentieth century, the natural distribution areas of red deer on both sides of the Pyrenees became closer because of restocking from central Iberia to areas south of the Pyrenees and from French populations to areas north of the Pyrenees. We analyzed the genetic structure of red deer populations in the Pyrenees to investigate the underlying processes of population contact and hybridization. The analysis of microsatellite genotypes showed 2 genetic clusters. One of these clusters associated with Iberian red deer, whereas the other presented European non‐Iberian genetic composition. Migration and hybridization events occurred between both genetic clusters, mostly in the eastern part of the sampling area. The Pyrenees is currently a secondary contact zone caused by anthropogenic translocations, and a risky hybrid belt for red deer genetic conservation.
... Deer have cultural, ecological and an increasing economic importance. Being among the most important game animals for trophies, their populations have been managed, translocated and selectively hunted throughout their history and distribution area [26][27][28][29][30]. Recently a worldwide "deer industry" has been developed, whereby animals are farmed for venison and to some extent for antler products [31][32][33]. ...
Microsatellites are widely applied in population and forensic genetics, wildlife studies and parentage testing in animal breeding, among others, and recently, high-throughput sequencing technologies have greatly facilitated the identification of microsatellite markers. In this study the genomic data of Cervus elaphus (CerEla1.0) was exploited, in order to identify microsatellite loci along the red deer genome and for designing the cognate primers. The bioinformatics pipeline identified 982,433 microsatellite motifs genome-wide, assorted along the chromosomes, from which 45,711 loci mapped to the X- and 1096 to the Y-chromosome. Primers were successfully designed for 170,873 loci, and validated with an independently developed autosomal tetranucleotide STR set. Ten X- and five Y-chromosome-linked microsatellites were selected and tested by two multiplex PCR setups on genomic DNA samples of 123 red deer stags. The average number of alleles per locus was 3.3, and the average gene diversity value of the markers was 0.270. The overall observed and expected heterozygosities were 0.755 and 0.832, respectively. Polymorphic Information Content (PIC) ranged between 0.469 and 0.909 per locus with a mean value of 0.813. Using the X- and Y-chromosome linked markers 19 different Y-chromosome and 72 X-chromosome lines were identified. Both the X- and the Y-haplotypes split to two distinct clades each. The Y-chromosome clades correlated strongly with the geographic origin of the haplotypes of the samples. Segregation and admixture of subpopulations were demonstrated by the use of the combination of nine autosomal and 16 sex chromosomal STRs concerning southwestern and northeastern Hungary. In conclusion, the approach demonstrated here is a very efficient method for developing microsatellite markers for species with available genomic sequence data, as well as for their use in individual identifications and in population genetics studies.
... Initial hybridisation events are likely to ensue between resident red hinds and sika stags migrating into the area. Sika stags are aggressive during the rut (Haanes et al. 2010) and lack of female mate choice in Cervids enables any behavioural mating barriers to be broken. One possible management method proposed is the active control of pioneering sika stags transgressing boundaries to mate with red hinds (Ratcliffe 1987). ...
Globalisation and invasive alien species (IAS) are creating current and damaging effects worldwide. Wildlife management is necessary to preserve the biodiversity of our global flora and fauna, whilst balancing the needs of people with those of wildlife. It is imperative to work to achieve the optimal management strategy on various levels from financial, to ethical and practical. The genetic integrity of Scotland’s native red deer is threatened, following the introduction of sika deer and subsequent hybridisation. This review summarises the problems and potential management strategies associated, as a case study for IAS policy. ?
... The impact of anthropogenic hybridization on the evolution of organisms is difficult to evaluate in natural populations because it entails a long term monitoring of several fitnessrelated traits (Allendorf et al., 2001). Nevertheless, it is well known that hybridization may reduce fitness, disrupt gene-adapted complexes and alter the genetic structure of populations (Muhlfeld et al., 2009;Haanes et al., 2010;Senn et al., 2010;Huisman et al., 2016). However, what are the hybridization effects on the genetic diversity of populations? ...
Anthropogenic hybridization is one of the greatest threats to global biodiversity. It incites human-mediated gene flow between non-native/exotic and native taxa, which can have irreversible effects on native species or locally adapted populations, eventually leading to extinction. The red deer, Cervus elaphus, is a game species that, due to its extraordinary economic value, has been introduced in several regions throughout Europe. However, the consequences of those introductions on native populations, namely on their genetic background, have been poorly addressed. This study is focused on the Iberian Peninsula and aims to: (i) assess the extent of anthropogenic hybridization/introgression of introduced red deer into the native Iberian populations; (ii) evaluate the impact of red deer management regimes on the observed hybridization/introgression patterns; and (iii) assess how hybridization/introgression influence the current genetic diversity of native Iberian populations. A set of 11 microsatellites and a 329 bases pair fragment of the mitochondrial D-loop gene were used to estimate nuclear admixture and mitochondrial introgression in 1,132 individuals sampled across 46 red deer populations throughout Iberia. A Bayesian approach implemented in the STRUCTURE program was employed to investigate the proportion of admixture between native populations and non-native red deer. Results showed that 17% of individuals presented signs of non-native recent ancestors and 10.1% had non-native mitochondrial haplotypes, reaching an overall hybridization/introgression rate of 23%. Non-native or hybrid individuals were found throughout 40 Iberian red deer populations, and the percentages per population varied between 3.3 and 75.0%, independently of the management regime. Mitochondrial introgression was observed across 15 Iberian red deer populations, being more frequent in free-ranging individuals (16.2%) than in fenced populations (9.2%) but was completely absent from public-owned populations. Nuclear genetic diversity correlated positively with the proportion of hybrid individuals in public-owned populations. The genetic footprint of historical and current human-mediated translocations of non-native red deer into the Iberian Peninsula is evidenced in this study, highlighting the need to implement effective measures to avoid such practices both in Portugal and Spain, in order to preserve the endogenous genetic patrimony of the Iberian red deer populations.
Genome‐wide technologies open up new possibilities to clarify questions on genetic structure and phylogeographic history of taxa previously studied with microsatellite loci and mitochondrial sequences. Here, we used 736 individual red deer ( Cervus elaphus ) samples genotyped at 35,701 single nucleotide polymorphism loci (SNPs) to assess the population structure of the species throughout Europe. The results identified 28 populations, with higher degrees of genetic distinction in peripheral compared to mainland populations. Iberian red deer show high genetic differentiation, with lineages in Western and Central Iberia maintaining their distinctiveness, which supports separate refugial ranges within Iberia along with little recent connection between Iberian and the remaining Western European populations. The Norwegian population exhibited the lowest variability and the largest allele frequency differences from mainland European populations, compatible with a history of bottlenecks and drift during post‐glacial colonization from southern refugia. Scottish populations showed high genetic distance from the mainland but high levels of diversity. Hybrid zones were found between Eastern and Western European lineages in Central Europe as well as in the Pyrenees, where red deer from France are in close contact with Iberian red deer. Anthropogenic restocking has promoted the Pyrenean contact zone, admixture events in populations on the Isle of Rum and in the Netherlands, and at least partly the admixture of the two main lineages in central‐eastern Europe. Our analysis enabled detailed resolution of population structure of a large mammal widely distributed throughout Europe and contributes to resolving the evolutionary history, which can also inform conservation and management policies.
Simple Summary
Population genetic structure and individual multilocus heterozygosity are vital for wildlife management. Traditionally, microsatellite markers have been used to estimate population genetic parameters, but single-nucleotide polymorphisms (SNPs) have gained popularity due to their greater measurement precision. This study compared genetic estimates at the population and individual levels using microsatellite and SNP markers in red deer (Cervus elaphus). The findings revealed correlations between parameters estimated with both markers that were associated with the level of genetic diversity and genetic differentiation. However, microsatellites showed lower accuracy in representing the distribution of genetic diversity among individuals.
Abstract
The analysis of population genetic structure and individual multilocus heterozygosity are crucial for wildlife management and conservation. Microsatellite markers have traditionally been used to assess these genetic parameters. However, single-nucleotide polymorphisms (SNPs) are becoming increasingly popular. Our goal here was to determine to what extent SNPs can provide better insights than microsatellites into the overall genetic status and population genetic processes in the species. To this end, we genotyped 210 red deer (Cervus elaphus) in the Spanish wild population with both 11 microsatellites and 31,712 SNPs. We compared parameters related to population genetic structure and individual multilocus heterozygosity obtained with both types of markers. Our results showed correlations between parameters measured using both microsatellites and SNPs, particularly those related to the level of genetic diversity and genetic differentiation. However, we found notably lower precision of microsatellites in measuring the distribution of genetic diversity among individuals. We conclude that microsatellites can be used to monitor the overall genetic status and detect broad patterns in red deer populations. Nevertheless, the greater precision of SNPs in inferring genetic structure and multilocus heterozygosity leads us to encourage scientists and wildlife managers to prioritize their use whenever possible.
Here we report the first thorough genetic characterization of the long understudied red deer population of Belarus in regards to its ancestry according to mtDNA sequence analysis. Employing a 328 base pair segment of the mitochondrial control region (d-loop) from 30 deer specimens of either sex recently harvested across the country, we have discovered 6 haplotypes belonging to 2 of the widely described European red deer lineages, or haplogroups: Iberian (A) and Maraloid (E), clarifying the range limits of both lineages in the region. Combining this data with a comparative analysis of genetic diversity and historical records, we conclude that the Belarusian population of red deer has an artificially mixed origin, though it remains unclear how desirable such a state of the local population is, in terms of sustainable management, use and conservation. Inquiries into ancient DNA are required in order to recognize the lineages closest to the now lost autochthonous population of Belarus.
We describe extensions to the method of Pritchard et al. for inferring population structure from multilocus genotype data. Most importantly, we develop methods that allow for linkage between loci. The new model accounts for the correlations between linked loci that arise in admixed populations (“admixture linkage disequilibium”). This modification has several advantages, allowing (1) detection of admixture events farther back into the past, (2) inference of the population of origin of chromosomal regions, and (3) more accurate estimates of statistical uncertainty when linked loci are used. It is also of potential use for admixture mapping. In addition, we describe a new prior model for the allele frequencies within each population, which allows identification of subtle population subdivisions that were not detectable using the existing method. We present results applying the new methods to study admixture in African-Americans, recombination in Helicobacter pylori, and drift in populations of Drosophila melanogaster. The methods are implemented in a program, structure, version 2.0, which is available at http://pritch.bsd.uchicago.edu.
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.
Greenland ice-core data have revealed large decadal climate variations over the North Atlantic that can be related to a major source of low-frequency variability, the North Atlantic Oscillation. Over the past decade, the Oscillation has remained in one extreme phase during the winters, contributing significantly to the recent wintertime warmth across Europe and to cold conditions in the northwest Atlantic. An evaluation of the atmospheric moisture budget reveals coherent large-scale changes since 1980 that are linked to recent dry conditions over southern Europe and the Mediterranean, whereas northern Europe and parts of Scandinavia have generally experienced wetter than normal conditions.
The first edition of this book has established itself as one of the leading references on generalized additive models (GAMs), and the only book on the topic to be introductory in nature with a wealth of practical examples and software implementation. It is self-contained, providing the necessary background in linear models, linear mixed models, and generalized linear models (GLMs), before presenting a balanced treatment of the theory and applications of GAMs and related models. The author bases his approach on a framework of penalized regression splines, and while firmly focused on the practical aspects of GAMs, discussions include fairly full explanations of the theory underlying the methods. Use of R software helps explain the theory and illustrates the practical application of the methodology. Each chapter contains an extensive set of exercises, with solutions in an appendix or in the book’s R data package gamair, to enable use as a course text or for self-study.