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Conservation Genetics ISSN 1566-0621Volume 14Number 1 Conserv Genet (2013) 14:237-242DOI 10.1007/s10592-012-0431-1

Non-indigenous introgression into theNorwegian red deer population

H. Haanes, J. Rosvold & K. H. Røed

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SHORT COMMUNICATION

Non-indigenous introgression into the Norwegian red deerpopulation

H. Haanes • J. Rosvold • K. H. Røed

Received: 3 September 2012 / Accepted: 23 November 2012 / Published online: 13 December 2012

� Springer Science+Business Media Dordrecht 2012

Abstract Rates of introgression from non-indigenous

into native populations are increasing worldwide, often as a

result of anthropogenic translocation events. In ungulates

translocations have been common, especially among deer.

European red deer consists of two distinct lineages, one

western and one eastern. These probably originate from

different glacial refuges, but it is unknown to what extent

they hold different adaptations. Here we address dispersal

and introgression into the Norwegian mainland population

from an introduced island stock consisting of an admixture

of both European lineages. The last decade this stock has

grown considerably in number and dispersal could be

expected to have increased. We therefore used samples

separated by a 5 year interval from Otterøya, adjacent

mainland areas and a more distant sub-population. Bayes-

ian assignment analysis verified the genetic structure and

identified dispersal between the Otterøya stock and the

adjacent mainland coastal areas. Three individuals (two

newly sampled) with second or third generation non-

indigenous origin were found among the adjacent mainland

samples (5 and 3 %, respectively). Two individuals with

first and second generation mainland-origin were found on

Otterøya (old samples). This suggests some non-indigenous

introgression from Otterøya into the mainland Norwegian

population.

Keywords Non-indigenous dispersal �Bayesian assignment � Cervus elaphus

Introduction

Worldwide, human-mediated translocations increase the

rates of introgression from non-indigenous into native

populations (Allendorf et al. 2001). In addition, range

shifts, especially in temperate areas, also involve

increased population admixture (IPCC 2007). Potential

negative effects include introgression of non-indigenous

gene copies, loss of local adaptations and breaking up of

co-adapted gene complexes (Rhymer and Simberloff

1996; Burke and Arnold 2001). Alternatively, increased

levels of genetic variation after admixture may have

positive consequences for population viability through

heterosis effects or reduced inbreeding depression

(Frankham 1995; Coulson et al. 1998), depending on the

genetic divergence (Allendorf et al. 2001). However, to

be able to determine the outcome of introgression and

admixture, long-term monitoring is suggested (Fischer

and Lindenmayer 2000).

Non-indigenous introductions have been common in

game management (Fischer and Lindenmayer 2000),

especially in the red deer (Cervus elaphus, Hartl et al.

1995, 2003). Many European red deer populations are

morphologically (Lønnberg 1906; Whitehead 1993) and

genetically differentiated (Gyllensten et al. 1983; Kuehn

et al. 2003). However, a main dichotomy is found between

H. Haanes (&)

Department of Biology, Centre for Conservation Biology,

Norwegian University of Science and Technology, 7491

Trondheim, Norway

e-mail: hhaanaes@gmail.com

J. Rosvold

Section of Natural History, NTNU Museum of Natural History

and Archaeology, Norwegian University of Science and

Technology, 7491 Trondheim, Norway

K. H. Røed

Department of Basic Sciences and Aquatic Medicine, Norwegian

School of Veterinary Science, P.O. Box 8146 Dep, 0033 Oslo,

Norway

123

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DOI 10.1007/s10592-012-0431-1

Author's personal copy

East and West Europe, which is characterised by distinct

mtDNA lineages originating from different glacial refuges

(Ludt et al. 2004; Skog et al. 2009; Niedzialkowska et al.

2011; Zachos and Hartl 2011). Assessments of the multi-

tude of translocations have been difficult (Hartl et al. 2003;

Niedzialkowska et al. 2011; Zachos and Hartl 2011) but

introductions across this main dichotomy do not seem to

have had any large genetic impact (Skog et al. 2009),

except in the British Isles where several stocks are admixed

with the North-African lineage (Nussey et al. 2006; Carden

et al. 2012).

Moreover, one century ago 17 red deer of German-

Hungarian origin were introduced into the much reduced

stock on the Norwegian island Otterøya (Die-Woche 1902;

Collett 1909). These introduced individuals were thus a

cross between both European lineages. Genetic analyses

show that the present Otterøya stock consists of an

admixture of Norwegian and Hungarian red deer, but their

body size and the population growth do not indicate any

negative effects of introgression (Haanes et al. 2010a).

A very low dispersal rate has been estimated (Haanes et al.

2010a) but it could be expected to have increased recently

considering the increasing population density. Generally,

the number of harvested red deer per km2 correlates well

with other direct measures of density over time (Mysterud

et al. 2007) and from 2002 the number of culled red deer

increased from 211 to 331 in 2007 on this 143 km2 large

island. To investigate for any recent dispersal we per-

formed additional sampling on both Otterøya and in the

adjacent mainland coastal areas.

Methods and materials

A total of 307 samples were used in this study; 176 from

2002 and our previous study of Otterøya (Haanes et al.

2010a), 83 from two more distant mainland locations in the

southeast (Haanes et al. 2010b), while the rest were new

samples from Otterøya (n = 16) and adjacent mainland

areas (n = 32, Table 1; Fig 1). All these were genotyped in

14 polymorphic microsatellite loci that show Mendelian

heredity in Norwegian red deer (Haanes et al. 2005; labo-

ratory protocol cf. Haanes et al. 2010a, b). In addition, 33

samples (from Haanes et al. 2010a) plus 42 of the new

samples were sequenced in a 463 base region of the mito-

chondrial D-loop adjacent to the tRNApro gene using the

primers 50-AATAGCCCCACTATCAGCACCC (L15394)

and 50-TATGGCCCTGAAGTAAGAACCAG (H15947)

(cf. Flagstad and Røed 2003; Haanes et al. 2010a).

To verify the genetic structure (Haanes et al. 2010a, b) and

to address dispersal from Otterøya, STRUCTURE 3.1

(Pritchard et al. 2000) was first run with uniform priors, an

admixture model (a = 1, amax = 10), correlated allele

frequencies (Falush et al. 2003), 100,000 burnins cycles

and 500,000 MCMC iterations in 10 runs for each K value

(K [ [1, 9]). Genetic structure was interpreted from DK,

which is negatively related to variance among runs of

increasing K values (Evanno et al. 2005). This genetic struc-

ture was then applied, using information on where individuals

were sampled in STRUCTURE (POPINFO = 1) to identify

dispersers of first, second or third generation origin (GENS-

BACK [ [0, 2]).

Table 1 Sampled localities, the according geographic population

(2010b) i.e. adjacent (AM) or distant mainland (DM), the Munici-

pality number (Mun nr), approximate distance in kilometres to

Otterøya (Dist km), year of sampling, number of samples (n) and

originating study (Ref.: 1 = Haanes et al. 2010a, 2 = Haanes et al.

2010b)

Population Mun nr Locality name Dist km Years n Reference

Otterøya 1747 Otterøya – 2007 16 New

Otterøya 1747 Otterøya – 2002 40 1

AM 1744 Overhalla 20 2007 3 New

AM 1725 Namdalseid 30 2007 8 New

AM 1742 Grong 40 2007 2 New

AM 1721 Verdal 60 2007 13 New

AM 1721 Verdal 60 2002 15 1

AM 1630 Afjord 80 2002 16 1

AM 1617 Hitra (island) 160 2002 37 1

AM 1613 Snillfjord 150 2002 9 1

AM 1635–1646 Skaun-Rennebu 150–190 2002 27 1

AM 1571 Halsa 220 2002 6 New

AM 1563 Sunndal 250 2002 32 1

AM 0432 Rendalen 300 2002 15 2

DM 0819 Nome 600 2002 68 2

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The sequence data was used to verify the private

mtDNA haplotype on Otterøya (Haanes et al. 2010a) and to

investigate for introgression into the mainland Norwegian

population.

Results

The mtDNA haplotype previously described as non-

indigenous and private to Otterøya (Haanes et al. 2010a)

was not found among any of the samples from adjacent

mainland areas. Furthermore, as described before (Haanes

et al. 2010a, b) the STRUCTURE analysis showed a main

genetic dichotomy between Otterøya and the Norwegian

mainland (Figs. 2, 3a) with a lower hierarchical structure

within the mainland population (i.e. between adjacent

coastal areas and the distant reference population). The

subsequent STRUCTURE analysis with information on

sampling locations was therefore performed for K = 3. It

showed that three individuals sampled in adjacent main-

land areas originated from Otterøya, one of second gen-

eration origin (adult male) and two as third generation

descendants (males, one subadult and one adult). Two of

these, both from Namdalseid situated approximately 30

kilometres (km) from Otterøya, were new samples. The

third was from Afjord, situated 80 km from Otterøya. In

addition, on Otterøya one first generation disperser from

mainland Norway and one second generation descendant

were identified (samples from Haanes et al. 2010a). Pos-

terior probabilities of assignment without population

information and with population information (K = 3) for

these individuals are given in Table 2 and Fig. 3.

Discussion

The last century the general trend in the Norwegian red

deer population has been major growth and expansion

(Forchhammer et al. 1998; Mysterud et al. 2007). The

genetically distinct stock on Otterøya has also grown

considerably in number since 2002 when we detected only

one sample in the adjacent mainland areas that assigned to

Otterøya (Haanes et al. 2010a). It is therefore not surprising

that we now detected signs of increased emigration from

Otterøya (Table 2, Fig. 3). One adult and one sub-adult

male, second and third generation descendants from

Otterøya respectively, were sampled at closely situated

mainland localities within the same municipality. They

were too genetically distinct to be father and son (mismatch

in four loci) but could be descendants of the same disperser

from Otterøya. By comparison, the previously detected

Otterøya descendant (Haanes et al. 2010a), which was an

adult male (third generation origin), was so distant in time

(5 years) and space (80 km) that it probably descended

Fig. 1 Map of a Europe with Norway (No), Germany (Ge) and Hungary (Hu), and b the red deer sampling localities with the corresponding

Municipality numbers

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from another dispersal event from Otterøya. If only adja-

cent areas less than 100 km away are considered, the

number of individuals with a partial origin from Otterøya

(n = 3, Table 2) constitutes 5 % of the samples in these

areas (n = 57). If the two samples from 2007 are descen-

dants from one dispersing individual the according per-

centage would be 3.5, which is also a relatively high figure.

In addition, the two samples from Otterøya with first and

second generation mainland-origin provide support that red

deer disperse across the Otterøya sounds and that intro-

gression can be expected from this non-indigenous-

admixed stock.

Compared to other European red deer populations, the

mainland Norwegian population is genetically distinct,

possibly as a consequence of postglacial founder effects,

subsequent isolation and genetic drift during a major

Fig. 2 Mean posterior probabilities (Ln (P(D)) averaged across ten runs (for each K value) for the red deer data (n = 307) and corresponding

DK values given different numbers of subpopulations (K [ [1, 9])

Otterøya Adjacent Mainland Distant mainland

Otterøya Adjacent Mainland Distant mainland

(b)

(a)Fig. 3 Individual posterior

probabilities (y-axis) of

Bayesian assignment

(STRUCTURE) to two or three

clusters (different colours)

among red deer from Otterøya,

adjacent and more distant

mainland Norway. The analysis

was first done without any

information on where

individuals were sampled

(a localities separated by

vertical lines) and then with

such information (b for K = 3).

(Color figure online)

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population decline from the 16th to the 19th century AD

(Haanes et al. 2011a, 2010b; Rosvold et al. 2012). The

Otterøya stock on the other hand, which is genetically

distinct from the Norwegian population, represents a mix

from both the eastern and western European lineages of red

deer (Haanes et al. 2010a). Compared with Norway, the

source areas for the introduction on Otterøya (Germany

and Hungary) are situated in quite different climates and

habitats (Mysterud et al. 2002; Matrai et al. 2004). Con-

sidering the time since the postglacial colonisation by red

deer (more than 8,000 years ago), one concern is whether

the Norwegian population have developed indigenous local

adaptations which may be threatened by introgression. This

would advocate for measures to avoid dispersal from

Otterøya. However, the lack of any observed negative

effects from introgression within the Otterøya stock more

probably reflects a high level of phenotypic plasticity in

European red deer and genetic differentiation through

genetic drift rather than selection. Such plasticity is also

supported by the thriving of several British Isles stocks

which are admixed with the North African/Sardinian line-

age (Nussey et al. 2006; Carden et al. 2012). Moreover, and

of greater concern, even hybridisation with and introgres-

sion from sika deer (Cervus nippon) is reported from the

British Isles (Goodman et al. 1999; McDevitt et al. 2009a).

Hybridisation is common within the red deer species

complex (Hartl et al. 1995, 2003) but negative effects are

known between as genetically and morphologically dif-

ferent taxa as the wapiti (Cervus canadensis) and the red

deer (Asher et al. 2005). By comparison, some of the

thriving Scandinavian moose (Alces alces) stocks (e.g.

Grøtan et al. 2009) consist of an admixture of long time

separated lineages (Haanes et al. 2011b). Moreover, in

caribou (Rangifer tarandus) admixture of lineages with

different adaptations has even involved positive effects

through increased plasticity in migratory behaviour

(McDevitt et al. 2009b). Further studies of convergence

zones with admixture between lineages holding divergent

adaptations would thus be interesting.

Acknowledgments Thanks to all the hunters and game managers in

the municipalities of Northern Trønderlag who has put such an

interest into this project, especially Aksel Hakonsen in the adminis-

tration of the Municipality Namsos.

References

Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The

problems with hybrids: setting conservation guidelines. Tree 16:

613–622

Asher GW, Archer JA, Scott IC et al (2005) Reproductive perfor-

mance of pubertal red deer (Cervus elaphus) hinds: effects of

genetic introgression of wapiti subspecies on pregnancy rates at

18 months of age. Anim Reprod Sci 90:287–306

Burke JM, Arnold ML (2001) Genetics and the fitness of hybrids.

Annu Rev Genet 35:31–52

Carden RF, McDevitt AD, Zachos FE et al (2012) Phylogeographic,

ancient DNA, fossil and morphometric analyses reveal ancient

and modern introductions of a large mammal: the complex case

of red deer (Cervus elaphus) in Ireland. Quatern Sci Rev

42:74–84

Collett R (1909) Hjorten i Norge (Cervus elaphus atlanticus), nogle

biologiske meddelelser (in Norwegian). Bergens Mus Aarbok

6:9–31

Coulson TN, Pemberton JM, Albon SD et al (1998) Microsatellites

reveal heterosis in red deer. Proc Biol Sci 265:489–495

Die-Woche (1902) Rochwildtransport nach Norwegen (in German).

Reitz publishing. Berlin, pp 1111–1113

Evanno G, Regnaut S, Goudet J (2005) Detecting the number of

clusters of individuals using the software STRUCTURE: a

simulation study. Mol Ecol 14:2611–2620

Falush D, Stephens M, Pritchard JK (2003) Inference of population

structure using multilocus genotype data: linked loci and

correlated allele frequencies. Genetics 164:1567–1587

Fischer J, Lindenmayer DB (2000) An assessment of the published

results of animal relocations. Biol Conserv 96:1–11

Flagstad Ø, Røed KH (2003) Refugial origins of reindeer (Rangifertarandus L.) inferred from mitochondrial DNA sequences.

Evolution 57:658–670

Table 2 Sample information and STRUCTURE results for each identified disperser between Otterøya (Ott) and the adjacent mainland popu-

lation (AM)

Sample info Without info With info

ID Loc Pop qOtt qAM ppS Alt g0 g1 g2 Sign Reference

A7 Afjord AM 0.31 0.69 0 Ott 0 0.07 0.93 *** 1

N5 Namdalseid AM 0.19 0.79 0.09 Ott 0 0.01 0.9 *** 0

N5 Namdalseid AM 0.59 0.33 0 Ott 0.01 0.78 0.22 *** 0

O8 Otterøya Ott 0.01 0.94 0 AM 1 0 0 *** 1

O5 Otterøya Ott 0.42 0.57 0.01 AM 0 0.93 0.07 *** 1

For each sample (ID), the location (Loc) and geographic population (Pop) where it was sampled. STRUCTURE results without population

information; individual assignment coefficients for Otterøya (qOtt) and the adjacent mainland population (qAM). STRUCTURE results with

population information; posterior probabilities for correct assignment to the given/sampled population (ppS) and probabilities for ancestry

originating in an alternative subpopulation (Alt) in zero (gensback0; g0), one (g1) and two (g2) generations back in time (with K = 3).

Originating study given (Ref.: 0 = new sample, 1 = Haanes et al. 2010a)

Conserv Genet (2013) 14:237–242 241

123

Author's personal copy

Forchhammer MC, Stenseth NC, Post E, Langvatn R (1998)

Population dynamics of Norwegian red deer: density-depen-

dence and climatic variation. Proc Biol Sci 265:341–350

Frankham R (1995) Conservation genetics. Annu Rev Genet

29:305–327

Goodman SJ, Barton NH, Swanson G, Abernethy K, Pemberton JM

(1999) Introgression through rare hybridisation: a genetic study

of a hybrid zone between red and sika deer (Genus Cervus) in

Argyll, Scotland. Genetics 152:355–371

Grøtan V, Sæther B-E, Lillegard M, Solberg EJ, Engen S (2009)

Geographical variation in the influence of density dependence

and climate on the recruitment of Norwegian moose. Oecologia

161:685–695

Gyllensten U, Ryman N, Reuterwall C, Dratch P (1983) Genetic

differentiation in four European subspecies of red deer (Cervuselaphus L.). Heredity 51:561–580

Haanes H, Rosef O, Veiberg V, Røed KH (2005) Microsatellites with

variation and heredity applicable to parentage and population

studies of Norwegian red deer (Cervus elaphus atlanticus). Anim

Genet 36:454–455

Haanes H, Røed KH, Mysterud A, Langvatn R, Rosef O (2010a)

Consequences for genetic diversity and population performance

of introducing continental red deer into the northern distribution

range. Conserv Genet 11:163–1665

Haanes H, Røed KH, Flagstad Ø, Rosef O (2010b) Genetic structure

in an expanding cervid population after population reduction.

Conserv Genet 11:11–20

Haanes H, Røed KH, Perez-Espona S, Rosef O (2011a) Low genetic

variation support bottlenecks in Scandinavian red deer. Eur J

Wildl Res 57:1137–1150

Haanes H, Røed KH, Solberg EJ, Herfindal I, Sæther BE (2011b) Genetic

discontinuities in a continuously distributed and highly mobile

ungulate, the Norwegian moose. Conserv Genet 12:1131–1143

Hartl GB, Nadlinger K, Apollonio M et al (1995) Extensive

mitochondrial-DNA differentiation among European red deer

(Cervus-elaphus) populations: implications for conservation and

management. Z Saugetierkd-Int J Mamm Biol 60:41–52

Hartl GB, Zachos F, Nadlinger K (2003) Genetic diversity in

European red deer (Cervus elaphus L.): anthropogenic influences

on natural populations. CR Biol 326:37–42

IPCC (2007) Intergovernmental Panel on Climate Change Fourth

Assessment Report. http://www.ipcc.ch. Last accessed May

2009

Kuehn R, Schroeder W, Pirchner F, Rottmann O (2003) Genetic

diversity, gene flow and drift in Bavarian red deer populations

(Cervus elaphus). Conserv Genet 4:157–166

Lønnberg E (1906) On the geographic races of red deer in Scandinavia.

Ark Zool 3:1–19

Ludt CJ, Schroeder W, Rottmanm O, Kuehn R (2004) Mitochondrial

DNA phylogeography of red deer (Cervus elaphus). Mol

Phylogenet Evol 31:1064–1083

Matrai K, Szemethy L, Toth P, Katona K, Szekely J (2004) Resource

use by red deer in lowland nonnative forests, Hungary. J Wildl

Manag 68:879–888

McDevitt AD, Edwards CJ, O’Toole P et al (2009a) Genetic structure

of, and hybridisation between, red (Cervus elaphus) and sika

(Cervus nippon) deer in Ireland. Mamm Biol 74:263–273

McDevitt AD, Mariani S, Hebblewhite M et al (2009b) Survival in

the Rockies of an endangered hybrid swarm from diverged

caribou (Rangifer tarandus) lineages. Mol Ecol 18:665–679

Mysterud A, Langvatn R, Yoccoz NG, Stenseth NC (2002) Large-

scale habitat variability, delayed density effects and red deer

populations in Norway. J Anim Ecol 71:569–580

Mysterud A, Meisingset EL, Veiberg V et al (2007) Monitoring

population size of red deer: an evaluation of two types of census

data from Norway. Wildl Biol 13:285–298

Niedzialkowska M, Jedrezejewska B, Honnen A-C et al (2011)

Molecular biogeography of red deer Cervus elaphus from eastern

Europe: insights from mitochondrial DNA sequences. Acta

Theor 56:1–12

Nussey DH, Pemberton J, Donald A, Kruuk LEB (2006) Genetic

consequences of human management in an introduced island

population of red deer (Cervus elaphus). Heridity 97:56–65

Pritchard JK, Stephens M, Donnelly P (2000) Inference of population

structure using multilocus genotype data. Genetics 155:945–959

Rhymer JM, Simberloff D (1996) Extinction by hybridization and

introgression. Annu Rev Ecol Syst 27:83–109

Rosvold J, Røed KH, Hufthammer AK, Andersen R, Stenøien HK

(2012) Reconstructing the history of a fragmented and heavily

exploited red deer population using ancient and contemporary

DNA. BMC Evol Biol 12:191. doi:10.1186/1471-2148-12-191

Skog A, Zachos FE, Rueness EK et al (2009) Phylogeography of red

deer (Cervus elaphus) in Europe. J Biogeogr 36:66–77

Whitehead GK (1993) The Whitehead encyclopedia of deer. Swan

Hill Press, Shrewsbury

Zachos FE, Hartl GB (2011) Phylogeography, population genetics

and conservation of the European red deer Cervus elaphus.

Mamm Rev 41:138–150

242 Conserv Genet (2013) 14:237–242

123

Author's personal copy