Download conservation of genetic biodiversity in changing landscape

ISBN 952-10-2817-3 (pdf)
ISSN 1235-4449
4.1. Conservation of genetic biodiversity in a changing landscape,
with special reference to capercaillie (Tetrao urogallus) in
Finland
Hannaleena Mäki-Petäys, Markku Orell
University of Oulu, Department of Biology, P.O.Box 3000, FI-90014 Oulu, Finland.
[email protected] ()
CONSERVATION GENETICS
Conservation genetics is the theory and practice of genetics in the conservation of
species as dynamic entities, which are capable of evolving to cope with environmental
changes to minimise the risk of extinction (Frankham et al. 2002). Conservation
genetics is a relatively young discipline and it is developing rapidly due to the new
molecular techniques available (Smith & Wayne 1996). Although ecological,
economical, and political factors may be of primary concern for avoiding the extinction
of most endangered species, long-term persistence, genetics and related considerations
have also become the focus of conservation efforts. This has only recently become
possible because new molecular techniques have facilitated genetic studies of
endangered species (Hedrick 2001).
As a discipline, conservation genetics also includes the resolution of taxonomic
uncertainties and the delineation of management units. It may additionally involve the
genetic management of small populations to ensure that as much genetic diversity is
maintained as possible, as well as the forensic use of molecular genetic analyses to
increase our understanding of a species’ biology. Conservation genetics focuses on the
processes within small, fragmented populations, and on practical approaches designed
to minimise any harmful trends. Small population size is typically the main reason for
the loss of genetic diversity, whereas restricted gene flow can prevent the exchange of
alleles between fragmented populations (Frankham et al. 2002).
Genetic diversity
Genetic diversity encompasses the whole variety of alleles and genotypes present in a
population or species. It is typically described by measuring polymorphism, average
heterozygosity and allelic diversity. Genetic diversity can be measured for many
different traits, including quantitative characters, deleterious alleles, proteins, nuclear
DNA loci, mitochondrial DNA, chloroplast DNA and chromosomes (Hedrick 1999).
The maintenance of genetic diversity is a primary objective in the management of
wild and captive populations of threatened species. The loss of genetic diversity, i.e.
genetic erosion, is often associated with reduced reproductive fitness (Crnokrak and
Roff 1999). Further, genetic diversity is the raw material for adaptive evolutionary
Anneli Jalkanen & Pekka Nygren (eds.) 2005. Sustainable use of renewable natural
resources — from principles to practices. University of Helsinki Department of Forest
Ecology Publications 34. http://www.helsinki.fi/mmtdk/mmeko/sunare
Mäkipetäys & Orell
Fig. 1. Male capercaillie on tree top is
an impressive sight that has become
rare in Finnish forests. Maintenance of
sufficient genetic variation in the
population is essential to ensure the
viability of the species in the future.
Photo: Pekka Nygren
change, and thus a prerequisite for the evolution of populations to cope with
environmental changes (Lande 1995).
The risk of genetic erosion is highest in small, isolated populations because of
increased random genetic drift, elevated inbreeding and reduced interpopulation gene
exchange (Gilpin 1991, Raijmann et al. 1994, Hedrick 2001). This can particularly be
the case where a single continuous population has been fragmented into smaller subpopulations.
Habitat fragmentation
Habitat loss and fragmentation due to human land use are considered to be the most
important deterministic threats to many species. Commercial logging has resulted in
large-scale changes in forest structure, which in turn affect forest species at the
population level. The viability of a species may additionally be jeopardised by
demographic, genetic or environmental stochasticity – factors which are amplified in
small populations (Holsinger 2000, Keller and Weller 2002). From a genetic point of
view, habitat fragmentation has several impacts on population genetic structure and
diversity. Restricted gene flow together with small population size has been shown to
lead to the genetic differentiation of populations and to loss of heterozygosity and allelic
richness, causing inbreeding depression. Inbreeding and loss of genetic diversity can
reduce reproduction in the short term and diminish the capacity of populations to
2
Conservation of genetic biodiversity in a changing landscape
respond to environmental change in the long term, leading to an increased risk of
extinction (Keller and Weller 2002).
The effects of fragmentation depend critically upon the level of gene flow among
the fragments, which is in turn dependent on factors related to environmental and
population patterns, such as the number and spatial structure of populations. The effects
of fragmentation are also time-dependent, as well as being influenced by the dispersal
ability of the species and associated migration rates between the remaining habitat
fragments (e.g. Frankham et al. 2002).
In this paper we concentrate on the effects of fragmentation on the genetic
population structure of the capercaillie (Tetrao urogallus) in Finland, including genetic
diversity and gene flow. It is assumed that the capercaillie suffers from forest
fragmentation, and it is suggested to be an ‘umbrella species’ of old-growth forest
(Suter et al. 2002). More information on the capercaillie is thus urgently needed to
facilitate conservation.
DECLINED POPULATIONS OF THE CAPERCAILLIE
The capercaillie is protected by law in several European countries and it is included in
the respective national Red Books (Hilton-Taylor 2000). In Finland, the relative density
of the species has declined rapidly since the 1940s due to various human activities
(Lindén and Rajala 1981). The current population size is on the average 300,000
breeding individuals (Helle et al. 1999b). This is about one third of the species’
population in the 1960s. In addition to this overall decline in population size, the
species’ sex-ratios have also changed over recent decades (Helle et al. 1999a).
Previously the Finnish population was female-biased (60% females, 40% males), but in
Southern Finland females currently only make up around 50% of the population,
although they still constitute around 60-65% of total populations in the north (Helle et
al. 1999a).
Several reasons have been put forward to explain the population decline of the
capercaillie. Increased predation pressure associated with changes in the structure of
forest landscape has been proposed as a factor (Storaas et al. 2001). Nowadays game
hunting extends over wider areas as the intensifying network of forest roads has reduced
the numbers of remote natural reserves for the capercaillie. Although hunting may have
led to decline on a local scale, the most seriously affected populations are in Southern
Finland where hunting pressure is the lowest. This would indicate that the major threats
to the capercaillie are forest fragmentation and changes in the age composition of
forests due to human land use (Helle 1999a, b).
Capercaillie mating occurs at leks that consist of groups of males visited by
females. Distribution of mating is highly distorted so that only a few males manage to
reproduce (Höglund and Alatalo 1995). This type of breeding behaviour means that the
effective population size of the capercaillie is considerably smaller than the actual
population size, because of the high number of non-breeding males. This makes the
species even more vulnerable to environmental disturbances.
The lekking behaviour of the capercaillie affects dispersal behaviour, which in
turn, has an effect on the gene flow between breeding areas, i.e. leks. Males tend to be
devoted to their leks, while females can visit several leks during their lifetime (Storch
1997), even though most females tend to return to the same lek and mate with the same
male year after year (Hjorth 1970, Wegge and Larsen 1987). It has been suggested that
3
Mäkipetäys & Orell
the capercaillie has sex-biased natal dispersal with males being the philopatric sex
(Koivisto 1963, Lindén 2002). Earlier studies are based on ecological data and did not
include the use of molecular markers to address the question of differential dispersal
between the sexes. There are many difficulties in determining the relative contributions
of males and females to gene flow using ecological methods, since the sample sizes
needed are relatively large. Furthermore, dispersal rates are often unreliable, as
dispersers do not necessarily breed (Frankham et al. 2002). New molecular methods
have great potential for examining sex-specific gene flow. Many other subjects can
more easily be investigated by using molecular, rather than ecological methods,
including estimates on how closely individual birds are inter-related.
An other important issue, in addition to dispersal behaviour, is the uncertainty
regarding the existence of different sub-species of the capercailllie in Finland. Previous
work has indicated that three different subspecies – Tetrao urogallus urogallus, T. u.
major, and T. u. uralensis – occur in Finland (Johansen 1957, Lindén and Teeri 1985).
This conclusion has mainly been based on observed morphological differences
(Helminen 1963, Lindén and Väisänen 1986) and behavioural differences (Jaakola
1999) between sub-species. However, there is no information that indicates whether
these subspecies should be treated as separate conservation units or a single unit in the
planning of management programmes.
When planning land use and forestry at the landscape level, it is important that the
level of gene flow between leks is known. Protected forests in eastern Finland, such as
those adjoining the “Green Belt” forests of Russian Karelia, may ultimately serve as
important source areas for maintaining the genetic diversity of capercaillie subpopulations in western Finland, and even more widely for the long-term persistence of
the species in the whole Fennoscandia.
THE GENETIC STRUCTURE OF THE CAPERCAILLIE IN FINLAND
We began the studies on the population genetics of the capercaillie in Finland in spring
2001 with the collection of information on the genetic diversity of the capercaillie
population. At first, we focused on the spatial structure of the population, and the
relatedness of individuals within leks. The data have a good coverage over the country
(Fig. 2), which makes it possible to analyse dispersal patterns of the capercaillie at
different spatial scales more reliably than previously. Information on genetic diversity
and gene flow can be linked with the landscape data in GIS (Geographical Information
Systems) to estimate the effects of forest fragmentation on these patterns. Analysis at
the landscape level is particularly important in Finnish forests near Russian Karelia,
becuase the forests on Russian side of the border have been considered as a potential
source of immigrant birds that could maintain the genetic diversity of the Finnish
capercaillie population in the future.
We have also designed our study to resolve taxonomic uncertainties and to define
conservation and management units for declining populations. The ultimate goal of the
study is to determine suitable management options for the species and to provide
information for helping to ensure that land use and forestry are planned in an
ecologically sustainable way.
4
Conservation of genetic biodiversity in a changing landscape
Fig. 2. Locations of sampled leks
(indicated
by
Š)
in
Finland.
Subpopulations
(max.
distance
between samples 50 km) are circulated
by black line, whereas different colours
(blue, green, yellow and red) indicate
four groups obtained by genetic
analyses. Zonation is based on the
subspecies distribution.
Genetic analyses
Samples for genetic analyses were collected from the lekking sites of the capercaillie.
Samples were fresh faeces collected under the trees, in which males have stayed over
several nights. The minimum distance between the samples was 60 meters, which
should be adequate to separate the sleeping sites of different males in territories.
Females lack territories, thus only one female sample per lek-site was collected, with
the exception that faeces were less than one day old. The sex of the sample in the field
was estimated from the size of the faeces. Later the sex of all samples was confirmed by
DNA-based sex identification (Griffiths et al. 1998).
The study involved the examination of the degree of genetic variability in the
Finnish capercaillie population using co-dominant nuclear microsatellites and single
stranded conformation polymorphism (SSCP) from mitochondrial DNA (mtDNA), as
molecular markers. The mtDNA differs from nuclear DNA as it is inherited only from
the mother, whereas nuclear DNA is inherited from both parents. Using these two
different markers allowed us to examine the factors such as sex-specific gene flow.
Microsatellite loci are segments of DNA with very short sequences repeated in
tandem at one or more places in the genome (Queller et al. 1993). The large number of
microsatellite loci, and their high variability, makes them potentially important tools for
examining the genetic structure of the populations. We used nine species-specific
microsatellite loci developed by Segelbacher et al. (2000) for revealing the nuclear
variation. In total, we genotyped about 500 individuals collected from 200 leks (Fig. 2).
All loci used were independent and highly variable.
5
Mäkipetäys & Orell
Table1. Number of individuals (Nind) in subpopulations, number of microsatellite alleles
(Nall) and gene diversity (HE) calculated over loci by software FSTAT.
Nind
Nall
HE
Sodankylä
15
Meltaus
24
Rovaniemi
24
Palokas
18
Simo
22
Litokaira
32
Posio
14
P-Kuusamo
47
E-Kuusamo
48
Syöte
54
Pudasjärvi
20
Pohjanmaa
9
K-Suomi
27
E-Suomi
31
56
74
60
65
56
64
61
74
71
87
67
21
71
69
0,76
0,77
0,76
0,82
0,72
0,70
0,73
0,75
0,73
0,75
0,76
0,88
0,76
0,75
Table 2. Number of individuals (Nind) and alleles (Nall.), expected (HE) and observed
(HO) heterotsygosity, and FST values with standard errors. All values are estimated over
subpopulations and loci by using software FSTAT.
Nind.
Nall.
HE
HO
FST
Microsatellites
Females
Males
Total
105
280
385
107
128
137
0.74
0.75
0.76
0.54
0.56
0.55
0.035 ± 0.012
0.025 ± 0.003
0.025 ± 0.004
SSCP
187
15
0.030
SSCP is based on 3-dimensional conformation, as determined by a single-stranded
nucleotide sequence, and rate of its migration in polyaclylamide gel (Hayashi 1991).
Even a single nucleotide difference may change the conformation of the single strands
enough to change their mobility in the gel. Thus SSCP is a useful method for detecting
single nucleotide polymorphism without having to sequence the homologous DNA
fragments isolated from a large number of individuals. To examine the genetic variation
in mtDNA, we genotyped ca. 200 samples from 120 leks by using SSCP. The segment
used in this study was originally designed for the grey partridge (Perdix perdix) by
Liukkonen-Anttila et al. (2002). All genotypes were verified by sequencing 40 samples
for both directions.
6
Conservation of genetic biodiversity in a changing landscape
Results
Genetic population structure and gene flow
We have already obtained preliminary results on the genetic diversity and population
structure of the capercaillie in Finland. Relatively high genetic diversity, measured as
the number of alleles and gene diversity, was found in all studied subpopulations (Table
1). There was no genetically differentiated subpopulations when microsatellite data was
analysed by using Bayesian clustering (BAPS; see Corander et al. 2003, 2004).
Moreover, the genetic differentiation of subpopulations estimated by FST was relatively
low (Table 2). The FST indicates the probability that two alleles drawn randomly from a
population fragment are identical by descent. Additionally, studies using microsatellites
have as yet shown no clear signs at the genetic level of the existence of subspecies of
the capercaillie. However, more structure was found for mtDNA (Table 2) by Bayesian
analyses, but it did not match the suggested distribution of subspecies (Fig. 2). Most
genetically differentiated and geographically constant group consisted of leks located in
north-eastern Finland (Syöte, Pohjois-Kuusamo and Etelä-Kuusamo). This supports the
results of Liukkonen-Anttila et al. (2004), with no mtDNA sequence structuring related
to suggested capercaillie subspecies’ ranges in Finland. However, some rare haplotypes
and high genetic diversity in north-eastern Finland was also found in this study.
According to our preliminary results, the genetic differentiation at the lek level
was relatively strong (FST = 0.094 ± 0.01), indicating partly restricted gene flow
between leks. Also the level of inbreeding coefficients, or the probability that two
alleles in an individual are identical by descent (FIS), were quite high
(FIS = 0.182 ± 0.031). Similar and even higher inbreeding values in lek level (0.19–0.31)
has been recorded for other grouse species (lesser prairie chicken Tympanuchus
pallidicinctus; Bouzat and Johnson 2004). The partly restricted gene flow together with
high level of inbreeding could be a consequence of kin selection in leks, as described for
the black grouse (Tetrao tetrix) (Höglund et al. 1999). Kin selection theory predicts that
by joining a lek where a relative is likely to reproduce, the attractiveness of the lek is
raised and males unsuccessful in obtaining copulations may gain via inclusive fitness.
Sex-Biased dispersal
The preliminary result based on comparison of genetic population structure between
sexes and between differently inherited markers indicate that males have a stronger
impact upon gene flow than earlier assumed. The result of roughly equal gene flow of
sexes do not agree with the previously held assumption that females are the dispersing
sex, whereas males are highly devoted to their leks. This is particularly interesting
because earlier studies have mainly concentrated on the average dispersal distances of
the sexes, but not on the maximum distances. Yet long dispersal distances can have an
important role in the level of gene flow, and in mixing the different gene pools of
populations. Further, earlier dispersal estimates are based on ecological studies, which
poorly measure the effective dispersal affected by factors like polygamy, i.e the
distortion of mating, of the species. Although the female would be the more often
dispersing sex, the rare long dispersing males can have strong influence on the genetic
structure of the leks. The dispersal of males with high fitness further magnifies strength
of the male gene flow as only one or few males in a lek can reproduce. It is also possible
that the dispersing male is not superior itself, but its offspring will have heterosis
advantage in a new lek site. In the black grouse, males that never obtained a lek territory
7
Mäkipetäys & Orell
had lower level of heterozygosity than males that were observed in a territory, possibly
showing the effects of heterosis (Höglund et al. 2002). The unexpected results also
imply that more information will be needed on the structure of leks and the lekking
behaviour of the capercaillie for designing conservation practices that ensure genetic
diversity and facilitate efficient dispersal and gene flow between leks in the future.
Implications for conservation and management
The preliminary results of our study support the importance of the connectivity of
forests in the management of capercaillie populations. In forest management, it is
important to maintain a sufficient network of both current well-functioning and
potential yet unoccupied lek sites for sustaining efficient natal dispersal of the
capercaillie. Moreover, the importance of male dispersal may earlier have been
underestimated. This should be taken into account when planning hunting and game
management. When considering the conservation and/or management unit of the
capercaillie, our results support the importance of populations in NE Finland. More
detailed analyses in landscape level are needed to obtain information for local
management.
Even though we found high level of genetic diversity in all subpopulations in
Finland, it does not necessarily imply that the capercaillie is not genetically vulnerable.
Changes in allelic distributions and reduction of genetic diversity can take quite a long
time unless the population goes through a severe bottleneck. The forest fragmentation in
Finland may be too recent to be detected in genetic analyses, and the observed level of
genetic diversity may reflect the past situation rather than the current one. High level of
inbreeding and partly restricted gene flow between leks indicate that limited dispersal
caused by, for example, forest fragmentation can have severe consequences in genetic
diversity of the species in the long term.
Male contribution in gene flow may be stronger than earlier thought. Male
dispersal may be connected to the long distance dispersal for new habitat patches,
including establishment of new leks. Therefore, the habitat availability may strongly
affect the genetic diversity of the populations. If there is a factor, like the mating
system, that increases the level of inbreeding in populations, it magnifies still the
importance of rare dispersal events. The strength of male dispersal is also closely related
to the polygamy of the species. Changes in landscape structure tend to decrease the size
of the leks, which in turn may decrease the level of polygyny. It has been observed that
larger leks with many displaying males attract more females than smaller leks (Alatalo
et al. 1992). Therefore, we assume that the size of the leks also has an important
influence on maintaining genetic diversity in population.
Dispersal can be linked to mortality of the sexes. Forest fragmentation can
increase the predation especially of the dispersing sex. Hunting may also increase
mortality of dispersing individual. To be able to discuss on the relation between
dispersal, mortality and fragmentation, local analyses of dispersal behaviour in different
habitats are needed. In general, there may be differences in dispersal behaviour between
geographical areas in Finland. The dispersal behaviour may vary between different
environments depending, for example, on the availability of habitats in that area. It is
too early to say discuss the local results as the analyses are still in process.
There was no clear evidence for the existence of subspecies in Finland,
confirming the results of Liukkonen-Anttila et al. (2004). Thus, the subspecies would
not be the best management units of the capercaillie. However, some structuring was
8
Conservation of genetic biodiversity in a changing landscape
found, and especially NE Finland differed from the other areas in terms of mtDNA
haplotype distribution. This result supports the idea that gene flow from the east can be
important in the maintenance of the genetic diversity in western Finland.
ACKNOWLEDGEMENTS
We want to thank the staff of Arctic Centre (University of Lapland), Finnish game and
Fisheries institute, Metsähallitus, and the Oulanka research station for their
contributions to work in the field, and Joanna Aalto and Laura Törmälä for work in the
lab. Many thanks also to David Hughes, Tuija Liukkonen and Pekka Pamilo giving
helpful comments on the manuscript. The study was funded by the Academy of Finland
(52772), the Finnish Cultural foundation, North Ostrobothnian Fund of the Culture
Foundation, Finnish Game Foundation and European Social Fund (Naturpolis
Kuusamo).
REFERENCES
Alatalo, R., Höglund, J., Lundberg, A. & Sutherland, W.J. 1992. Evolution of black
grouse leks: female preference benefit males in larger leks. Behav. Ecol. 3: 53-59.
Berg, L.M., Lascoux, M. & Pamilo, P. 1998. The infinite island model with sexdifferentiated gene flow. Heredity 81: 63-68.
Bouzat, J.L. & Johnson, K. 2004. Genetic structure among closely spaced leks in a
peripheral population of lesser prairie-chickens. Mol. Ecol. 13: 499-505.
Corander, J., Waldmann, P. & Sillanpää, M.J. 2003. Bayesian analysis of genetic
differentiation between populations. Genetics 163: 367-374.
—, Waldmann, P., Marttinen, P. & Sillanpää, M.J. 2004. BAPS 2: enhanced
possibilities for the analysis of genetic population structure. Bioinformatics 20:
2363-2369.
Crnokrak, P. & Roff, D.A. 1999. Inbreeding depression in the wild. Heredity 83: 260270.
Ennos, R.A. 1994. Estimating the relative rates of pollen and seed migration among
plant populations. Heredity 72: 250-259.
Gilpin, M. 1991. The genetic effective size of a metapopulation. Biol. J. Linn. Soc. 42:
165-175.
Griffiths, R., Double, M.C., Orr, K. & Dawson, R.J.G. 1998. A DNA test to sex most
birds. Mol. Ecol. 7, 1071-1075.
Frankham, R, Ballou, J.D. & Briscoe, D.A. 2002. Introduction to conservation genetics.
Cambridge University press. 617 p.
Hayashi, K. 1991. PCR-SSCP: a simple and sensitive method for detection of mutations
in the genomic DNA. PCR Methods Applic 1: 34-38.
Hedrick, P.W. 1999. Genetics of populations. Jones and Bartlett Publishers. 553 p.
— 2001. Conservation genetics: where are we now? Trends Ecol. Evol. 16: 629-636.
Helle, P., Kurki, S. & Lindén, H. 1999a. Change in the sex ratio of the Finnish
capercaillie Tetrao urogallus population. Wildl. Biol. 5: 25-31.
—, Lindén, H., Aarnio, M. & Timonen, K. 1999b. Metso ja metsien käsittely.
Metsähallituksen metsätalouden julkaisuja 20. (in Finnish)
9
Mäkipetäys & Orell
Helminen, M. 1963. Composition of the Finnish populations of Capercaillie, Tetrao
urogallus, and Black Grouse, Lyrurus tetrix, in the autumns of 1952-61, as
revealed by a study of wings. Papers Game Res. 23: 1-24.
Hjorth, I. 1970. Reproductive behaviour in Tetraonidae with specieal reference to
males. Viltrevy 7: 584-588.
Holsinger, K.E. 2000: Demography and extinction in small populations. In: Young, A.
G. and Clarke, G. M. (ed.). Genetics, demography and viability of fragmented
populations. Cambridge university press. P. 55-75.
Höglund, J. & Alatalo, R.V. 1995. Leks. Princeton University Press.
—, Alatalo, R., Lunberg, A., Rintamäki, P. & Lindell, J. 1999. Microsatellite markers
reveal the potential for kin selection on black grouse leks. Proc. R. Soc. Lond. B
266: 813-816.
—, Piertney, S.B, Alatalo, R.V., Lindell, J., Lundberg, A. & Rintamäki, P.T. 2002.
Inbreeding depression and male fitness in black grouse. Proc. R. Soc. Lond. B
269: 711-715.
Hilton-Taylor, C. (compiler) 2000. 2000 IUCN Red List of Threatened Species. IUCN,
Gland, Switzerland and Cambridge, UK.
Jaakola, M. 1999. Metson (Tetrao urogallus) soidinkäyttäytymisessä esiintyvät erot eri
metsoroduilla Suomessa. Unpublished MSci thesis. University of Joensuu,
Finland 30 p. (In Finnish).
Johansen, H. 1957. Rassen und Populationen des Auerhuhns (Tetrao urogallus).
Viltrevy 1: 233-266. (In German).
Keller, L.F. & Weller, D.M. 2002. Inbreeding effects in wild populations. Trends Ecol.
Evol. 5: 230-240.
Koivisto, I. 1963. Über den Ortswechsel der Geschlechter beim Auerhuhn nach
Markierungsergebnissen. Vogelwarte 22: 75-79. (In German).
Lande, R. 1995. Mutation and conservation. Conserv. Biol. 9: 782-791.
Lindén, H. 2002. The capercaillie – a focal species in landscape ecology at three
different scales. Finnish Game res. 48: 34-45.
— & Rajala, P. 1981. Fluctuations and long-term trends in the relative densities of
tetraonid populations in Finland, 1964-1977. Finnish Game Res. 39: 13-34.
— & Teeri, T. 1985. Genetic differentiation in the capercaillie, Tetrao urogallus,
populations. Hereditas. 102: 297-299.
— & Väisänen, R.A. 1986. Growth and sexual dimorphism in the skull of the
Capercaillie Tetrao urogallus: a multivariate study of geographical variation.
Ornis Scand. 17: 85-98.
Liukkonen-Anttila, T., Rätti, O., Kvist, L., Helle, P. & Orell, M. 2004. No clear genetic
structuring or subspecies ranges in the capercaillie (Tetrao urogallus) in Finland.
Ann. Zool. Fennici 41: 619-633.
—, Uimaniemi, L., Orell, M. & Lumme, J. 2002. Mitochondrial DNA variation and
phylogeography of the grey partridge (Perdix perdix) in Europe: from Pleistocene
history to present day populations. J. Evol. Biol. 15: 971-982.
Queller, D.C., Strassmann, J.E. & Hughes, C.R. 1993. Microsatellites and kinship.
Trends Ecol. Evol. 8: 285-288.
Raijmann, L.E.L., Van Leeuwen, N.C., Kersten, R. Oostermeijer, J.G.B. Den Nijs,
H.C.M. & Menken, S.B.J. 1994. Genetic variation and outcrossing rate in relation
to population size in Gentiana pneumonanthe L. Conserv. Biol. 8: 1014-1026.
Segelbacher, G., Paxton, R. J., Steinbruk, G., Trontelj, P. & Storch, I. 2000.
Characterization of microsatellites in capercaillie Tetrao urogallus (AVES). Mol.
Ecol. 9: 1919-1952.
10
Conservation of genetic biodiversity in a changing landscape
Smith, T.B. & Wayne, R.K. 1996: Molecular genetic approaches in conservation.
Oxford University Press. 483p.
Storaas, T. Kastdalen, L. & Wegge, P. 2001. Forest fragmentation increases brood
mortality of grouse by mammalian predators: a hypothesis. Finnish Game Res.
27. 86-93.
Storch, I. 1997. Male territoriality, female range use, and spatial organisation of
capercaillie Tetrao urogallus leks. Wildl. Biol. 3: 149-161.
Suter, W., Graf, R.F. & Hess, R. 2002. Capercaillie (Tetrao urogallus) and avian
biodiversity: testing the umbrella-species concept. Conserv. Biol. 3: 778-788.
Wegge, P. & Larsen, B. B. 1987. Spacing of adult and subadult male common
Capercaillie during the breeding season. Auk 104: 481-490.
11