7
Animal Generics 1986, 17, 335-341 Genetic variability in fallow deer, Damu duma L. G. B. HARTL, A. SCHLEGER & M. SLOWAK Forschungsinstitutfiir Wildtierkunde der Veterinarmedizinischen Universitat Wien, Vienna, Austria Summary. Twelve blood proteins and enzymes were tested for polymorphism in a herd of fallow deer, Duma duma L., bred for meat production in Western Germany, to investigate the genetic constitution of the population. Although an enzyme polymorphism was detected (Catalase) for the first time in this species, electrophore- tic variation is very low in comparison to other large ungulates. Possible explanations for this finding, such as recent inbreeding and a past genetic bottleneck, are given. The relationship between low genetic variation in biochemical marker systems and fitness is discussed. Keywords: fallow deer, protein and enzyme polymorphism, genetic variability, catalase, starch gel electrophoresis Introduction Populations of game animals are often exposed to phenomena which may cause extensive loss of genetic variability, like random genetic drift, inbreeding and founder effects. The main reasons are increasing isolation of wildlife populations by alteration of the landscape and the establishment of artificial populations in enclosures together with consequent annual reductions of population size by culling. Only a few large mammalian species such as red deer (Bergmann 1976; Gyllensten et al. 1983; Albert 1984), moose (Ryman et al. 1977, 1980; Wilhelmson et al. 1978; Gyllensten et al. 1980; Reuterwall 1980; Chesser et al. 1982), white-tailed deer (Manlove et ul. 1975, 1976; Ramsey et a/. 1979; Smith et al. 1984), reindeer (Roed 1985a, b, c), chamois (Nascetti et al. 1985; Miller & Hartl 1986a, b), ibex (Hartl 1986), wild boar (Hartl & Csaikl, in press; Smith et al. 1980; Steinmann 1976) and fallow deer (McDougall & Lowe 1968; Pemberton 1984; Pemberton & Smith 1985) have been extensively studied by biochemical genetic methods to investigate the genetic constitution of populations. Genetic variability in fallow deer, Dama duma L., is of particular interest, as attempts are being made to breed this species for meat production, as described by Bogner (1978) and Schick et al. (1983). In this study we present data on the genetic variability of an artificially founded herd, which has been bred for this purpose for about 10 years. Correspondence: I>r G. B. Hartl, Forschungsinstitut fur Wildtierkunde der Veterinarmedizinischen Universitat Wien, SavoyenstraBe 1, A-1160 Wien, Austria. Accepted I May 1986 335

Genetic variability in fallow deer, Dama dama L

Embed Size (px)

Citation preview

Page 1: Genetic variability in fallow deer, Dama dama L

Animal Generics 1986, 17, 335-341

Genetic variability in fallow deer, Damu duma L.

G . B. HARTL, A. SCHLEGER & M. SLOWAK Forschungsinstitutfiir Wildtierkunde der Veterinarmedizinischen Universitat Wien, Vienna, Austria

Summary. Twelve blood proteins and enzymes were tested for polymorphism in a herd of fallow deer, Duma duma L. , bred for meat production in Western Germany, to investigate the genetic constitution of the population. Although an enzyme polymorphism was detected (Catalase) for the first time in this species, electrophore- tic variation is very low in comparison to other large ungulates. Possible explanations for this finding, such as recent inbreeding and a past genetic bottleneck, are given. The relationship between low genetic variation in biochemical marker systems and fitness is discussed. Keywords: fallow deer, protein and enzyme polymorphism, genetic variability, catalase, starch gel electrophoresis

Introduction

Populations of game animals are often exposed to phenomena which may cause extensive loss of genetic variability, like random genetic drift, inbreeding and founder effects. The main reasons are increasing isolation of wildlife populations by alteration of the landscape and the establishment of artificial populations in enclosures together with consequent annual reductions of population size by culling. Only a few large mammalian species such as red deer (Bergmann 1976; Gyllensten et al. 1983; Albert 1984), moose (Ryman et al. 1977, 1980; Wilhelmson et al. 1978; Gyllensten et al. 1980; Reuterwall 1980; Chesser et al. 1982), white-tailed deer (Manlove et ul. 1975, 1976; Ramsey et a/. 1979; Smith et al. 1984), reindeer (Roed 1985a, b, c), chamois (Nascetti et al. 1985; Miller & Hartl 1986a, b), ibex (Hartl 1986), wild boar (Hartl & Csaikl, in press; Smith et al. 1980; Steinmann 1976) and fallow deer (McDougall & Lowe 1968; Pemberton 1984; Pemberton & Smith 1985) have been extensively studied by biochemical genetic methods to investigate the genetic constitution of populations. Genetic variability in fallow deer, Dama duma L., is of particular interest, as attempts are being made to breed this species for meat production, as described by Bogner (1978) and Schick et al. (1983). In this study we present data on the genetic variability of an artificially founded herd, which has been bred for this purpose for about 10 years.

Correspondence: I>r G. B. Hartl, Forschungsinstitut fur Wildtierkunde der Veterinarmedizinischen Universitat Wien, SavoyenstraBe 1, A-1160 Wien, Austria. Accepted I May 1986

335

Page 2: Genetic variability in fallow deer, Dama dama L

336 G. B. Hart1 et al.

Material and methods

In 1983 whole blood samples were colleited from 81 fallow deer (females and young males) from a total herd of 120 at the Bayerische Landesanstalt fur Tierzucht at Grub in Western Germany. Details on breeding techniques and management at this station are given by Bogner (1978) and Schick ef al. (1983). Haemolysates and sera were prepared according to Csaikl et al. (1980) and stored at -20°C for several months. In 1984 and early 1985 a further 37 serum samples and 18 whole blood samples were collected from different animals from the same herd. Horizontal starch gel electrophoresis was carried out using the following buffer systems: - a continuous phosphate buffer described in Csaikl et al. (1980) for LDH, 6-PdD,

- a continuous tris-citrate buffer described in Manlove ef al. (1975) for MDH; - a discontinuous histidine-sodium citrate buffer described in Brewer & Sing

(1970) for CAT; - a continuous tris buffer described by Gahne (1960) and a discontinuous

borate-tris buffer described by Sandberg & Bengtsson (1970) for Hb; - a discontinuous tris-borate buffer described by Scott (1970) for Alb and Tf; and - a discontinuous citrate-borate buffer described by Braend (1970) for Pra.

After electrophoresis the gels were sliced and stained: for LDH, 6-PGD, G-6-PD, SOD, GPI and MDH as described by Csaikl et al. (1980), for ES according to Shaw & Prasad (1970), and for CAT according to Thorup et al. (1961). Serum proteins were stained with amido black.

To exclude the possibility of misinterpretation due to degradation of proteins in frozen samples, freshly prepared blood samples from three fallow deer kept at our institute were also screened. Except for a slight decrease in enzyme activity in the older samples no ageing effects were found in the banding patterns.

The genetic interpretation of the electrophoretic patterns was based on the principles described by Harris (1980) and Harris & Hopkinson (1976).

G-6-PD, SOD, ES and GPI;

Results

Table 1 lists the enzymes and serum proteins studied and the putative loci and alleles found. In terms of the putative number of genetic loci involved, LDH, MDH, 6-PGD, G-6-PD, CAT and SOD could be easily interpreted according to Harris & Hopkinson (1976). The enzyme glucosephosphate isomerase (GPI) showed a phenotype similar to the banding patterns observed in red deer by Gyllensten ef al. (1983), possibly indicating the presence of two loci. In ES two anodally migrating isoenzymes with very different mobility were scored, possibly being the gene products of two different loci. In Alb, Pra and Hb a single invariant band and in Tf a three-banded phenotype were found. For the calculation of the proportion of polymorphic loci and average heterozygosity, P and H respectively, each of the serum proteins was assessed to be the product of one locus.

Page 3: Genetic variability in fallow deer, Dama dama L

Genetic variability in fallow deer 337

Table 1. List of enzymes and proteins studied with putative numbers of loci and alleles found ( n = sample size)

Putative Variants (putative EC number Enzyme name Abbrevation loci alleles found) n

1.1.1.27

1.1.1.37

1.1.1.44

1.1.1.49

1.11.1.6 1.15.1.1

3.1.1.1

5.3.1.9

Lactate dehydrogenase Malate dehydrogenase 6-phosphogluconate dehydrogenase Glucose-6-phosphate dehydrogenase Catalase Superoxide dismutase Esterase

Glucosephosphate isomerase Proteins Albumin Prealbumin Transferrin Haemoglobin

LDH

MDH

6-PGD

G-6-PD

CAT SOD

ES

GPI

Alb Pra Tf Hb

A B S

1

1

1 A

1 2 1 2

1 1 1 1

1 1 1

1

1

2 1

1 1 1 1

1 1 1 1

18

18

18

18

81 18

18

58 40

118 118 118 81

None of the enzymes and serum proteins showed variation except catalase. The CAT isoenzymes migrate anodally but are poorly resolved. However, after several electrophoretic runs, where identical patterns could be scored in each specimen, an allelic interpretation seemed possible to us. We assume that the Cat locus is polymorphic, with the two different single banded phenotypes corresponding to the putative Cat homozygotes. Both homozygotes and the putative heterozygote phenotype were scored (Fig. 1). However, the number of heterozygotes observed was not in agreement with the Hardy-Weinberg expectations (Table 2). This may be caused by the breeding structure of the herd, where only two males are used for

Table 2. The observed and expected catalase phenotypes in fallow deer

n = 81 A AB B X2 df

Observed 48 22 11 8.039* 1 E:xpected 43.16 31.93 5.90

* P(O.1 Frequency of putative allele a = 0.730, of putative allele b = 0.270

Page 4: Genetic variability in fallow deer, Dama dama L

338 G. B. Hart1 et al.

Figure 1. Phenotypes and allelic interpretation of Catalase. The most common allele is designated ‘u ’ . The five-banded pattern in the heterozygous phenotype is hypothesized with respect to the tetrameric structure of the enzyme (Harris & Hopkinson 1976) but could not be resolved on the gel.

breeding (though different ones every year). Using the same techniques a polymorphism in CAT was detected in horses as well by Schleger (1974). Calculated according to the formulae given by Ayala (1977) in the fallow deer herd studied the proportion of polymorphic loci is 0.066 and average heterozygosity is 0-018.

Discussion

Until now only fallow deer populations from Great Britain have been studied extensively by biochemical genetic methods (McDougall & Lowe 1968; Pemberton 1984; Pemberton & Smith 1985). Although a relatively large number of loci, individuals and populations were surveyed no genetic variation was detected. A first study of a small sample of German fallow deer also revealed no polymorphism at 13 protein loci (Scheil, personal communication). Our data are based on the investiga- tion of 12 serum proteins and enzymes in a Bavarian population, which was founded by mixing specimens from different sites and origins in Germany. Our results support the hypothesis that European fallow deer are generally depauperate in electrophore- tically detectable protein variants. Apart from a possible polymorphism in haemo- globin detected by Butcher & Hawkey (1977) we report the first polymorphism in a protein system found in fallow deer. Unfortunately, catalase has not been studied before in this species, so nothing can be said for the present about the distribution of this polymorphism in European fallow deer populations.

Pemberton & Smith (1985) discuss several possible explanations for the lack of protein variants in British fallow deer, e.g. inbreeding for different colour morphs and a genetic bottleneck when this species was introduced into Great Britain or even before. Considerable genetic variability may also have been lost in continental populations by consequent inbreeding for different colour morphs or other

Page 5: Genetic variability in fallow deer, Dama dama L

Genetic variability in fallow deer 339

morphological features throughout most of Europe (see Ueckermann & Hansen 1983). On the other hand, our data support the hypothesis that low genetic variability in European fallow deer might be the result of a genetic bottleneck already occurring before fallow deer were introduced to Great Britain. Thus, the loss of genetic variability may indeed date back to the times when this species became extinct over most of Europe during the last glaciation, or when it was reintroduced by man some 12 00&5000 years ago (see Pemberton & Smith 1985).

Low electrophoretic variability probably due to genetic bottlenecks in population history is reported for a variety of large mammalian species such as Pkre David deer (Ryder et al. 1981), alpine ibex (Hart1 1986), the polar bear (Allendorf et al. 1979), elephant seal (Bonnell & Selander 1974) and cheetah (O’Brien el al. 1983). Only in the last species is a negative effect of reduced genetic variability on fitness suggested. As a consequence of inbreeding, Ralls et a f . (1979) found an increase of juvenile mortality in 15 species of captive ungulates. In contrast, fallow deer are reported to be rather resistant to inbreeding depression (Schick et a f . 1983; Ueckermann & Hansen 1983; Pemberton & Smith 1985). This could be explained after examination of the two different effects of inbreeding or genetic drift. On one hand, genetic variability is lost, which may have a long-term effect on the adaptive potential of a species. Nothing can be concluded about such an effect in fallow deer for the present. On the other hand, over a period of prolonged inbreeding, most deleterious genes may also be lost, which makes a population resistant to the dramatic short-term effects of inbreeding. In fallow deer the latter explanation might be the case and some selection mechanisms favouring inbreeding have been suggested by Smith (1979). In our 1 bpulation no malformations have been detected over about 10 years. After foundation of the herd the rate of juvenile mortality and still births was rather high, but was probably the result of catching pregnant females. In time the losses were reduced as a result of greater experience in management of fallow deer at this station (Schick 1982; Bogner, personal communication).

Acknowledgement

The authors are indebted to Prof. Dr H. Bogner, president of the Bayerische Landesanstalt fur Tierzucht at Grub, for the gift of material together with useful information about the population studied and to Dr P. Matzke, Dr J. Kotremba, Tzt H. Kren and Mr Popp for the dynamical help in sampling. We are also grateful to Prof. Dr W. Schleger and the members of the institute of Animal Breeding of the Veterinary University of Vienna for stimulating discussions and to Dr F. Csaikl for reading the manuscript.

References

Albert S. (1984) Untersuchung der Hamoglobin-Varianien lion Roiwild (Cervus elaphus L.) mit Hiye der Elektrofokussierung. - Ein Beiirag zur Analyse der genetischen Infrastruktur einheimischer Rotwild- Populationen. Dissertation, Justus Liebig University, Giel3en.

Allendorf F.W., Christiansen F.B., Dobson T. , Eanes W.F. & Frydenberg 0. (1979) Electrophoretic variation in large mammals. I. The polar bear, Thalarctos maritimus. Hereditas 91, 19-22.

Page 6: Genetic variability in fallow deer, Dama dama L

340 G. B. Hartl et al.

Ayala F.J. (1977) The genetic structure of populations. In: Evolufion (ed. by T. Dobzhansky, F. J . Ayala, G . L. Stebbins & J . W. Valentine). W. H. Freeman & Co, San Francisco.

Bergmann F. (1976) Beitrage zur Kenntnis der Infrastrukturen beim Rotwild. Teil 11. Erste Versuche zur Klarung der genetischen Struktur von Rotwildpopulationen an Hand von Serumprotein-Polymorphis- men. Zeitschrift fur Jagdwissenschaft 22, 28-35.

Bogner H. (1978) Damwild - Ein landwirtschaftliches Nutztier? Tierurzrliche Praxis 6 , 257-65. Bonnell M.L. & Selander R.K. (1974) Elephant seals: genetic variation and near extinction. Science 184,

Braend M. (1970) Genetics of horse acidic praealbumins. Genetics 65,495 Brewer G.J. & Sing C.F. (1970) An Infroduction to lsozyme Techniques. Academic Press, London. Butcher P.D. & Hawkey C.M. (1977) A comparative study of haemoglobins from the artiodactyla by

Chesser R.K., Reuterwall C . & Ryman N. (1982) Genetic differentiation of Scandinavian moose Alces

Csaikl F., Engel W. & Schmidtke J. (1980) On the biochemical systematics of three Apodemus species.

Gahne B. (1960) Zmmunogenetica Edinburgensis 132. Gyllenstens U., Reuterwall C . , Ryman N. & Stahl G . (1980) Geographical variation of transferrine allele

Gyllensten U. , Ryman N., Reuterwall C. & Dratch P. (1983) Genetic differentiation in four European

Harris H. (1980) The Principles of Human Biochemical Genetics. North Holland, Amsterdam. Harris H. & Hopkinson D.A. (1976) Handbook of enzyme electrophoresis in human genetics. North

Holland, Amsterdam. Hartl G.B. (1986) Steinbock und Gemse im Alpenraum - genetische Variabilitat und biochemische

Differenzierung zwischen den Arten. Zeitschrift fur Zoologische Systematik und Evolutionsforschung 24.

Hartl G.B. & Csaikl F. Genetic variability and differentiation in wild boars (Sus scrofa ferus L.): comparison of isolated populations. Journal of Mammalogy (In press).

McDougall E.I. & Lowe V.P.W. (1968) Transferrin polymorphism and serum proteins of some British deer. Journal of Zoology 155, 131-40.

Manlove M.N., Avise J.C., Hillestad H.O.. Ramsey P.R., Smith M.H. & Straney D.O. (1975) Starch gel electrophoresis for the study of population genetics in white-tailed deer. Proc. Ann. Conf. S. E. Assoc. Game and Fish Comm. 29, 392-403.

Manlove M.N., Smith M.H.. Hillestad H.O., Fuller S.E., Johns P.E. & Straney D.O. (1976) Genetic subdivision in a herd of white-tailed deer as demonstrated by spatial shifts in gene frequencies. Proc. Ann. Conf. S. E. Assoc. Game and Fish Comm. 30, 487-92.

Miller C. & Hartl G.B. (1986a) Genetic variation in chamois from the Alps (Rupicapra rupicapra L.). Proceedings of the 1st Symposium on Cyiogenetics and Biochemical Generics in Wild Animals, Giejlen, 25-26 October 1985. (In press).

Miller C . & Hartl G.B. (1986b) Genetic variation in two alpine populations of chamois (Rupicupru rupicapra L.). Zeitschrift fur Suugefierkunde 51, 114-21.

Nascetti G . , Lovari S.. Lanfranchi P., Berducou C., Mattiucci S. tk Bullini L. (1985) Revision of Rupicapra genus 111: electrophoretic studies demonstrating species distinction of chamois populations of the Alps from those of the Appennines and Pyrenees. In: Biology and Managemeni ofMounfain Ungulates (ed. by S. Lovari), pp. 56-62. Croom Helm, Beckenham.

O'Brien S.J., Wildt D.E., Goldman D. , Merril C.R. & Bush M. (1983) The cheetah is depauperate in genetic variation. Science 221, 459-62.

Pemberton J.M. (1984) A genetic study of British fallow deer using gel electrophoresis. In: The Fallow Deer m a m a dama L.). Proceedings of a Symposium held in Budapest, 16-17January (ed. by S. Toth).

90S9.

isoelectric focusing. Comparative Biochemisrry and Physiology 56B, 335-9.

alces populations over short geographical distances. Oikos 39, 125-30.

Comparative Biochemistry and Physiology 65B, 41 1-4.

frequencies in three deer species from Scandinavia. Hereditas 92,237-41.

subspecies of red deer (Cervus elaphus L.). Heredity 51, 561-80.

pp. 85-8.

Page 7: Genetic variability in fallow deer, Dama dama L

Genetic variability in fallow deer 341

Pemberton J.M. & Smith R.H. (1985) Lack of biochemical polymorphism in British fallow deer. Heredity

Ralls K., Brugger K. & Ballou J. (1979) Inbreeding and juvenile mortality in small populations of ungulates. Science 206, 1101-3.

Ramsey P.R., Avise J.C., Smith M.H. & Urbston D. (1979) Genetics of white-tailed deer in South Carolina. Journal of Wildlife Management 43, 13642.

Reuterwall C. (1980) Genetic variation in a large game species, the moose (Alces alces): patterns of differentiation and some management implications. PhD Thesis, University of Stockholm.

Roed K.H. (1985a) Comparison of the genetic variation in Svalbard and Norwegian reindeer. Canadian Journal of Zoology 63, 2038-42.

Roed K.H. (19851,) Genetic variability in Norwegian semi-domestic reindeer (Rangifer tarandus L.). Hereditas 102, 177-84.

Roed K.H. (1985~) Genetic differences at the transferrin locus in Norwegian semi-domestic and wild reindeer (Rangifer tarandus L.). Hereditas 102, 199-206.

Ryder O.A.. Brisbin P.C., Bowling A.T. & Wedemeyer E.A. (1981) Monitoring genetic variation in endangered species. In: Evolution Today. Proceedings of the Second International Congress of Systematic and Evolutionary Biology (ed. by G . G. E. Scudder & J . L. Reval), pp. 417-24.

Ryman N., Beckman G., Bruun-Petersen G . & Reuterwall C. (1977) Variability of red cell enzymes and genetic implications of management policies in Scandinavian moose (Alces alces). Hereditas 85,157-62.

Ryman N., Reutrrwall C., Nygren K. & Nygren T. (1980) Genetic variation and differentiation in Scandinavian moose (Alces alces): are large mammals monomorphic? Evolution 34, 1037-49.

Sandberg K. & Bengtsson S. (1970) Polymorphism of haemoglobin and 6-phosphogluconate dehydro- genase in horse erythrocytes. Proceedings of the 12th European Conference on Animal Blood Groups and Biochemical Polymorphism, Budapest, p. 275.

Schick R. (1982) lintersuchungen zur Haltungstechnik und Wirtschaftlichkeit der nutztierartigen Haltung von Dam wild (Cervus dama L . 1958) unter Berucksichtigung bayerischer Standortbedingungen. Dissertation, Universitat fur Bodenkultur, Vienna.

Schick R., Bogner H. , Matzke P., Braun W., Burgstaller G. & Vollert H. (1983) Untersuchungen zur Haltungstechnik und Wirtschaftlichkeit der nutztierartigen Haltung von Damwild im Vergleich zur Koppelschafhal tung. Bayerisches Landwirtschaftliches Jahrbuch 4, 396455.

Schleger W. (1973) Genetischer Polymorphismus im Serum und Erythrozytenhamolysat beim Pferd. Wiener Tieriirzfliche Monafsschrift 61. Jhrg., Heft 11, 293-300. Heft 12, 321-43.

Scott A.M. (1970) A single acid gel for the separation of albumins and transferrins in horses. Animal Blood Groups and Biochemical Genetics 1, 253.

Selander R.K. & Kaufman D.W. (1973) Genic variability and strategies of adaptation in animals. Proceedings of the National Academy of Sciences of the USA 70, 1875-7.

Shaw C.R. & Prasad R. (1970) Starch gel electrophoresis of enzymes - a compilation of recipes. Biochemical Genetics 4,297-320.

Smith R.H. (1979) On selection for inbreeding in polygynous animals. Heredity 43, 205-11. Smith M.H.. Baccus R. , Hillestad H.O. & Manlove M.N. (1984) Population genetics of the white-tailed

deer. In: Ecoiogy and Management of White-tailed Deer(ed. by L. Halls), pp. 119-28. Stackpole Books, New York.

Smith M.W., Smith M.H. & Lehr-Brisbin I. Jr (1980) Genetic variability and domestication in swine. Journal of Mammalogy 61, 39-45.

Steinmann H. (1976) Biochemische Polymorphismen in Bsterreichischen Wildschweinpopulationen (Sus scrofa ferus). Dissertation. Veterinarmedizinische Universitat Wien.

Thorup O.A., Strole W.B. & Leave11 B.S. (1961) A method for the localization of catalase on starch gels. Journal of Laboratory and Clinical Medicine 58, 122.

Ueckermann E. & Hansen P. (1983) Das Damwild. Paul Parey, Hamburg und Berlin. Wilhelmson M., Juneja R.K. & Bengtsson S . (1978) Lack of polymorphism in certain blood proteins and

55, 199-207.

enzymes of European and Canadian moose (Alces alces). Naturaliste canadiensis 105, 445-9