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Home , Dama (genus), European fallow deer, Meles (genus), Moose, Mule deer, Reindeer

Heredity 55 (1985) 199-207 The Genetical Society of Received 6 February 1985

Lack of biochemical polymorphism in British fallow

J. M. Pemberton* Wildlife Management Group, Department of Pure and Applied Zoology, University of Reading, Whiteknights, and R. H. Smith P.O. Box 228, Reading RG6 2AJ

Seven-hundred and ninety-four samples of fallow deer ( dama L.) blood or tissue were collected from 37 sites in England and Wales. A selection of these samples was screened for electrophoretic variation at each of 30 loci (minimum of 88 samples per locus). No genetic variation was found. Possible explanations for the lack of polymorphism are discussed. It is suggested that experienced a genetic bottleneck during a period of captivity in or times.

INTRODUCTION

Electrophoresis has been used to generate genetic Most of the applications mentioned above data about a number of deer . To date at imply the presence of considerable intraspecific least 70 papers and reports have been written in polymorphism in deer, which is certainly true for this field. The information obtained has been used the four species on which studies have so far con- to study genetic differentiation between species centrated. Most work on the Old World (Baccus et a!., 1983), subspecies (Gyllensten et a!., (Rangifer tarandus tarandus) has been limited to 1983; Dratch and Gyllensten, in press) and popula- a single locus, transferrin, at which major surveys tions (Soldal and Staaland, 1980; Ryman et a!., have each revealed between 7 and 12 alleles 1980; Gyllensten et a!., 1983; Dratch and (Braend, 1964; Turubanov and Shubin, 1971; Gyllensten, in press) and to examine population Zhurkevich and Fomicheva, 1976; Soldal and subdivision, givinginsightsintodispersal Staaland, 1980; Røed, in press). The remaining behaviour (Manlove et aL, 1976; Ramsey et aL, three species have been surveyed extensively both 1979; Chesser et a!., 1982). Other authors have geographically and in terms of the number of loci sought relationships between performance and screened, and table 1 summarises the principal genotype (Johns et a!., 1977; Smith et a!., 1982; studies. Points to notice are that none of the species Cothran et a!., 1983) or changes in genotype completely lacks detectable variation and that the frequencies over time (Baccus eta!., 1977; Chesser white-tailed deer shows an apparently higher level et a!., 1982), suggesting the action of natural selec- of genetic variation than , and tion. Among practical uses, the discrimination of wapiti. Indeed, all the white-tailed deer popula- species from blood spots or tissue scraps is of value tions and some of the moose and wapiti popula- in law enforcement (Oates et aL, 1979; Lawton tions studied have average heterozygosities (H) and Sutton, 1981; McClymont et a!., 1982) and greater than the H for all (H = genetic information is of obvious interest to con- 0.033-0.039)derived by various authors (Powell, servationists, for example in the planning of 1975; Nevo, 1978; Avise and Aquadro, 1982; introductions (Smith eta!., 1976; Ryder eta!., 1981; Baccus et a!., 1983) which argues further against Gyllensten et a!., 1983). A number of uses for the generalisation that large mammals are electrophoresis studies can also be envisaged in monomorphic (see Ryman et a!., 1980). the growing deer farming industry, ranging from The present study was undertaken as a first the assessment of genetic differences between lines step towards using electrophoretically-detectable to paternity testing. variation to investigate the occurrence of *Presentaddress: Department of Zoology, University College in fallow deer (Dama dama L.) London, Gower Street, London WC1E6BT. populations (Smith, 1979). Previously published 200 J. M. PEMBERTON AND R. ft SMITH

Table I Summary of the mostextensive genetic surveys ofdeer speciesto date Number (and location) of Number Range of average populations of loci heterozygosity Species surveyed screened (H) found Reference white-tailed deer 8 (SE. USA) 35 0049—0092 Smith et a!., in press ( virginianus) moose 18 () 23 0006-0047 Ryman ci a!., 1980 (Alces alces) red deer and wapiti 22 (NW. ) 34 0000-0031 Gyllensten ci al., 1983 ( elaphus) 11 (NW. USA) 28 0004-0060 Dratch and Gyllensten, in press electrophoresis and isoelectric focusing studies of blood sampled) while samples of muscle only were fallow deer include a survey of serum proteins, obtained from 51 carcasses in a butcher's cold especially transferrin, by McDougall and Lowe store. (1968), haemoglobin studies by Maughan and Fig. I also gives a rough indication of the Williams (1967), Butcher and Hawkey (1977) and number of sampled per site which ranged Lawton and Sutton (1981) and the screening of from one (four sites in Berkshire and Hampshire) LDH by Munday et a!. (1974). Only the Butcher to 126 (Margam Park, South Wales). The "sites" and Hawkey (1977) study suggested a polymorph- themselves consisted of 14 more-or-less enclosed ism in fallow deer. However, besides the small parks and 23 areas holding wild fallow deer. number of loci screened, all the studies mentioned In addition to fallow deer samples, 133 blood involved limited sampling of individuals and/or samples and 14 post mortem tissue sets were collec- populations. Since initial small surveys of the ted from red deer from two sites and blood samples species shown in table I also sometimes failed to were taken from six (Munliacus reevesi) reveal variation (e.g., transferrin: Braend, 1962; from one site, for comparative purposes. Johnson, 1968; Seal and Erickson, 1969) the pre- Blood was collected into heparinised tubes vious fallow deer studies do not necessarily indi- (Vacutainer and Sterilin). Blood samples from live cate the outcome of a more thorough study. deer and from some freshly deer were brought Indeed, given the results of existing large surveys to Reading in a vacuum flask containing melting of deer species (see above), the widespread, geneti- ice and were processed within 48 hours of collec- cally controlled coat colour polymorphism of Brit- tion. Blood samples collected by stalkers were ish fallow deer (Chapman and Chapman, 1975, posted to Reading and processed on arrival. After pp. 23-3 1) and a suggestion of genetically deter- centrifugation (3000 rpm for 15 minutes) the mined skeletal variation in this species (Chapman plasma was drawn off, separated into aliquots and and Chapman, 1969), the present survey was fully frozen. All samples were stored at —30°C. Approxi- expected to reveal genetic variation. mately 2 ml of the remaining red cells were washed and centrifuged two to three times in 8 ml 0.85 per cent NaC1 solution. When a clear supernatant was MATERIALSAND METHODS produced, the red cells were lysed with 1 ml dis- tilled water, divided into aliquots and frozen. Bloodand post mortem tissues were collected from Post mortem tissues collected by stalkers were fallow deer from the sites in England and Wales stored in domestic freezers until retrieved. The shown in fig. 1. In total 794 individual deer from samples were brought to Reading in a vacuum flask 37 sites were sampled in some way, but we empha- packed with solid CO2 to prevent thawing. The size the heterogeneity of the samples. Blood was tissues were kept frozen until immediately before obtained by bleeding live deer (389 animals), by electrophoresis when sections weighing approxi- post mortem sampling (280 animals) and by taking mately 600mg were homogenised in an equal aliquots of samples collected by other researchers volume of distilled water. All homogenising was (43 animals). Post mortem tissue sets consisting of carried out by hand in a ground glass homogeniser muscle, and were collected by stalkers (Gallenkamp) or with a pestle and mortar, when from 179 animals (including 148 which were also 200 mg sterilised sand was added to aid grinding. LACK OF POLYMORPHISM 201

• >30 • 11—30 . •<11

••.I ••.'

• S.

Figure 1Sites in England and Wales from which fallow deer samples were obtained; size of circle indicates number of animals sampled.

Homogenates were centrifuged (3000 rpm for 15 mammals, because they stain up at the same time minutes) and the supernatant was then used in as the "target" loci, or because they are cheap to electrophoresis. stain or easy to resolve. Electrophoresis was carried out using a mixture In a project with a fixed time limit, the number of Shandon and home made equipment. General of loci which can be screened is inversely related procedure for horizontal starch gel electrophoresis to the number of individuals screened at each did not differ importantly from that described by locus. In the present study, after the first few loci Manlove et a!. (1975). Buffer systems and stain had been screened, calculations were made to help recipes were taken from the literature or followed decide how many samples from the "sample bank" those in use in the laboratory of Professor R. J. needed to be examined at a locus and found to be , University College London. In several cases indistinguishable for that locus to be regarded as more than one buffer system was tried. Preferred monomorphic. Taking a locus in which the rarer buffer systems, tissues used and references to allele is at frequency 001 as a minimum criterion detailed methods are given in table 2. Full details of polymorphism and assuming Hardy-Weinberg are given in Pemberton (1983). equilibrium, each individual examined gives a Haemoglobin was focused in 03 mm thick 7 probability of 098 of not detecting such a poly- per cent acrylamide gels containing pH 6-8 morphism. The probability of detecting poly- Ampholines (LKB) at a concentration of 02 per morphism is then (1_0.981)=0.02 after one cent. Seventeen chroma Whatman paper was sample, (1_0.98b0)=0.18 after 10 samples, etc. soaked in 1 M H3P04 at the anode and I M NaOH Whereas the probability of detecting polymorph- at the cathode. Samples were loaded on pieces of ism increases rapidly with the first few samples 1 MM filter paper laid on the surface of the gel. examined, the reward (in terms of increased proba- Voltage was applied via a focusing jacket made in bility of detecting polymorphism) in return for the Zoology Department workshop. effort decreases as the probability approaches FO. The loci screened were chosen because they In the present study, it was decided, somewhat are known to be polymorphic in deer or other arbitrarily, to try to examine at least 100 individuals 202 J. M PEMBERTON AND R. H. SMITH

Table 2Electrophoresis methods and sample sizes used in the present study. Key: under Tissues studied": p plasma, h haemolysate, 1liver, k kidney, m muscle; under "Reference and Method": gel concentration indicated as %, poly. = polyacrylamide,disc, discontinuous buffer system Reference and Method (electrophoresis on starch gels except Tissues No. of No. of No. of Protein where stated) studied loci animals study sites

Tf (transferrin) Manlove eta!. (1975). 124% lithiump 368 13 hydroxide. Alb (albumin) AsforTf p 368 13 sag (slow a-globulin) AsforTf p 368 13 Hb (haemoglobin) After Lawton and Sutton (1981). Isoelectric h 224 15 focusing, 7% poly. GPD (glycerol-3-phosphateHarris and Hopkinson (1976). 11% tris-I, k 88 13 dehydrogenase EDTA-maleate SDH (sorbitoldehydro-Op't Hof eta!.(1969).12% tris-phosphate. I 100 14 genase) LDH (lactate dehydro-Manlove eta!. (1975).124% disc. tris- m 2 134 18 genase) citrate. MDH (malatedehydro-Harris and Hopkinson (1976). 11% phos- k, I, m 2 109 17 genase) phate-citrate. IDH (isocitrate dehydro-As for MDH k,l,m 2 109 17 genase) 6-PGD (6-phosphogluconateHarris and Hopkinson (1976), under ADA. I,h 151 20 dehydrogenase. 11%phosphate. GDH ( dehydro-Harris and Hopkinson (1976). 11% Iris- I 115 14 genase) citrate. G6PDH (glucose 6-phos-After Ruddle eta!.(1968)13% tris-E1)TA-1, h 132 15 phate dehydrogenase) borate. SOD (super-oxide dis-As for LDH and G6PDH. I, m, h 2 207 22 mutase) GOT(glutamateoxaloace-DeLorenzo and Ruddle (1970). 12% k, I Ilt 16 tate transamimase) citrate-phosphate. AK (adenylate kinase) Harris and Hopkinson (1976). 11% his- k, I 107 14 tidine-citrate. POM (phosphogluco-Harris and Hopkinson (1976). 11% Iris- I 105 15 mutase) EDTA-maleate. Est (esterases) As for Tf. p 2 230 17 AP (acid phosphatase) As for 6-PGD h 115 14 CA (carbonic anhydrase) As for G6PDH h 2 107 9 GPI (glucose phosphateHarris and Hopkinson (1976). 11% tris- k 101 16 isomerase) citrate. at each locus, giving a probability of 087 of detect- et a!.,1980; Dratch and Gyllensten, in press). To ing a borderline polymorphism. Table 2 shows the avoid such problems, each locus screened in the number of individuals examined for each system: present study was examined in samples represent- the target of 100 was achieved for all except one ing several sampling sites. Table 2 shows the num- system, GPD (88 samples, see table 2). ber of sampling sites represented by the samples A related decision concerned which samples screened for each system. from the "sample bank" to examine. Previous Finally, to maximise the use made of samples, genetic studies of deer species have revealed con- different combinations of samples were used in the siderable between-population variation in the level screening of different loci. of polymorphism detected (table 1). Preliminary surveys of moose and wapiti involving RESULTS limited sampling of populations (Ryman ela!., 1977;Cameron and Vyse, 1978) were taken to Underthe electrophoresis conditions employed, indicate that these species had unusually low levels none of the presumed 30 loci screened in the fallow of polymorphism, a finding which was not borne deer samples showed variation which could be out by subsequent, more extensive surveys (Ryman interpreted on a genetic model. LACK OF POLYMORPHISM 203

Broadly speaking, band patterns were as expec- revealed that the variants were post-collection ted on the basis of previous studies of deer (e.g., changes probably caused by bacterial growth while Manlove et a!., 1975). The following account uses the samples were in transit (Lowe and McDougall, the locus designations of Allendorf and Utter 1961). Results from posted blood samples were (1979) in which, when an enzyme is encoded by therefore excluded from the final figure for the more than one locus, locus products are labelled number of individuals examined for transferrin from cathode to anode. In brief, IDH-2, G6PDH, given in table 2. Occasional aberrant results at SOD-2, Est-2 and Aib zymograms consisted of a other loci did not coincide with the band patterns single anodal band of high mobility; GPD, MDH- expected for heterozygotes on the basis of the 2, GDH, SOD-i, GOT-2, AK-i and -2, PGM-1 subunit structure known in other mammals and and -2, CA-i and -2 and slow a-globulin could usually be attributed to denaturing of the zymograms consisted of a single anodal band of sample. A putative genetic polymorphism in the moderate mobility; IDH-1 and 6-PGD zymograms slow a-globulin region of plasma was discounted consisted of a single anodal band of low mobility. on the basis of results from repeat bleedings of GOT-i was revealed as a cathodal band of medium individual deer and from deer of known related- mobility while SDH and MDH-i products formed ness held in enclosures for breeding studies (Smith a single cathodal band of low mobility. The and Johnson, 1982). remaining locus products formed more complex While failing to reveal genetic polymorphism band patterns. LDH-i and -2 products combined in the fallow deer samples, the electrophoresis in tetramers to form five isozymes ranging from systems detected previously described transferrin the origin to the anode, as described in the white- and IDH-2 polymorphisms in the red deer tailed deer (Manlove, et a!., 1975). Fallow deer (McDougall and Lowe, 1968; Gyllensten et al., transferrin consisted of a double-banded anodal 1983) and a previously undescribed transferrin system of moderate mobility, as described by polymorphism in the Reeve's muntjac, involving McDougall and Lowe (1968). Double-banded two alleles. The pH 6—8 isoelectric focusing unam- anodal patterns were also observed for the plasma biguously demonstrated foetal haemoglobin in esterase system designated Est-1 and for AP for neonatal fallow deer, repeated the finding of which a similar band pattern has been described haemoglobin polymorphism in Reeve's muntjac in other mammals (Harris and Hopkinson, 1976). (Maughan and Williams, 1967) and revealed vari- As recorded by previous workers (Butcher and ation in red deer haemoglobin patterns, not pre- Hawkey, 1977; Lawton and Sutton, 1981), focused viously described. fallow deer haemoglobin also consists of two major bands. The GPI zymogram consisted of three evenly spaced anodal bands, a pattern also DISCUSSION observed in other deer species which has prompted speculation that, in cervids, two GPI loci are Thepresent study does not show that British fallow expressed (Manlove et a!., 1975; Ryman et a!., deer totally lack electrophoretically-detectable 1977; Gyllensten eta!., 1983), although there is as genetic variation. The survey involved a sample of yet no firm evidence for this suggestion. loci, buffer systems, sites and individual deer. At Certain (notably LDH, MDH, 6- each level a different or bigger sample might have PGD, GOT and CA) tended to produce sub-bands led to the discovery of polymorphism. Neverthe- after storage for several months. In the case of less, given the sample sizes employed in the present LDH, treatment of the samples with dithiothreitol study (see Materials and Methods) and assuming removed the sub-bands indicating that they were our electrophoresis was of equivalent resolving due to the formation of sulphydryl-glutathione power to that of other workers in the field (in bonds during storage (Harris and Hopkinson, support of which we point to the polymorphisms 1976). Storage of haemolysates produced met- found in red and muntjac deer) it appears likely haemoglobin bands which could be distinguished that British fallow deer really do have a lower level from the true haemoglobin bands by their brown of genetic variation than other deer species studied colour. Blood samples arriving by post which had to date. haemolysed in transit sometimes showed stepwise We know of no convincing selectionist theory changes in transferrin band mobility giving an predicting a low level of genetic variation in the overall pattern like that which might be expected fallow deer compared with other deer species. The for a transferrin polymorphism. Experiments "environmental grain" hypothesis of Selander and 204 J. M. PEMBERTON AND R. H. SMITH

Kaufman (1973), which predicts low levels of vari- 10,000 to 5000 years before the present) distributed ation in large, highly mobile species and vice versa throughout Europe. Although red deer and roe has attracted some interest in the literature (e.g., deer ( capreolus) are the first and fourth Cameron and Vyse, 1978) but was not supported most widely represented species respectively, there by a recent interspecific comparison of large graz- are no definite reports of fallow deer, suggesting ing mammals (Baccus et aL, 1983). Presumably the the species was scarce or absent at that time. The environmental grain hypothesis would predict a oldest post glacial finds of European fallow deer higher level of variation in fallow deer than in are at early Neolithic sites (5000 to 4000 years n.e.) moose, red deer and wapiti, which is not borne in and Bulgaria (Chapman and Chapman, out by our findings. We are therefore forced to the 1975, p. 44). Subsequent evidence of the presence conclusion that the lack of variation found in the of fallow deer comes from Hittite, Greek and present study reflects a genetic bottleneck in the Roman artefacts (Zeuner, 1963, p. 430; Chapman history of British fallow deer. Such a bottleneck and Chapman, 1975, p. 46) and these cultures might have occurred at a number of points in appear to have fostered the increase and spread history. of the species. Indeed, it seems likely that the First, a bottleneck might have occurred when entire distribution of European fallow deer outside the fallow deer was introduced to Britain. the South Eastern corner of Europe is due to Palaeontological evidence suggests that the species introductions by man (Chapman and Chapman, died out in Britain during the last glaciation 1980). (Chapman and Chapman, 1975, p. 45). It is pos- In the history outlined, there is no obvious date, sible that the introduced animals were few in num- from the time man started to transport and intro- ber and were forced to inbreed for several gener- duce fallow deer onwards, when a genetic bottle- ations, losing genetic variation in the process neck affecting the entire descendent population (though this is by no means inevitable, cf. the might have occurred. Two main possibilities there- Reeve's muntjac, another species introduced to fore exist. First, perhaps a natural catastrophe such Britain). A problem with this theory is that there as the last glaciation, which left only a popu- are several documented introductions of fallow lation of European fallow deer surviving in S.E. deer to Britain since Norman times, when the main Europe for the interval 10,000 to 5000 years n.y., introduction was probably made (Chapman and was the direct cause of the bottleneck. Alterna- Chapman, 1975, p. 49). For example, introductions tively, perhaps the most serious loss of genetic were made in 1612 from , in 1661 from variation took place during enforced inbreeding (Shirley, 1867) and in the 19th Century when man first took the fallow deer into captivity, from Denmark (Whitehead, 1950, p. 153). If con- which was presumably sometime in the interval tinental European fallow deer have a higher level 10,000 to 3000 years B.P. of electrophoretically detectable polymorphism it History does not relate which of these theories is surprising that polymorphism is not found in is more likely, but a feature of modern fallow deer the British population as a result of introductions. may give a clue. European fallow deer have a In this context it is interesting to note that a recent widespread, genetically-controlled coat colour survey of 13 loci in a sample of 35 German fallow polymorphism, individuals ranging from all-white, deer failed to reveal intraspecific polymorphism through various spotted types, to all-black. It is (H.G. Scheil, personal communication). A more difficult to understand how, in a bottleneck caused extensive study of continental European fallow by the glaciation, coat colour variation could have deer is clearly desirable. been retained while electrophoretically-detectable Alternatively, a genetic bottleneck might have variation was lost. On the other hand, coat colour occurred before the introduction of the fallow deer variation is a notable characteristic of domestic to Britain. Under this hypothesis, mainland animals (including the most highly domesticated European fallow deer would also have a low level deer species, the reindeer) and is believed to have of electrophoretically-detectable polymorphism. been selected by man early in the The idea calls for an examination of the species' process (Zeuner, 1963). Although there is no infor- earlier history. mation on the origin of the colour varieties of It seems that during the last glaciation the fallow deer, they are generally regarded as European fallow deer went extinct not only in selected (Chapman and Chapman, 1975, p. 73). It Britain, but also over much of Europe (Lister, is possible that the coat colour varieties were 1984). Jarman (1972) reviews data on mammalian expressed as a result of inbreeding during the remains at 165 Mesolithic sites (i.e., dating from initial domestication of fallow deer and were LACK OF POLYMORPHISM 205 retained by man, while invisible variation (detect- some cases, it seems that the Northern elephant able now by electrophoresis) was lost. seal Mirounga angustirostris (Bonnell and The idea of a genetic bottleneck at least 3000 Selander, 1974), the Atlantic Odobenus ros- years ago often provokes suggestions that novel manus rosmanus (Simonson et a!., 1982), the red mutation would since have replaced lost variation. vulpes (Simonson, 1982), the beech Calculation of how many mutations would be Martes foina (Simonson, 1982), the polar expected by now is hampered by lack of informa- Thalarctos maritumus (Allendorf et a!., 1979; tion, especially concerning the neutrality or other- Larsen et a!., 1983) and the (O'Brien et wise of mutants and historical population size. a!., 1983) all show exceptionally low levels of vari- However, if it can be assumed that fallow deer ation as revealed by electrophoresis. Speculating selection coefficients are comparable with those of on the cause of this lack of polymorphism, it is other deer species, one approach is to examine the noticeable that excepting the fallow deer all the rate at which electrophoretically-detectable alleles species with little detectable variation are car- arise and persist in other species of deer. Elec- nivores. Baccus et aL (1983) suggested that "car- trophoresis studies now exist which compare old nivorous species might be expected to have lower and new world forms of moose (Reuterwall, 1980), heterozygosities due to smaller average population red deer (Baccus eta!., 1983; Dratch and Gyllen- size caused by their position in the trophic pyramid sten, in press) and reindeer (Baccus et a!., 1983) of numbers or the social structure of their popula- for which the last possible genetic contact (barring tions," but immediately question the theory recent introductions) was roughly 10,000 years B.P., because the lupus ( et aL, 1976), at the end of the glaciation. The data from these the Canis latrans (Fisher et a!., 1976) and studies suggest that at a single locus, a detectable the Macquarie Island Mirounga new mutation becomes established once in every leonina (McDermid et a!., 1972) all have relatively 18,000 to 72,000 years. So, in a sample of 30 loci high average heterozygosities. The theory, of between one and five mutations would be expected Baccus et aL, is certainly unsatisfactory if one to appear and persist in a 3000 year interval (details imagines that it is the mean population size of a of the calculation are given in Pemberton, 1983). species over a stretch of time per se which deter- Low as these rough estimates of detectable new mines the amount of genetic drift and hence affects mutations are, they should be reduced still further the level of variation. However, in fact it is down- when the population size of fallow deer over the ward fluctuations in population size which cause last few thousand years (affecting the absolute the greatest loss of genetic variation. Therefore, mutation rate) is taken into account. What low levels of variation may be expected in those evidence there is (Jarman, 1972, see above) sug- species which maintain low population sizes and gests a far larger red deer than fallow deer popula- tend to fluctuate. Higher levels of variation are tion in Neolithic Europe. Present day fallow deer expected either where average population size is population estimates are frequently no more than high or where fluctuations are rare. guesses, but the figures are an order of magnitude Finally, we consider the possible consequences smaller than those for red deer, moose and rein- of a low level of variation for the fallow deer. First, deer. Toth (1984), reviewing available estimates, the finding lends support to the idea that British puts the fallow deer population of the world fallow deer experience low levels of inbreeding excluding Britain at 164,000. For Britain, Gibbs et depression (Smith, 1979) since it suggests that com- a!. (1975) guess at 50,000 wild fallow deer. Even paratively few recessive deleterious alleles would allowing for enclosed fallow deer in Britain the be expressed on inbreeding. Second, if one accepts world population estimate for the species would that variation at loci detectable by electrophoresis hardly equal the 255,000 red deer living in (or at linked loci) is not selectively neutral, various alone (Red Deer Commission, 1980). Such con- predictions follow. In the context of deer farming, siderations suggest that the number of detectable heritabilities of quantitative characters will be mutations arising at 30 loci since the proposed lower than in more polymorphic (as revealed by fallow deer bottleneck could indeed be negligible. electrophoresis) species and Although we now know that it is wrong to correspondingly less successful. Within-herd vari- generalise that all species of large have ance of production characters such as live weight low levels of variation, it does appear that a rela- is lower in fallow deer than in red deer on New tively high proportion of large mammals have little Zealand deer farms, supporting this prediction (G. detectable polymorphism. Although additional Asher, personal communication). In the wild, sampling of populations would be desirable in fallow deer will not adapt to altered environmental 206 J. M. PEMBERTON Al'lD R. H. SMITH conditions as successfully as other more COTHRAN, F. (C, ('I-lESSER, R. K., SMFIH, M. H. AND JOHNS, polymorphic species. Here we point to the low 1983. Influence of genetic variability and maternal factors on fetal growth in white-tailed deer. , estimated world population for fallow deer (dis- .37, 282-291. cussed above), the lower rate of spread of intro- OF LORENZO, R. J. ANT) RUDOLF, I-. H. 1970. Glutamate oxalate duced fallow deer compared with red deer in New transanlinase (GOT) genetics in Mus musculus:linkage, Zealand (Caughley, 1963; Chapman and Chap- polymorphism and phenotypes of the GOT.2 and GOT-I man, 1980) and the perhaps rather subjective com- loci. Biochem. ., 4, 259-273. DRATCH, P. ANI) GYI.I.,ITNSTEN, U. In press. Genetic differenti- ment that in Britain the fallow deer has nowhere ation of red deer and North American (wapiti): acheved the pest status of red or . evidence for subspecific status. In Fennessy, P. and Drew, K. (eds.) The Biology of Deer Production. Acknowledgements 1. Pemberton acknowledges support by the FISHER, R. A., PUTT, W. AND HACKEL, F. 1976. An investigation Science and Engineering Research Council and the Eorestry of the products of 53 gene loci in three species of wild Commission under the CASE. scheme. More than 50 people : Canis lupus, (anis latrans and Canisfamiliaris. were involved in collecting samples, and we thank them all. 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