J . Zool., Lond. (1974) 174,245-254

Reproductive compatibility of voles from separate continents (Mammalia : Clefhrionomys)

P. R. GRANT Biology Department, McGill University, Montreal, P . Q., Canada

(Accepted 12 March 1974)

(With 1 figure in the text)

The North American Red-backed vole, CIethrionomys gapperi, and the Eurasian Bank vole, C. glureolus, are probably derived from a common ancestor. They have been isolated from each other for a minimum of 20,000 generations, probably many more. Interbreeding experiments in the laboratory show that in that time only partial reproductive isolation has developed. They interbreed as frequently as do pure strain pairs, and produce litters of approximately the same size. Hybrids exhibit reduced viability, but this may be partly an artifact produced by the laboratory rearing conditions. If they ever made contact in nature the most likely outcome appears to be selection against hybrids leading to full speciation and the establishment of contiguous allopatry. It is recommended that they be considered semispecies, in the terminology of Mayr (1963), and retain their separate names.

Contents

Introduction. . . . . . . . Methods . . . . . . . . Results . . . . . . . . Comparison with Godfrey’s results Conclusions . . . . . . . . Discussion . . . . . . . .

Evolutionary divergence . . Taxonomy . . . . . .

Summary . . . . . . . . References . . . . . . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

Page . . . . . . . . . . 245 . . . . . . . . . . 246 . . . . . . . . . . 247 . . . . .. . . . . 249 . . . . . . . . . . 250 . . . . . . . . . . 250 . . . . .. . . .. 250 .. . . . . . . . . 251 .. . . . . . . . . 252 . . . . . . . . . . 253

Introduction It is difficult to know if morphologically different and geographically isolated popula-

tions of animals deserve subspecific or specific rankings, since the crucial test of inter- breeding (Mayr, 1963) is not performed in nature. Breeding experiments can help resolve the matter by revealing how much reproductive compatibility, if any, exists. Extrapolations are then made on the basis of its converse, reproductive incompatibility (isolation), making due allowance wherever possible for the lack of correspondence between nature and the experimental situation.

A well investigated example is provided by the Eurasian Bank vole, Clethrionomys glareolus (Schreber). Four island populations are morphologically different enough from the population on mainland Britain and from each other to have convinced early taxono- mists of their individual and separate species status (see Corbet, 1964). However, Steven (1953, 1955) and later Godfrey (1957, 1958) demonstrated that all five populations are

245

246 P . R . G R A N T

interfertile in the laboratory, and that the offspring of all possible crosses are fertile too. (A parallel demonstration with mainland and island forms of the mouse Apodemus sylvaticus was made by Jewel1 & Fullagar (1965).) British and European mainland C. glareolus have also produced hybrids in the laboratory (Rauschert, 1963). These studies show that the populations in allopatry have not developed reproductive isolation, whereas C. glareolus produce sterile male hybrids when crossed with C. rutilus and C. frater (Rauschert, 1963 ; Spannhof, 1960), and are therefore obviously specifically distinct from them.

On the other hand Fl and F, British vole hybrids were less viable than pure race off- spring (Godfrey, 1958). This fact together with race specific discriminatory behaviour exhibited in a reproductive context and tending to positive assortative mating led Godfrey to suggest that if the populations ever established contact in nature, natural selection would act against the hybrids, and the process of speciation would continue beyond its present incipient stage to completion. Another possible outcome of this hypothetical contact is ecological segregation into different habitats, with a limited degree of inter- breeding at or close to habitat boundaries (e.g. see Harris, 1954; Ingles & Biglione, 1952). This hypothesis is plausible since the island and mainland populations already occupy different habitats to some extent (Corbet, 1964; Steven, 1953), but is uncertain because Microtus agrestis might competitively exclude C. glareolus from grassland (Grant, 1972). Nevertheless, in either case we might follow Mayr (1963) and regard C. glureolus as a superspecies comprising mainland and island semispecies ; populations with some of the characteristics of separate species and with some of the characteristics of subspecies. McCarley (1954a, 6, 1963, 1964) has described a situation in Texas with Peromyscus leucopus and P. gossypinus which has these ingredients, and populations of Dicrostonyx torquatus (Rausch & Rausch, 1972) and Sorex vugrans (Findley, 1955; but see Hoffmann, 1971) provide other possible examples.

If island and mainland populations of this vole are not reproductively isolated, are populations on separate continents ? Taxonomists consider the North American Red- backed vole, Clethrionomys gapperi (Vigors) to be specifically distinct from the related and morphologically similar C. glareolus. This distinction is supported by the discovery of biochemical differences (Johnson, 1968), but recently it has been questioned (Southern, 1964), partly because they are now known to have the same chromosome number (Matthey, 1956). The opportunity arose to examine their potential for inter- breeding in the laboratory, and thus of extending the work of Steven (1953, 1955) and Godfrey (1957, 1958), following some experiments on habitat selection and competition (Grant, 1970a). This paper presents a reassessment of the evolutionary divergence of these voles in the light of results of breeding experiments reported herein, and results of a comparative study of their reproductive behaviour (Herzog, 1972).

Methods A laboratory colony of Clethrionomys was established with three groups of newly caught

animals; C. gapperi from Quebec, and C. glareolus from England (Arnside), and the Welsh Island of Skomer (see Grant, 1970a for further details). Breeding pairs were kept in stainless steel wide-meshed cages, measuring 60 x 25 x 22 cm, which were designed for both the breeding of animals and for making observations on their behaviour. Each cage contained sawdust on the floor, a cardboard nest box with cotton for nesting material, a water bottle, sunflower seeds,

REPRODUCTIVE COMPATIBILITY OF VOLES 247

apple and chunks of mouse food pellets supplied ad lib. Temperature was constant at 68"-70"F, and the daily cycle of artificial light and dark matched the natural local (Montreal) photoperiod.

The breeding programme extended from September 1966 to January 1971. Breeding occurred in all months of the year but mainly in the period April to November. Single race and mixed pairs, mostly Quebec with Arnside animals, were maintained for 1-12 months before being changed. Cages were checked every other day. Litters were not disturbed until the young were observed outside the nest box, although some nests were carefully scrutinized if births or deaths were suspected. Animals were weighed at irregular intervals after a minimum age of 3 weeks. Adult males were not removed after a pregnancy or parturition. Young were removed and paired within 2 weeks of weaning.

Results Table I gives the results of the breeding programme. Nine pairings of Quebec and

Arnside animals were made, and four produced litters, one of them twice. The ratio of number of litters to number of pairings (0.56) is approximately the same as for single race

TABLE I Breeding results

Skomer/ Skomer

Amside/ Quebec/ Arnside Quebec

Quebec/ Arnside

No. pairings (P) No. litters (L) LIP No. litter sizes

1 2 3 4 5 6 .?

life at weaning, in months (ex)

Expectation of

19 15 0.79

1 3 2 6 3 0 3.5

19.3

29 21 14 1 1 0.48 0.52

0 0 2 1 3 1 7 5 1 4 1 0 3.7 4.1

24.9 6.9

9 5 0.56

1 0 1 2 0 1 3.6

8.7

pairs, although Skomer pairs produced proportionally more litters. Both Quebec and Arnside females produced hybrid litters and exhibited no obvious differences in behaviour in rearing them. The mean number of young per litter does not vary much among the four groups, and the differences are not statistically significant. The absence of any meaningful difference is further indicated by the fact that the modal number of young per litter is the same (four) for all four groups.

Survivorships of Skomer, Quebec, Arnside and hybrid offspring are shown in Fig. 1 ; the sizes of the four groups are 52, 45, 52 and 18 respectively. It can be seen that survival is highest among Arnside animals and lowest among hybrids. Hybrids differ from Quebec animals principally in the first nine months of life, and most conspicuously in the first month. However, after weaning hybrids had a higher expectation of further life than the Quebec animals (Table I); the difference is not statistically significant, but both had a

248 P. R. GRANT

significantly lower expectation of further life at weaning than the Arnside and Skomer animals (P<O.Ol). High mortality in the nest in each group was associated with agitated behaviour of the mother. Dead young were most frequently found bitten on the head, in or just out of the nest, at weights of 2-6 g (i.e. in their first week of life). Hybrids reared by Quebec and by Arnside females did not differ in survival.

Those hybrids which survived beyond the first month showed a progression in body weight in their first few months no different from Quebec and Arnside offspring. Initially they were paired in error with Arnside offspring. Later the error was corrected, but two short attempts to produce an F, generation from them were unsuccessful.

The hybrid-Arnside pairings yielded one litter of four young, which may be designated QAAA according to the relative contribution of Quebec and Arnside genetic Subsequently litter mates were paired and these produced two litters of two

material. and four

Months FIG. 1 . Survivorship curves of English (A) , Welsh (S), North American (Q) and hybrid ( Q / A ) voles in the

laboratory.

young respectively (also QAAA). A further five litters were produced from other crosses; the constitution of these offspring according to the same scheme, was QAA and QAAA. The mean number of young per litter from the total of eight litters was 3-75, close to the value realized by Arnside animals. The modal value was, once again, four. No sexual differences were noted in the viability and fertility of the hybrids.

The six Q A hybrids which survived long enough to develop an adult pelage, could be assigned without difficulty, to one parental phenotype or the other on the basis of dorsal pelage colour-brick-red, characteristic of Quebec animals (three), or a more orange-red, characteristic of Arnside animals (three). Offspring designated Q A A (five) or Q A A A (35) were all of the Arnside phenotype.

Behavioural and physiological correlates were observed as well. Q A hybrids with the brick-red phenotype exhibited the rapid and erratic escape behaviour characteristic of Quebec animals, either wild-caught or laboratory-reared, while those with the orange-red phenotype were, like Arnside animals, relatively more calm in the presence of an observer. In this respect QAA and QAAA behaved like Arnside animals. No attempt was made to subject this to a systematic test, but the difference was obvious to the eye of an experienced

REPRODUCTIVE COMPATIBILITY O F VOLES 249

observer. The physiological correlate was the deposition of extensive subcutaneous fat- In the summer of 1967 the first Arnside and Skomer animals started putting on fat, perhaps in response to a daylength which for them at that time of year was unnaturally short, and by early winter almost all wild-caught and laboratory-reared animals had done the same. All Q A with the Arnside phenotype, and QAA and QAAA animals, did so as well. None of the Quebec animals, nor any of the QA hybrids, with the Quebec pelage did

At the end of the programme Quebec and Skomer animals were paired. One litter was produced but did not survive to weaning. For a variety of reasons this result is not strictly comparable with the results of Quebec-Arnside pairings. However, the low ratio of litters produced to number of pairings (0.2) raises the possibility of greater reproductive incompatibility between Quebec and Skomer than between Quebec and Arnside animals.

Comparison with Godfrey’s results In Godfrey’s (1957, 1958) studies of British island and mainland populations of C.

glareolus mean litter size was 3.3 (N=159) for pure races combined, 4.1 (N=60) for hybrids. Weaning success was higher for hybrids (84 %) than for pure strains (69 %), but life expectancy at weaning was only six months for hybrids and eight months for pure races. Mortality was even heavier among Fz animals.

In the present experiments hybrids did not have larger litters or higher survival to weaning than pure race animals, but their life expectancy at weaning was superior to one parental type (Quebec). The net result in both studies was reduced viability among hybrids.

Maximum longevity of British mainland animals and hybrids was approximately the same in the two studies, 37 and 15 months respectively in the present study, 40 and 16 months in Godfrey’s. However the pattern of survival was quite different. Thus in Godfrey’s study 50 % mortality among British mainland animals had occurred in the first seven months, but not until the 20th in mine. This difference is perhaps attributable to the more crowded conditions in Godfrey’s experiments than in mine. In both studies survival was artificially high, since few animals live more than a few months in the wild (Chitty & Phipps, 1966; Newson, 1963; Smyth, 1968; unpublished data for Quebec).

The results with C. glareolus of both Godfrey’s study and mine are similar to those of the most extensive study to date, that of Buchalczyk (1970). In a study of 782 litters born in the laboratory the mean number of young per litter was 3.6 (cf. Table I), 15 % of young died in the first two weeks and the maximum longevity was around four years.

In summary the results of Godfrey’s study and mine are largely similar, the conspicuous differences being (a) an Fz generation (exhibiting low viability) was produced by Godfrey’s study but not in the present one, (b) hybrids suffered heavier mortality in the nest in the present study than in Godfrey’s study.

The failure to produce an F2 generation in the present study is perhaps due to the minimal opportunity of breeding afforded the Fl’s, rather than any incompatibility. It is unfortunate that it was not possible to pair the F1’s for long enough to resolve this important point.

It is possible that the high nestling mortality of hybrids in the present study is due to unusual parental behaviour. Quebec animals were more agitated and nervous than either Arnside or Skomer animals, more prone to respond adversely to disturbances in the laboratory, and hence more likely to neglect the offspring or exhibit aberrant behaviour

so.

250 P. R . G R A N T

towards them. In fact many hybrid and Quebec young were killed by a parent. This parental influence on litter viability might be magnified by parental dissimilarity; the presence of an unlike parent may have increased the agitation of the Quebec parent. The effect on the young would not be expected to end necessarily at weaning if the normal physiological and psychological development of the young had been adversely affected up to this time. It could therefore account for the difference in viability between Quebec and Arnside.

Temperamentally Skomer and Quebec animals are the most different, Skomer animals being tame, easy to handle and exhibiting much less fright reaction than either British mainland or Quebec animals (Godfrey, 1957, 1958; Herzog, 1972). Skomer and Quebec animals produced only one hybrid litter, which failed to survive to weaning. This is consistent with the above hypothesis. It is interesting to note that the greatest juvenile hybrid death in Godfrey’s study occurred when the mother was a Skomer animal. This strengthens the view that the reciprocal behaviour of young and parent is an important contributor to the viability of the young.

I f the foregoing explanation is correct, mortality of nestlings may be unnaturally high in the laboratory. In nature the male would not be confined to within 60 cm of the female, the female would be less stressed from this source and better able to rear young to in- dependence. Therefore the low viability of hybrids compared with pure race animals in the present study, and compared with both hybrids and pure race animals in Godfrey’s study, may be a misleading product of the artificial rearing conditions in the laboratory to which Quebec animals respond poorly.

Conclusions The experiments demonstrate that C. glareolus and C. gapperi are capable of inter-

breeding, and producing fertile offspring. They interbreed as frequently as do pure race pairs, and produce litters of approximately the same size. Hybrid offspring exhibit reduced viability, but this may be something of an artifact produced by the laboratory rearing conditions.

Using the same stocks, Herzog (1972) made a detailed, comparative study of the reproductive behaviour of pure race pairs in relation to the oestrus cycle of the female. Differences were found among all three groups, and were as large between Arnside and Skomer pairs as between either and Quebec pairs.

Therefore full reproductive isolation has not developed in geographical isolation. This parallels the findings of Godfrey with mainland and island populations of C. glareolus, and necessitates a discussion of the evolutionary divergence and taxonomy of C. glareolus and C. gapperi.

Discussion Evolutionary divergence

The segregation of pelage colour phenotypes among the Q A hybrids suggests a simple Mendelian inheritance. Steven (1953) came to a similar conclusion with regard to the inheritance of‘ the distinctive pelage of Skomer animals, and it may be inferred from the hybrids of C. glareolus and C. frater (Zimmermann, 1965). Quantitative traits, such as some of the behavioural characteristics expressed in reproduction, are likely to have a more complex inheritance (Falconer, 1960). But when the likely duration of genetic

REPRODUCTIVE COMPATIBILITY OF VOLES 25 1

isolation of North American and European populations is taken into account, the sur- prising thing is that relatively little divergence between the Eurasian and North American populations has occurred. Moreover Quebec and British populations are at opposite ends of a longitudinal chain, which once extended across a Bering land bridge for an unknown distance either side of it, but is now broken by sea and by the presence of unsuitable habitat occupied by C. rutilus in its vicinity. If difference is a correlate of distance, they should be expected to be the most different pair of populations, despite reproductive compatibility of at least two neighbouring links in the chain (Rauschert, 1963; see also Zimmermann, 1965).

How long have the populations been isolated ? Cfethrionomys may have weak powers of dispersal across water barriers (Grant, 1970b), so the separation of the continental populations probably coincided with or preceded the last Bering Strait incursion. Accord- ing to Hopkins (1967: 465) this occurred 10,000 years ago. To convert to generations, and assuming a minimum of two generations per year (Peterson, 1966; Southern 1964), this figure should be at least doubled, possibly trebled (cf. Southern, 1964). Therefore, the populations were derived from a single ancestral population about 20,000 generations ago. This is a conservative estimate. The land bridge at the time of the incursion was covered by tundra or steppe vegetation (Colinveaux, 1967), more suitable to C. rutilus than C. gfareolus which almost certainly inhabited it much earlier during a warmer period.

Compare this with British mainland and island populations. If Corbet’s (1961) sup- position is correct, voles colonized the islands as a result of an assisted passage with Man in late Iron Age times (c . 2000 B.P.: Jewell, 1965). The Skomer population and possibly the other island populations, has the demographic features of low production, low mor- tality, delayed maturity and elevated longevity (Fullagar, Jewell et al., 1963 ; Jewell, 1966) characteristic of small island populations and which in combination determine the pro- duction of a single generation only per year. Thus, if the assumptions are correct, the Skomer population isolated from the British mainland population for 2000 generations has diverged to a roughly similar extent as has the North American population isolated for at least ten times as long. It appears that evolution has been conservative on continents, less so on islands.

Part of the reason for this difference may lie in the ecologies of the populations. Fami- liarity with the ecological characteristics of British and Quebec populations impresses me with their similarity. They occupy similar habitats, have similar diets, similar activity patterns and similar predators (references in Grant, 1970b). Natural selection on the two populations is therefore likely to be similar. In contrast, island populations off Britain occupy different habitats and, on Skomer at least, diet, activity patterns and predators are different too (Buxton & Lockley, 1950; Fullager, Jewell et al., 1963; Herzog, 1972; Corbet, 1964). This contrast is sufficient to justify invoking different selection pressures, and a different rate of evolution. In other words short time and large environ- mental difference has been approximately equivalent to long time and small environmental difference in producing selective responses in Clethrionomys. In addition the island populations may have been subjected to the founder effect, and possibly random drift.

Taxonomy Godfrey (1958) attempted to answer the question of what would happen if the island

and mainland populations established contact in nature. It is worth asking the same

252 P. R. G R A N T

question of North American and European populations, for the answer influences the taxonomic treatment of morphologically similar but allopatric populations. Four possible outcomes can be suggested : (1) ecological character displacement, eventually permitting coexistence ; (2) Competitive replacement (exclusion) of one by the other; (3) the establish- ment of contiguous geographical ranges; (4) interbreeding, extensive genic introgression and population fusion. Reproductive character displacement might be expected to occur in the first three situations.

The first possible outcome can be ruled out on the grounds that their ecologies are too similar for natural selection to cause the necessary minimum degree of divergence that would permit coexistence. The last possible outcome can be set aside by a more indirect argument. Mate preference of North American and European voles is not known, but if mainland and island populations of European voles exhibit a mating preference for same-race animals (Godfrey, 1958 ; Rauschert, 1963), North American and European animals would probably discriminate similarly in each other’s presence in nature. Positive assortative mating and selection against hybrids, as indicated by viabilities in the labora- tory, would lead to full speciation. This eliminates the fourth outcome, and there remain outcomes (2) and (3). It is unlikely that one population is competitively superior to the other throughout the other’s range, and able to replace it completely. Therefore, whether partial or no competitive replacement occurs, the most likely ultimate outcome is the third, reproductive isolation and the establishment of contiguous allopatry (parapatry). In such cases the two populations should be considered semispecies, in Mayr’s (1963) terminology, comprising a single superspecies.

According to current practice semispecies are given different names in a binomial nomenclature to emphasize their affinity with full species. I therefore recommend retention of the names C. glareolus and C. gapperi for the Eurasian and North American populations respectively.

If the island and mainland British voles have reached an approximately similar stage along the path towards the development of full reproductive isolation, perhaps they should also be viewed as semispecies and given specific names in recognition of that view.

Summary The North American Red-backed vole, Clethrionomys gapperi and the Eurasian Bank

vole, C. glareolus, are probably derived from a common ancestor. They have been isolated from each other for a minimum of 20,000 generations, probably many more. Interbreeding experiments in the laboratory show that in that time only partial reproductive isolation has developed. They interbreed as frequently as do pure race pairs, and produce litters of approximately the same size. Hybrids exhibit reduced viability, but this may be partly an artifact produced by the laboratory rearing conditions. If they ever made contact in nature, the most likely outcome appears to be selection against hybrids leading to full speciation, and the establishment of contiguous allopatry. It is recommended that they be considered semispecies, in the terminology of Mayr (1963), and retain their separate names.

The West Wales Naturalists’ Trust and Mr David Saunders made it possible for me to secure the Skomer animals, and I am grateful for their help. I thank W. 0. Pruitt, Jr, H. N. Southern,

REPRODUCTIVE COMPATIBILITY O F VOLES 253

D. M. Steven and K. Sittmann for their valuable comments on the manuscript, and M. Hughes and R. Shoofey for technical assistance. The study was supported by research grant A2920 (N.R.C. Canada) and by a grant from McGill University.

R E F E R E N C E S Buchalczyk, A. (1970). Reproduction, mortality and longevity of the Bank vole under laboratory conditions.

Buxton, J. & Lockley, R. M. (1950). Island of Skomer. London & New York: Staples Press. Chitty, D. H. & Phipps, E. (1966). Seasonal changes in survival in mixed populations of two species of vole. J.

Colinveaux, P. A. (1967). Quaternary vegetational history of arctic Alaska. In The Bering Land Bridge: 207-231.

Corbet, G . B. (1961). Origin of the British insular races of small mammals and of the “Lusitanian” fauna. Nature,

Corbet, G. B. (1964). Regional variation in the Bank vole, Clethrionomysglareolus, in the British Isles. Proc. zool.

Falconer, D. S. (1960). Introduction to quantitative genetics. Edinburgh & London: 0l;ver & Boyd. Findley, J. S. (1955). Speciation of the wandering shrew. Univ. Kans. Publs Mus. nut. Hist. 9: 1-68. Fullagar, P. J., Jewell, P. A,, Lockley, R. M. & Rowlands, I. W. (1963). The Skomer vole (Clethrionomysglareolus

skomerensis) and Longtailed field mouse (Apodemus sylvaticus) on Skomer Island, Pembrokeshire in 1960. Proc. zool. SOC. Lond. 140: 295-314.

Godfrey, J. (1957). Behaviour differences between races of Bank Voles (genus Clethrionomys Tilesius). Unpubl. Ph. D. thesis, Univ. Edinburgh.

Godfrey, J. (1958). The origin of sexual isolation between bank voles. Proc. R. phys. SOC. Edinb. 27: 47-55. Grant, P. R. (1970~). Experimental studies of competitive interaction in a two-species system. 11. The behaviour

Grant, P. R. (1970b). Colonization of islands by ecologically dissimilar species of mammals. Can. J. 2001. 48:

Grant, P. R. (1972). Interspecific competition among rodents. A. Rev. Ecol. Syst. 3: 79-106. Harris, van T. (1954). Experimental evidence of reproductive isolation between two subspecies of Peromyscus

Herzog, A. G. (1972). The variation and regulation of Clethrionomys mating behavior. Unpubl. M.Sc. thesis,

Hoffmann, R. S. (1971). Relationships of certain Holarctic shrews, genus Sorex. Z. Saugetierk. 36: 193-200. Hopkins, D. M. (Ed.) (1967). The Bering Land Bri&e. Stanford: Stanford Univ. Press. Ingles, L. G . & Biglione, N. J. (1952). The contiguity of the ranges of two species of pocket gophers. Evolution,

Jewell, P. A. (1965). New research on the vole and field mouse of Skomer Island. Nature in Wales 9: 1-8. Jewell, P. A. (1966). Breeding season and recruitment in some British mammals confined on small islands. Symp.

zool. SOC. Lond. No. 15: 89-116. Jewell, P. A. & Fullagar, P. J. (1965). Fertility among races of the field mouse (Apodemus sylvaticus (L.)) and their

failure to form hybrids with the yellow-necked mouse (A. flavicollis Melchior). Evolution, Lancaster, Pa.

Johnson, M. L. (1968). Application of blood protein electrophoretic studies to problems in mammalian taxo-

Matthey, R. (1956). Cytologie chromosomique compark et systematique des Muridae. Mammalia 20: 93-123. Mayr, E. (1963). Animal species and evolution. Cambridge, Mass: Belknap Press. McCarley, W. H. (1954~). Natural hybridization in the Peromyscus leucopus species group of mice. Evolution,

McCarley, W. H. (19546). The ecological distribution of the Peromyscus leucopus species group in eastern Texas.

McCarley, W. H. (1963). Distributional relationships of sympatric populations of Peromyscus leucopus and P.

Acta theriol. 15: 153-178.

Anim. Ecol. 35: 313-331.

Hopkins, D. M. (Ed.). Stanford: Stanford Univ. Press.

LO&. 191: 1037-1040.

SOC. Lond. 143: 191-219.

of Microtus, Peromyscus and Clethrionomys species. Anim. Behav. 18: 41 1426 .

545-553.

maniculatus. Contr. Lab. vert. Biol. Univ. Mich. 70: 1-13.

McGill University.

Lancaster, Pa. 6: 204207.

19: 175-181.

nomy. Syst. Zool. 17: 23-30.

Lancaster, Pa. 8: 314-323.

Ecology 35: 375-379.

gossypinus. Ecology 44: 784-788.

254 P . R . G R A N T

McCarley, W. H. (1 964). Ethological isolation in the cenospecies Peromyscus leucopus. Evolution, Lancaster, Pa.

Newson, R. M . (1 963). Differences in numbers, reproduction and survival between two neighbouring populations

Peterson, R. L. (1966). The mammals of eastern Canada. Toronto: Oxford Univ. Press. Rausch, R. L. & Rausch, V. R. (1972). Observations on chromosomes of Dicrostonyx torquatus stevensoni Nelson

Rauschert, K. (1963). Sexuelle affinitat zwischen arten und unterarten von Rotelmausen (Clethrionomys). Biol. Zbl.

Srnyth, M. (1968). The effects of removal of individuals from a population of bank voles Clethrionomysglareolus.

Southern, H. N. (Ed.) (1964). The handbook ofBritish Mammals. Oxford: Blackwell. Spannhof, L, (1960). Histochemische Untersuchungen zur Sterilitat bei mannlichen Saugerbastarden (Artkreuzung

Steven, D . M. (1953). Recent evolution in the genus Clethrionomys. Symp. Soc. exp. Biol. 7 : 310-319. Steven, D . M. (1955). Untersuchungen iiber die britischen Formen von Clethrionomys. 2. Saugerierk. 20: 70-74. Zimmermann, K. (1965). Art-Hybriden bei Rotelmausen. Z . Saugetierk. 30: 3 15-320.

18: 331-332.

of bank voles (Clethrionomys glareolus). Ecology 44: 110-120.

and chromosomal diversity in varying lemmings. 2. Saugetierk. 37: 372-384.

82: 653-664.

J . Anim. Ecol. 37: 167-183.

der Rotelmause Clethrionomys glareolus 2’ C. rutilus). Zool. Anz. Suppl. 23: 99-107.

NOTE: This paper is dedicated to Professor David Steven, recently deceased, who was the first to conduct this type of study with Clethrionomys and who gave encouragement and advice in the present one.