Chromosomal evolution in Nearctic collared lemmings
The ultimate aim is to compare the geographical pattern of mtDNA variation and the distribution of chromosome races in the collared lemming to draw inferences concerning the origin of chromosome races.
Scientific background
The present investigation is a logical follow up to our studies initiated in 1994 which genetic diversity investigated in lemming populations along the Russian Arctic coast (Fedorov et al. 1999, Fredga et al. 1999). From a chromosomal point of view, collared lemmings are of particular interest due to their great chromosome diversity. Chromosomal variation occurs through centric fusions of acrocentric chromosomes and by variation in the number and type of supernumerary (B) chromosomes. In addition, species of the genus Dicrostonyx, but not Lemmus, have an exceptional mechanism for sex determination (for review see Fredga 1994). Fertile females with XY sex chromosomes occur together with XX females. Males have the normal XY sex chromosome constitution. In populations with XY females an excess of females is expected ( theoretically 7F:4M).
Field-work
Our intention was to collect as many lemmings as possible from the maximum possible number of sites. Therefore we joined theme A and the Red Camp for the fieldwork. As a rule 600 snap traps were set out at each site in a systematic and standardized way. In addition 100-200 snap traps and live traps (Sherman traps) were set in special places, e.g. outside active burrows and promising runways. A few lemmings were also caught by hand.
Collared lemmings were captured at 15 of the 17 sites visited, but brown lemmings at 3 sites only. The population density was low, or extremely low, at all sites, and in all 86 collared and 19 brown lemmings were caught. At two sites on the Canadian mainland voles were abundant. At site 10, the Ivvavik National Park close to the Alaskan border, 61 root voles (Microtus oeconomus), 4 singing voles (Microtus miurus), and 5 northern redbacked voles (Clethrionomys rutilus) were caught. At site 8, south of Amundsen Gulf, 61 root voles were captured. One masked shrew (Sorex cinereus) was trapped at each of sites 8 and 10. No ground squirrels or weasels were captured. Five live-trapped collared lemmings gave birth to 22 young in the animal container on board. These were included in the chromosome studies.
Laboratory work
For every animal caught, the following data were registered: species, sex, weight, body and tail length, condition (fat level), and reproductive status (for females the number and size of embryos, or number of scars; for males testes length, and whether tubuli in epididymis were visible or not). Site, date, time, trap line, and method of collection were also recorded.
Samples for DNA analyses from liver and kidney were taken from all lemmings, 22 root voles, 4 singing voles and 2 northern redbacked voles and stored at -80°C in abs. ethanol. We also collected samples for other colleagues: lung tissue for virus studies (Antti Vaheri et al.), stomach and intestine for endoparasite investigation (Heikki Henttonen and Voitto Haukisalmi), muscle tissue for analysis of organic pollutants (Henrik Kylin and Cecilia Agrell), and skulls of Dicrostonyx for morphological studies (Nikolai Smirnov). Skins were taken by Anders Hansson and Peter Mortensen for the Swedish Museum of Natural History.
Chromosome preparations were made on board from 104 collared lemmings, 11 brown lemmings and 19 root voles. Direct preparations from bone marrow (adult animals), or liver and spleen (3–4 day old young) were made according to Fredga (1987). Chromosome behaviour during male and female meiosis will be studied in the collared lemming. Preparations were made from the testes of four adult males. Samples from ovaries of four 3–4 day old females were prepared and stored at -80°C for further EM studies of synaptonemal complexes.
Preliminary results
Chromosome number and morphology were analysed in unbanded preparations from 53 animals on board, and thus 81 specimens remain to be analysed. Chromosome banding techniques will be applied to identify the individual chromosomes and to clarify the relationships between the karyotypes of the various Dicrostonyx populations. G-banding will reveal the composition of the biarmed chromosomes, and C-banding will probably facilitate the identification of the Y and B chromosomes. The preliminary results obtained are summarized below.
Dicrostonyx hudsonius. We visited only one site (1) within the distribution range of this species. The single male captured had 48 chromosomes and the karyotype was in agreement with that previously described for four specimens from the eastern shore of Hudson Bay (Krohne 1982).
Dicrostonyx groenlandicus. 42 specimens from 12 sites were analysed in the microscope. As expected, the karyotypes varied both within and between populations, but due to the small number of lemmings caught, it will be difficult to estimate chromosomal variation within populations, and also the sex ratio. The total number of collared lemmings represents 42 males and 44 females.
The chromosome number varied between 38 and 50, and this variation was due to Robertsonian translocations between single-armed autosomes and the presence of 0–4 B chromosomes of variable size and morphology.
The lemmings on Ellef Ringnes Island (the magnetic North Pole) had a unique karyotype with 38 chromosomes (four pairs of large to medium biarmed autosomes and no B chromosomes). This was surprising, because on other islands north of the Parry Channel the collared lemmings have 46 chromosomes. The lemmings analysed so far from Bathurst Island, Melville Island and Devon Island had 46 chromosomes, and this was also the case in populations on Prince Patrick Island, Ellesmere Island, Cornwallis Island and Devon Island studied by Borowik and Engstrom (1993). Chromosome variation within and between populations is more common on the islands south of the Parry Channel and on the mainland (Borowik and Engstrom, 1993; Engstrom et al. 1993). The single specimen analysed so far from Cape Bathurst had 50 chromosomes. The final chromosome and mtDNA analyses will reveal how the collared lemmings in this area should be subdivided in to phylogenetic groups.
XY females were found on Banks Island South (Site 9). Four of the five females captured were XY, the fifth was XX. Females analysed from the other sites were all XX.
Lemmus trimucronatus. Six brown lemmings were analysed from site 10. As expected all had 50 chromosomes and karyotypes of the Beringian type, characteristic for L. trimucronatus (cf Jarrell and Fredga, 1993). Microtus oeconomus. Five root voles were analysed from one locality (8), and all had 2n=30 and the normal karyotype. Same populations of this species in Scandinavia show chromosomal polymorphism due to centric fission of two metacentric pairs (Fredga et al.1980).
Dates
June–September 1999
Participants
Principal investigator
Vadim B. Fedorov
Department of Biology, University of Oslo
Norway
Principal investigator
Karl Fredga
Department of Conservation Biology and Genetics, Evolutionary Biology Centre, Uppsala University
Sweden
References
Borowik, O.A. and Engstrom, M. D. (1993). Chromosomal evolution and biogeography of collared lemmings (Dicrostonyx) in the eastern and High Arctic of Canada. Can. J. Zool. 71, 1481-1493.
Engstrom, M.D., Baker, A.J., Eger, J.L., Boonstra, R. and Brooks, R.J. (1993). Chromosomal and mitochondrial DNA variation in four laboratory populations of collared lemmings (Dicrostonyx). Can. J. Zool. 71, 42-48.
Fedorov, V.B., Fredga, K and Jarrell, G.H. (1999). Mitochondrial DNA variation and the evolutionary history of chromosome races of collared lemmings (Dicrostonyx) in the Eurasian Arctic. J. Evol. Biol. 12, 134-145.
Fredga, K (1987). Chromosome preparations in the field from mammals long after death. Stain technology 62, 167-171.
Fredga, K (1994). Bizarre mammalian sex-determining mechanisms. In: The Differences Between the Sexes. Short, R. V. and Balaban, E. (ed.), Cambridge Univ. Press, Cambridge, 419-431.
Fredga, K, Persson, A. and Stenseth, N. C. (1980). Centric fission in Microtus oeconomu.. A chromosome study of isolated populations in Fennoscandia. Hereditas 92, 209-216.
Fredga, K, Fedorov, V., Jarrell, G. and Jonsson, L. (1999). Genetic diversity in Arctic lemmings. Ambio 28, 261-269.
Jarrell, G. and Fredga, K (1993). How many kinds of lemmings? A taxonomic overview. In: The Biology of Lemmings. Stenseth, N. C. and Ims, R.A. (ed.), Academic Press, U.K., 45-57.
Krohne, D.T. (1982). The karyotype of Dicrostonyx hudsonius. J. Mamml. 63, 174-176.