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The Chromosome Complement of Sorex Common Shrew

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The Chromosome Complement of Sorex Common Shrew Heredity 61(1988) 225—229 The Genetical Society of Great Britain Received 18 January 1988 The chromosome complement of Sorex granarius—the ancestral karyotype of the common shrew (Sorex araneus)? J. M. Wójcik* and * MammalsResearch Institute, Polish Academy of J. B. Searlet Sciences, 17-230 Bialowieza, Poland. 1 Department of Zoology, University of Oxford, South Parks Road, Oxford OXI 3PS, U.K. We present the G-bandkaryotypeof Sorex granarius (Miller, 1910). With minor exceptions, each of the acrocentric autosomes in this karyotype is completely homologous to one of the chromosome arms in the karyotype of the common shrew (Sorex araneus L., 1758). If, as is the simplest interpretation, the karyotypic evolution in S. araneus is by repeated Robertsonian fusion, the karyotype in S. granarius represents the ancestral condition. We urge breeding studies to establish whether the designation of S. granarius as a full species is justified. INTRODUCTION In terms of chromosomal (structural) muta- tions, the simplest explanation for this variation is Thecommon shrew (Sorex araneus L., 1758) has that the ancestral karyotype of the common shrew one of the most variable karyotypes of any mam- consisted of acrocentric chromosomes. On this mal. Consequently, wild populations throughout hypothesis, the polytypic variation arises from its range have been the subject of much cytogenetic different pairs of the ancestral acrocentric chromo- analysis, particularly in recent years (e.g., Beicheva somes having joined at their centromeric ends (a and Kolevska, 1986; Fedyk, 1986; Hausser et a!., process generally termed Robertsonian, or centric, 1986; Searle, 1986a, b, 1987; Wójcik, 1986; Fedyk fusion) to form different, race-specific, combina- and Leniec, 1987; Halkka et aL, 1987; Searle and tions of metacentrics. If this is the case, the Robert- Wilkinson, 1987; Wójcik and Zima, 1987; Fredga, sonian polymorphism can be considered to result 1987). The species initially attracted interest (Shar- when both the ancestral acrocentric chromosomes man, 1956; Ford et aL, 1957) because it displays and the derived metacentric chromosomes are karyotypic polymorphism of a Robertsonian type, present in the same population. Thus, one can such that individuals within a population vary in explain the karyotypic variation in the common chromosome number while the number of chromo- shrew in terms of a single type of mutation, the some arms (the nombrefondamenta!) in the karyo- Robertsonian fusion of ancestral acrocentric type remains constant. In areas of polymorphism, chromosomes. An alternative, and less par- a particular chromosome arm may occur un- simonious, hypothesis is that the observed karyo- attached (i.e., as an acrocentric) or fused to another typic variation arose from ancestral metacentric chromosome arm (i.e., as part of a metacentric). chromosomes by two types of structural mutation: In the 1970s it was demonstrated, with the aid of Robertsonian (or centric) fission and either chromosome banding techniques, that the meta- Robertsonian fusion or whole-arm reciprocal centrics may be composed of different combina- translocation. All these forms of mutation have tions of chromosome arms in different parts of the been well-demonstrated in mammals (e.g., Robert- range of the species (Fredga, 1973; Fredga and sonian fusion in mouse: Leonard and Deknudt, Nawrin, 1977). These sets of metacentrics occur 1967; Robertsonian fission in the shrew S. in discrete geographical areas and may be con- coronatus: Olert, 1973; whole-arm reciprocal trans- sidered to define distinct karyotypic races which location in mouse: Crocker and Cattanach, 1981). form a patchwork throughout the northern On the assumption of an ancestral acrocentric Palaearctic range occupied by the species (e.g., in karyotype and only Robertsonian fusion muta- Sweden: Fredga and Nawrin, 1977; in Siberia: Král tions, Searle (1984) constructed a phylogeny for et a!., 1981; in Britain: Searle, 1984). the known karyotypic races of the common shrew, 226 J. M. WOJCIK AND J. B. SEARLE which fitted well with the geographic distribution araneus and S. granarius, it was essential to obtain of these races. good G-banded preparations of S. granarius. One Of the chromosome arms within the karyotype of us, J. M. W., collected one male and one female of the common shrew, it is those autosomes label- of this species from La Granja, Segovia, Spain in led g —ronthe basis of G-banding pattern (Halkka May 1987 and made mitotic chromosome prepar- et al., 1974; Fredga and Nawrin, 1977) which dis- ations according to a standard method (Wójcik, play Robertsonian variation. The sex chromosome 1986) after injection with colcemid (a metaphase complement is invariant and similar to other arrestant). species within what is now known as the S. araneus complex (Hausser et al., 1985), these all have an XX/XY1Y2 system (Fredga, 1970). The remaining RESULTSAND DISCUSSION six autosome arms (a, b, c,f t, u) are always pres- ent combined in the metacentrics af bc and tu in AG-banded karyotype of the female S. granarius the common shrew karyotype. In this paper we is shown in fig. 1. The chromosome number is seek evidence whether these metacentrics, in addi- 2n =36,and was 2n =37for the male, in confirma- tion to those composed of chromosome arms g — tion of the findings of Hausser et a!. (1985). In couldbe products of Robertsonian fusion. both individuals all the autosomes were acrocen- Within the S. araneus complex there are a tric, except for one pair, where there was poly- number of species which are morphologically morphism between a metacentric and an acrocen- extremely similar to S. araneus. One of these is the tric state; the male was homozygous acrocentric Iberian species, S. granarius (Miller, 1910), which and the female heterozygous (fig. 1). Hausser et was of great interest to us because conventional a!. (1985) report this polymorphism and illustrate chromosome preparations had revealed an acro- a heterozygous male. centric autosome karyotype with characteristics All the chromosomes of S. granarius appear similar to those expected in the putative ancestral homologous, or nearly so, to the chromosomes of karyotype of S. araneus (Hausser et a!., 1985). To the common shrew and can be labelled by the same examine the homology of the chromosomes of S. nomenclature (figs. I and 2). The sex chromosome >1 ! • \ 11)fl Ri m J k I i>I "). ::$jt; x x p q Figure 1 G-band karyotype of female S. granarius, with each arm labelled according to the standard nomenclature system of the common shrew (Halkka et a!., 1974; Fredga and Nawrin, 1977). CHROMOSOMES OF SOREX GRANARIUS 227 is 1 Ia '14'Ik.: f k3 a& (aM U t Figure2 Comparison between G-banded chromosome arms of S. granarius (left) and S. araneus. In each case, all chromosomes are cut from a single spread except for the tu of S. granarius which is the same as that illustrated in fig. 1. For S.araneus it was necessary to cut metacentrics af bc, ji,hiand gin at their centromeres for this comparison. Arrows indicate a dark band that is present on chromosome b of S. granarius but on chromosome arm c of S. araneus. set appears identical in the two species and the tonemal complex analysis in hybrids should autosomes of S. granarius (with the exception of resolve the mutation involved. the polymorphic pair) are apparently homologous (b) The karyotypic polymorphism in S. granarius with the chromosome arms a —cand f— r of S. involving one of the small autosome pairs is araneus. The metacentric state of the polymorphic not of a Robertsonian type (fig. 1). Instead the pair in S. granarius is homologous to tu of S. chromosome number remains constant in the araneus. Thus, in essence, the karyotype of S. different karyomorphs while the nombrefonda- granarius is the expected ancestral acrocentric mental changes. The metacentric form of tu karyotype of the common shrew on the simplest may differ from the acrocentric state by either model of karyotype evolution, repeated Robert- a pericentric inversion or a centric shift. The sonian fusion. Even two of those autosomes which former would appear more likely on the basis are invariably metacentric in the common shrew of chromosome band pattern (fig. 1), but karyotype, af and be, are found as acrocentrics a, prometaphase banding analysis and a study b, c and f in S. granarius. of the synaptonemal complexes of hybrids To a minor degree the karyotypic variation in would be desirable. S. granarius and S. araneus cannot wholly be (c) When chromosome arm j is in the acrocentric explained, in a mutational sense, by Robertsonian state in S. araneus (not illustrated) it has a fusions: distinct short arm, while acrocentric j in S. (a) There is a centromeric dark band on chromo- granarius has a terminal centromere. (This is some arm b (but not c) of S. granarius while particularly clear in conventional prepar- such a band is found on chromosome arm c ations: Fredga, 1973; Hausser et al., 1985; of S. araneus (fig. 2). This can most simply be J. M. Wójcik and J. B. Searle, unpublished explained by either a pericentric inversion or data.) As chromosome arm j appears to have a centric shift in the metacentric bc of S. the same banding pattern when an acrocentric araneus (or a karyotypic intermediate between in both S. granarius and S. araneus and when S. araneus and S. granarius). Clearly, banding part of a metacentric in S. araneus, it would on prometaphase chromosomes or synap- appear that arm j in the acrocentric condition 228 J. M. WOJCIK AND J. B. SEARLE in S. araneus differs from the other states of j CROCKER, M. AND CATTANACH, B. M. 1981. X-ray induction by a centric shift. This is discussed further in of translocations in mice carrying metacentrics (Robert- sonian fusions); detection of whole arm chromosome Searle and Fredga (in preparation).
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