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Home , Autosome, Shrew

Heredity 61(1988) 225—229 The Genetical Society of Received 18 January 1988

The complement of granarius—the ancestral of the (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 of any mam- consisted of acrocentric . 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 , 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 (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 chromosome 1986) after injection with colcemid (a 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 >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 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 . (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). exchanges. Mutation Research, 91, 353—357. Thus the chromosome complement of S. FEDYK, s. 1986. Genetic differentiation of Polish populations granarius may be closely similar to the ancestral of Sorex araneus L. II. Possibilities of flow between karyotype of S. araneus, with autosome arms a — chromosome races. Bull. Acad. Pol. Sci., 34, 161-171. r present as acrocentrics (while all these armsFEDYK, S. AND LENIEC, H. 1987. Genetic differentiation of f— Polish populations of Sorex araneus L. I. Variability of can be present in metacentrics in S. araneus and autosome arm combinations. Folio Biol. (Krakow), 35, a, b,cand f always are), but with tu, at least in 57—68. some individuals of S. granarius, already in a meta- FORD, C. F., HAMERTON, J. L. AND SHARMAN, G. B. 1957. centric state. However, to support this scheme of Chromosome polymorphism in the common shrew. Nature, karyotypic evolution it is desirable to make a much 180, 392-393. FREDGA, K. 1970. Unusual sex chromosome inheritance in larger comparison within the S. araneus complex mammals. Phil. Trans. R. Soc. Lond., B259, 15-36. and elsewhere within the genus Sorex. V. T. FREDGA, K. 1973. A new chromosome race of the common Volobouev (personal communication) is attempt- shrew (Sorex araneus) in Sweden. Hereditas, 73, 153—157. ing such an analysis. FREDGA, K. 1987. Chromosome races of the common shrew Finally, we would like to raise some taxonomic (Sorex araneus) in Sweden. What happens in the hybrid zones? In Brandham, P. E. (ed.) Kew Chromosome Confer- issues. Catzefiis et aL (1982) show that biochemical ence ii!, Allen and Unwin, London (In press). markers fail to separate S. granarius and S. araneus FREDGA,K. ANDNAWRIN, i. 1977. Karyotype variability in and recent papers by Hausser (1984) and Hausser Sorex araneus L. (, Mammalia). Chromosomes et a!. (1985) raise doubts about the significance of Today, 6, 153-161. HALKKA, L., HALKKA, 0., SKAREN, U. AND SODERLUND, V. previously reported morphological differences 1974. Chromosome banding pattern in a polymorphic between the species (Hausser et aL,1975).Our population of Sorex araneus from northeastern Finland. karyotypic studies indicate that apart from some Hereditas, 76, 305-314. minor rearrangements involving chromosome tu HALKKA, L., SODERLUND, V., SKAREN, U. AND HEIKKILA, .t. (which are not always present) and chromosome 1987. Chromosomal polymorphism and racial evolution of Sorex araneus L. in Finland. Hereditas, 106, 257-275. arms b, c and j, there is less difference between S. HAUSSER, .j.1984.Genetic drift and selection: Their respective granarius and some of the most acrocentric karyo- weights in the morphological and genetic differentiation types of S. araneus than between some karyotypes of four species of shrews in southern Europe (Insectivora, within the species S. araneus. Sorex granarius and Soncidae). Z. f zoot Systematik u. Evolutionsforschung, 22, 302-320. S. araneus are at present allopatric, so it is not HAUSSER, J., GRAF, J.-D. AND MEYLAN, A. 1975. Donhees possible to determine, without intrusive experi- nouvelles sur les Sorex d'Espagne et des Pyrénées (Mam- ments, whether they are good biological species. malia, Insectivora). Bull. Soc. Vaud. Sc. Nat., 348, 241-252. However, attempts should be made in captivity, HAUSSER, J., CATZEFLIS, F., MEYLAN, A. AND VOGEL, P. 1985. and preferably in a semi-natural situation, to deter- in the Sorex araneus complex (Mammalia: Insectivora). Acta ZooL Fennica, 170, 125—130. mine whether these soricines will interbreed and HAUSSER, J., DANNELID, E. AND CATZEFLLS, F. 1986. Distribu- if so, the extent of hybrid unfitness (and the contri- tion of two karyotypic races of Sorex araneus (Insectivora, bution of karyotypic difference to any fitness Soricidae) in Switzerland and the post-glacial recolonisa- reduction). tion of the Valais: First results. Z f zool. Systematik u. Evolutionsforschung, 24, 307—314. KRL. B., ANISKIN, V. M. AND VOLOBOUEV, V. T. 1981. Karyo- type variability in Siberian populations of Sorex araneus Acknowledgements We would like to thank Dr Santiago Reig (Soricidae, Insectivora). Folia Zoo!. Brno, 30, 23—37. Redondo for his help with collections. Dr Angela Douglas LEONARD, A. AND DEKNUDT, G. Fl. 1967. A neW marker for kindly read through the manuscript. J. B. S. is supported by chromosome studies in the mouse. Nature, 214, 504-505. the Royal Society of London. OLERT, .i. 1973. 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