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Chromosomal versus mitochondrial DNA evolution: tracking the evolutionary history of the southwestern European populations of the Sorex araneus group (Mammalia, Insectivora)

The shrews of the Sorex araneus group show one of the most spectacular chromosomal evolutions ever recorded in mammals. Eight karyologically well-differentiated species are recognized in this group. They are characterized by the presence in males of a X[Y.sub.1][Y.sub.2] sex chromosome complex, and most species additionally show intraspecific chromosomal polymorphism. Numerous studies on this chromosomal variation both at interspecific and at intraspecific levels have been published (recent reviews in Hausser 1994; Ivanitskaya 1994; Volobouev and Dutrillaux 1991). This paper is concerned with the southwestern European forms of the group, for which karyotypic relationships are quite easy to decipher. The three species, S. granarius, S. coronatus, and S. araneus, differ mainly by Robertsonian changes. Extensive studies of the polymorphism of S. araneus strongly argue that Robertsonian (centric) fusions rather than fissions played the major role in this karyotypic differentiation (but for a different point of view see Halkka et al. 1987). Phylogenies of the chromosomal races of S. araneus and reconstructions of the postglacial recolonization of Europe have been suggested on the basis of such fusion precedence (Searle 1984; Hausser et al. 1986, 1991; Searle and Wilkinson 1987).

Sorex granarius is generally considered to have a karyotype closely similar to the common ancestor of the restricted group considered here (Wojcik and Searle 1988; Volobouev and Catzeflis 1989; Volobouev and Dutrillaux 1991). If we follow the nomenclature for the chromosomes of S. araneus proposed by Searle et al. (1991), where the individual arms are labeled by letters according to their size and their G-band pattern, S. granarius has every autosomal arm (a to r) in an acrocentric form, whereas S. coronatus and S. araneus bear both a common fusion (af) and specific fusions of autosomal arms. It is thus tempting to suggest that S. granarius, which is now confined to central and northwestern Spain and Portugal, was isolated early from the mainstream of the group. This mainstream then acquired the fusion af, and eventually diverged to form the two species S. araneus (fusion bc; numerous chromosomal races and forms characterized by the presence of further fusions) and S. coronatus (ci and other fusions; additionally two centromeric shifts) (Volobouev and Catzeflis 1989). The detailed karyotypes of the forms considered here are given in table 1 and their distribution is summarized in figure 1.

Biochemical studies however produced results in contradiction with this appealing and straight-forward TABULAR DATA OMITTED model (Catzeflis et al. 1982; Catzeflis 1984): biochemically, S. granarius appears to be merely another population of S. araneus, and even S. coronatus is not obviously isolated from this species. A preliminary study of the mitochondrial DNA (mtDNA) of these forms clearly confirmed the results of Catzeflis and not the phylogeny constructed with chromosomes (Taberlet et al. 1991).

Chromosomal analysis was frequently used to establish phylogenies at different taxonomic levels (reviews in Sites and Moritz 1987; Baker et al. 1987). A reasonably good congruence between mtDNA markers and karyotype evolution was found, for example, for Sceloporus grammicus chromosomal races (Sites and Davis 1989) or for Triturus species (MacGregor et al. 1990). In the case presented here, however, it is at first view difficult to reconcile karyotype and mtDNA data in shaping the phylogeny of the shrews studied. New karyological data and a more detailed analysis of mtDNA sequences (cytochrome b gene) may help us to solve this problem.


Specimens Analyzed

Sampling localities, species, and karyotypic races of the individuals used in the present work are given in table 2. Except for the Sorex araneus sample from the Pyrenees, karyotypic results have been previously published (Hausser et al. 1991). TABULAR DATA OMITTED Two S. samniticus and two S. minutus were also included to find a suitable outgroup for assessing the phylogeny of the S. araneus group.


Five individuals caught near Lac des Bouillouses and Etang de Balcere, Pyrenees Orientales, in France, have been analyzed to complete our karyotypic data for this region, which is important for the understanding of the general evolution of this group. G-banded chromosomes were prepared after direct treatment of bone marrow or spleen cell suspensions according to Seabright (1971). Conventional Giemsa staining was also performed.

To compare karyotypic and mitochondrial DNA (mtDNA) phylogenies, parsimony analyses were computed for the races and species considered, using the PAUP program (Swofford 1990). The S. araneus "intermediate" form was excluded from the analysis because of its clearly hybrid origin (Hausser et al. 1991). The karyotype of another species of the S. araneus group, Sorex arcticus maritimensis from eastern Canada (Volobouev and Van Zyll de Jong 1988; Volobouev 1989) was used as an outgroup to root the trees obtained. This species is considered to have diverged early from the European forms studied here (Volobouev 1989; Volobouev and Dutrillaux 1991). Chromosomal characteristics have been coded 0 if present in S. arcticus and another taxon at least, 1 if present but not fixed, and 2 if present and apparently fixed either in S. arcticus alone or in other taxa. An intermediate state 1 (polymorphic populations) was postulated in the history of every mutation between states 0 and 2. As the homologies of the small chromosomal changes described by Volobouev (1989) are sometimes difficult to assess, we present here analyses using whole-arm rearrangements only (Robertsonian translocations and tandem translocations of the arms of the reference species, S. araneus). These analyses have been performed with these characters ordered with and without polarity, that is, with and without the possibility of reversing a Robertsonian fusion.

Sampling Localities and DNA Isolation

To assess which mtDNA clones are representative of each of the chromosomal races and species, we analyzed 27 individuals collected from various southwestern European localities. Additionally, five individuals collected outside our study area were analyzed for comparison. They come from Oxford., England (2), Eberswalde, Brandenburg, Germany (1), Zd'ar na Sazavou, Moravia, Czechoslovakia (1), and the Baba Mountains, Macedonia (1). Total genomic DNA was extracted from frozen tissue or samples preserved in 70% alcohol by digestion with proteinase K for 2-4 h at 37 [degrees] C, purified by extracting twice with phenol/chloroform and once with chloroform. The sample was then desalted and concentrated by ethanol precipitation (Kocher et al. 1989).

Enzymatic Amplification and Sequencing

A polymerase chain reaction was performed to generate mitochondrial sequences containing part of the cytochrome b gene. Conditions for DNA amplification and sequencing were as described by Kocher et al. (1989). Amplified mtDNA was purified either by electrophoresis in low melting temperature: agarose or by centrifugal dialysis in Ultrafree-MC (Millipore) columns, and used as the template in an asymmetric PCR to generate single-stranded DNA for sequencing (Gyllensten and Erlich 1988; Allard et al. 1991).

Initial amplification of a 307-bp region of the cytochrome b gene for the 32 shrews employed the primers L14841 and H15149 designed by Kocher et al. (1989); this first screening allowed us to compare the different sequences, to group the mtDNA clones, to choose an outgroup, and to select individuals for a more detailed analysis. A large part of the cytochrome b gene of the chosen individuals was then amplified and sequenced with primers L15162 and H15915 (Irwin et al. 1991).

Sequence Analysis

The number of substitutions per site was estimated using the two-parameter model of Kimura (1980). The genealogical relationships among the mtDNA haplotypes were obtained by parsimony analysis of the cytochrome b sequences using PAUP (Swofford 1990). Confidence values for internal lineages were assessed with the bootstrap option (Felsenstein 1985).


Karyotypic Data

The populations of Sorex araneus collected from Lac des Bouillouses and Etang de Balcere, both localities near Mount Carlit, Pyrenees Orientales, France, belong to the Western European Phylogenetic Group, WEPG (Searle 1984), and show a primitive karyotype for this group, with the metacentrics gm, hi, and jl only. Metacentric hi was present in a heterozygous state for five of the studied animals. Using the nomenclature rules defined by Searle et al. (1991), they can be provisionally defined as follows:

S. araneus, Carlit form

Karyotype: XX/X[Y.sub.1][Y.sub.2], af, bc, gm, h/i, jl, k, n, o, p, q, r, tu.

Phylogeny Based on Karyotype

Each of the two analyses of parsimony, considering either reversible or irreversible whole arm mutations, revealed only one most parsimonious tree, practically the same in both cases, with the same length and the same branching pattern. Their consistency index is 0.978; the only homoplasy concerns the lo metacentric, which is also responsible for the only difference between the two trees. It is considered to have fused twice (in branches leading to S. coronatus and to S. araneus Valais) in the analysis using irreversible characters. In the analysis using reversible characters, the absence of lo in the other taxa of S. araneus can be interpreted as simply a disappearance of the metacentric in a polymorphic population as well as a fission. No other fissions are involved in either tree. Bootstrap tests with 1000 replicates indicate that S. granarius is a sister group of S. coronatus--S. araneus in 91% (reversible mutations) or 87% (irreversible mutations) of the trees produced. The Carlit-Vaud-Acrocentric group is present in 90% of the cases. Analyses on the whole set of mutations as interpreted by Volobouev (1989) give the same branching pattern and suggest the same behavior for the whole-arm rearrangements.

Cytochrome b Gene Sequences

Table 3 gives the nucleotides at 45 variable sites of the cytochrome b gene among the 27 shrews assayed for southwestern Europe. The additional individuals of northern and eastern Europe are identical to the Vaud shrews, except for two transitions, C-T, found in the Oxford shrews (position 14,866 for two individuals, position 15,081 for one individual). Most of the substitutions are transitions (93.3%), in agreement with the transitional bias found previously in other mammalian species (Brown et al. 1982; Irwin et al. 1991). This first screening indicates the grouping of the southwestern European populations of the S. araneus group into three main mitochondrial lineages: CC = S. coronatus, CV = S. araneus Valais race, CA = S. granarius, S. araneus Carlit form, S. araneus VIA group (= Vaud, Intermediate, and Acrocentric forms) as well as the additional northern and eastern shrews studied. Sorex minutus differs from the S. araneus Vaud race by 24-25 substitutions (22-23 transitions, two transversions). Sorex samniticus differs by 18 substitutions (17 transitions, one transversion) and seems to be more closely related to individuals of the S. araneus group than S. minutus. Therefore, we have chosen S. samniticus as an outgroup for further analysis. To construct a phylogenetic tree, two additional parts of the cytochrome b gene were sequenced for S. samniticus and seven individuals representative of the different karyotypic races. Two individuals of the Valais race were included in this second round of sequencing, because the first sequences showed some variations between the southern and northern populations of this chromosomal race. A total of 777 base pairs were sequenced for these eight shrews. The sequence alignment is given in figure 3. The numbers of transition/transversion and silent/replacement substitutions are shown in table 4. Out of 777 base pairs, 93 sites were found to be variable including 86 transitions and nine transversions (2 sites with both transition and transversion). The substitutions on 4 variable sites induced amino acid changes at positions 212 (cysteine/serine), 295 (alanine/valine), TABULAR DATA OMITTED 303 (valine/methionine), and 306 (phenylalanine/leucine). This pattern of amino acid change agrees with the structural model of the cytochrome b (Howell 1989); all the observed changes occur on variable regions according to Irwin et al. (1991). The genetic distances among the different chromosomal taxa were computed from the sequence of figure 3 and are given in table 5.
TABLE 4. Numbers of transition/transversion and silent/replacement differences
among eight chromosomal races or species of the genus Sorex. These numbers are
deduced from the sequences of figure 3. The abbreviations of the individuals
are the same as in figure 3.

         S.arVaud   S.arAC   S.arIN   S.gran   S.arVI   S.arVS   S.coro

S.arVD      --        2/0      3/0      7/1     14/0     11/1     26/1
57/6 S.arAC      1/1       --       5/0      9/1     16/0     13/1     28/1
  59/6 S.arIN      2/1       3/2      --       8/1     13/0     10/1     27/1
    58/6 S.gran      7/1       8/2      9/0      --      17/1     13/2
25/2     57/7 S.arVI     13/1      14/2     13/0     18/0      --       3/1
  32/1     61/6 S.arVS     11/1      12/2     11/0     15/0      4/0      --
    26/2     58/7 S.coro     26/1      27/2     28/0     27/0     33/0
28/0      --      62/7 S.samn     60/3      61/4     62/2     62/2     65/2
  63/2     67/2      --

Phylogeny Based on mtDNA

Of the 93 variable sites of the sequences of figure 3, 23 are phylogenetically informative. The most parsimonious tree inferred from these variable sites is shown on figure 4. The bootstrap test (1000 replicates) indicates that the branching of the two individuals of the Valais race is highly significant (this group is present in 99.7% of the tree produced); therefore, we can assume that this chromosomal race is monophyletic for mtDNA. Using the data from table 4, an UPGMA and neighbor-joining (Saitou and Nei 1987) trees were computed, which showed exactly the same topology. The comparison of the trees built on the mtDNA and the karyotypic data clearly shows the difference in the branching of S. granarius obtained by the two approaches.


Our results confirm the presence in western Europe of three main and well-differentiated mitochondrial DNA (mtDNA) haplotype families in the Sorex araneus group. The CC and CV clones probably derive from early isolations of populations in the Iberian and Italian peninsulae. The present distribution of the CA clone, which includes Macedonia and Moravia, suggests an eastern origin. The phylogenetic tree inferred from the cytochrome b gene is approximately consistant with the UPGMA tree proposed by Catzeflis (1984) using protein electrophoresis. The main difference concerns the Valais race, which appears to be homogeneous for the mtDNA, whereas Catzeflis's results link the northern populations of this race to the VIA group rather than to their southern relatives (Gran Sasso). This discrepancy could be attributed to past hybridization between the northern populations of the Valais race and the VIA group, which was suggested elsewhere (Hausser et al. 1991).

Irwin et al. (1991) suggested, for the third position of codons of the cytochrome b gene in mammals, a silent divergence rate at approximately 10% per my. On this basis, we can estimate that the common maternal ancestor of the southwestern European taxa of the S. araneus group lived about 1 mya. The Valais and the VIA-granarius group would have a common ancestor 0.4 mya, and, in the CA clone, S. granarius and the VIA group would have a common ancestor 0.3 mya. Even if these estimations must remain qualified because of uncertainties in calibration, they are higher than the ones of Catzeflis (1984) on the basis of electrophoretic differences, who suggested 100,000 yr for the separation of S. araneus and S. coronatus, and 10,000 yr for the araneus-granarius divergence. Paleontological data also suggest a more recent divergence (Horacek and Lozek 1988). This discrepancy can be partially solved if we consider the size of the populations. The pace of haplotype extinction is in inverse ratio to the female population size (Avise et al. 1984). Ecological data suggest that, in favorable habitats, these territorial and rather ubiquitous animals presumably exist in very large continuous populations (Croin Michielsen 1966). Their very good dispersal power has also to be taken into account: for instance, S. araneus was shown to recolonize islands on frozen lakes easily (Hanski 1986). Therefore, we cannot exclude the possibility that the haplotype divergences have largely antedated the actual population isolations.

What remains is that S. granarius, which retains mostly primitive chromosomes, is the nearest genetic relative of the S. araneus of the CA lineage, and that is in apparent contradiction with the postulated chromosomal evolution. A way to solve this problem would be to admit a reverse evolution of the karyotype of this species, that is, a fission process reversing the af and bc metacentrics to their acrocentric condition. In this hypothesis, a primitive, "Acrocentric-like" population of the CA lineage would have extended in southwestern Europe, and then retreated, leaving an isolated population in Spain that undertook their own chromosomal evolution by fission. A second and recent extension of S. araneus populations, also followed by a retreat, TABULAR DATA OMITTED would have left the Carlit form in the Pyrenees. This repeated migration accounts for the divergence observed in the CA lineage between S. granarius and the S. araneus taxa. An alternative hypothesis would postulate that the first extension of populations of the CA clone toward Spain occurred before Robertsonian fusions appeared in the species studied here (except for tu). To choose between these two proposals, we have to evaluate the likelihood of fissions of af and bc metacentrics.

Fission is actually attested for S. coronatus, where two individual cases have been observed for metacentrics ci (Olert 1973) and kq (Rossier et al. 1993). Overall, the number of individuals analyzed in this species can be approximately evaluated to 300. It seems therefore that fission is a relatively frequent phenomenon. Nevertheless, these two single cases observed in a species otherwise monomorphic suggest a contrario that if fissions perhaps occur at a high rate, they were not able to establish themselves in populations of S. coronatus, where their success would have left polymorphic populations at least. It is more difficult to demonstrate unequivocally the occurrence of fissions in S. araneus, in which the presence of acrocentric chromosomes can be considered either as the product of fissions or as the remains of a former acrocentric state. Fissions and reciprocal translocations have been advocated to explain the present distribution of the Robertsonian metacentrics in southern Finland (Halkka et al. 1987) and in England (Searle et al. 1990). However, the general structure of the geographical distribution of the largest and of most of the medium-sized Robertsonian metacentrics strongly support the hypothesis of a large predominance of stable fusions, at least in the first steps of this chromosomal evolution (Searle 1984; Zima et al. 1988; Hausser 1994). Let us consider the case of the af metacentric. It is shared without known polymorphism by three species with contiguous and partially overlapping distributions (S. coronatus, S. araneus, and Sorex daphaenodon; Zima 1991). Each of the other autosomic arms b to r can be observed either isolated or involved into several alternative fusions in the same three species. It seems therefore unlikely that arm a fused independently with the same arm in three taxa: there are 15 available arms, plus the possibility that arm a remains isolated directly or after a fission. If one considers that fusion and fission are balanced processes, the probability of obtaining af by convergence in three taxa is therefore [16.sup.-3], or 0.00024. The same reasoning can be used for the bc metacentric in the numerous S. araneus chromosomal races. This metacentric is present and fixed in each of them. Some of these populations are genetically more separated from the alpine S. araneus than even S. coronatus (Catzeflis 1984). Long-term stability of these metacentrics is also indirectly suggested in S. araneus by the lack of centromeric heterochromatin, which is present in more recent metacentrics and could play an important part in Robertsonian processes (Garagna et al. 1991, quoting data of Searle 1983). Additionally, metacentric bc of S. araneus differs from the homologous arms of S. granarius and S. coronatus by another mutation which transferred a terminal dark G-band from arm b to arm c (Wojcik and Searle 1988; Volobouev 1989). Such a mutation may be reversible. Nevertheless, in this context, the hypothesis of a fission of both af and bc is neither the most likely one, nor the most parsimonious.

The alternative hypothesis implies that Robertsonian processes occurred relatively late in this group, long after the three main lineages of mtDNA have diverged. As stated by Baker et al. (1987), it is not possible to determine directly at what point in the past chromosomal rearrangements occurred and became established. Late changes in these taxa are thus as likely as early changes. This hypothesis, nevertheless, implies that Robertsonian metacentrics af and bc were able to pass from one to another of the mtDNA lineages, which implies that Robertsonian metacentrics and mtDNA lineages have different geographical behaviors.

Such mtDNA clones cannot easily pervade contiguous populations, except by the relatively slow process of random replacement of other clones, which can be accelerated only by strong bottlenecks in the relevant populations (for an example of mtDNA behavior in a hybrid zone see Nelson et al. 1987). In the case of the shrews under study, the difficulty in mixing mtDNA lineages is perhaps increased by the strict territoriality of the females through most of their life-span, whereas the males are far more vagile during the reproductive season and visit several female territories (Cantoni 1990). Consequently, mt-DNA clones, which are mostly--but not uniquely (Gyllensten et al. 1991)--transmitted by maternal inheritance, would be geographically more stable than nuclear markers. Such a behavior-induced restriction of female mediated gene flow was suggested by Birky et al. (1983) and actually shown for mule deer populations (Cronin et al. 1991). Therefore, mtDNA clones should be geographically displaced mainly by the movement of the populations themselves, when they invade a new territory. During a retraction phase, the fringe of mixed populations would usually disappear. A succession of contractions and expansions of the populations characterized by different mtDNA haplotypes can therefore be considered, which lead to successive isolations and contacts without inducing any extensive admixture of the mtDNA clones or even nuclear genes (Hewitt 1989).

It is thus possible to consider the presence in Europe, during a past interglacial, beside an isolated CA population in the mountains of Spain, of three parapatric population sets, characterized by the same acrocentric karyotype but already differentiated for mtDNA lineages. The genetic differentiation of these shrews is still far below the usual specific level (Catzeflis 1984). The populations in contact would therefore have been fully interfertile, and af metacentric would have spread across them--maybe together with the genetic features allowing these shrews to tolerate fusions. Arguments for a spreading of Robertsonian chromosomes across acrocentric populations are mostly indirect.

Simple Robertsonian heterozygotes in S. araneus do not suffer a noticeable reduction of fertility (Wallace et al. 1991; Mercer et al. 1991). A factor positively influencing the frequency of metacentrics is nevertheless needed to explain the rapid postglacial expansion postulated. Meiotic drive (preferential transmission of metacentrics) was suggested by Hausser et al. (1985) and at first view confirmed by the karyologic study of wild females and their litters (Searle 1986a). The further discovery of multiple paternity in shrew's litters (Searle 1990; Tegelstrom et al. 1991) weakened these indications. A better adaptive value of the carriers of homozygous metacentrics could be suggested (Baker and Bickham 1986), but good evidence of such selective processes in Sorex are scarce; the only evidence is given by Wojcik (1991) who showed rather that acrocentrics can be maintained in a population by environmental factors favoring heterozygotes. Most of the other cases of local polymorphism were explained by the presence of hybrid zones. We still lack good evidence for the mechanism explaining the unquestionable evolutionary success of the Robertsonian metacentrics over their acrocentric homologues.

Nevertheless, the geographical distribution of most of the Robertsonian metacentrics actually suggest that Robertsonian fusions spread across contiguous, primitively acrocentric populations (Zima et al. 1988; Hausser 1994). For instance, the geographical succession of Vaud, Intermediate, and Acrocentric karyotypic forms across the genetically homogenous VIA group in the western Alps, can be interpreted as the tracks left by a recent spreading of Robertsonian metacentrics into an Acrocentric population. This progression southward would have been stopped only by the occupation of the Rhone and Arve valleys by S. coronatus (Hausser et al. 1991). The northern extension of the WEPG metacentric gm in Sweden, in populations otherwise characterized by metacentrics of different origin like hn (Fredga and Nawrin 1977), and the relatively independant cline of frequency of pr across the hybrid zone between Oxford and Hermitage race in England (Searle 1986b, 1988) can also be interpreted as indications of such processes.

The geographical spreading of Robertsonian metacentrics would be stopped only where they meet geographical barriers or come in contact with other, incompatible metacentrics with monobrachial homologies. In the latter case, multivalents are formed during the meiotic process in the hybrids, which can lead to aneuploid gametes and thus to a more or less strong reduction in fertility. Recent work suggests that male heterozygotes for metacentrics with monobrachial homologies can be almost fully fertile (Mercer et al. 1992). Nevertheless, incompatibility problems probably occur in nature, as shown by the very well-documented examples given by the hybrid zones between Oxford and Hermitage race in England (Searle 1986b, 1988) and between races II and IV in northeastern Poland (Fedyk et al. 1991).

For the enzymatic markers studied by Catzeflis (1984), they are neither obviously favored by a selective process, nor by mechanical processes like meiotic drive. However, they are transmitted equally by both sexes and follow the rules of Mendelian genetics. They should therefore show a geographical behavior intermediate between those of mtDNA clones and of Robertsonian metacentrics, which is actually observed for instance at the limit between CA and CV lineages (Catzeflis 1984; Hausser et al. 1991). The overall consistency of the electrophoretic and mtDNA results reinforces our hypothesis about the migration of metacentrics across acrocentric populations--at least in the case of af and bc--and confirms the recentness of the "Robertsonian craziness" (Capanna 1991) of the araneus group.


We thank J. B. Searle, Oxford; J. Zima, Brno; and P. Vogel, Lausanne, who kindly provided comparison material from England, Yugoslavia, and Germany; we are grateful also to W. Wahli, Lausanne, for technical support. The constructive criticism of an earlier draft of this paper by G. M. Hewitt, Norwich, and J. B. Searle, Oxford, was highly appreciated. This work was undertaken as part of an agreement in research collaboration between the University of Lausanne (Switzerland) and the University Joseph Fourier of Grenoble (France).


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Author:Taberlet, Pierre; Fumagalli, Luca; Hausser, Jacques
Date:Jun 1, 1994
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