A MODEL OF A HYBRID ZONE BETWEEN TWO CHROMOSOMAL RACES OF THE COMMON SHREW (SOREX ARANEUS)

The common shrew (Sorex araneus) is subdivided into several karyotypic races in Britain. Two of these races meet near Oxford o form the “Oxford-Hermitage” hybrid zone. We present a model which describes this system a; a “tension zone,” i.e., a set of clines maintained by a balance between dispersal and selection against chromosomal heterozygotes. The Oxford and Hermitage races differ by Robertsonian fusions with monobrachial homology (kq, no versus ko), and so Fl hybrids between them would have low fertility. However, the acrocentric karyotype is found at high frequency within the hybrid zone, so that complex Robertsonian heterozygotes (kg no/q ko n) are replaced by more fertile combinations, such as (kg no/k q n o). This suggests that the hybrid zone has been modified so as to increase hybrid fitness. Mathematical analysis and simulation show that, if selection against complex heterozygotes is sufficiently strong relative to selection against simple heterozygotes, acrocentrics increase, and displace the clines for kg and no from the cline for ko. Superimposed on this separation is a tendency for the hybrid zone to move in favor of the Oxford (kg no) race. We compare the model with estimates of linkage disequilibrium and cline shape made from field data.     

The complex hybrid zone between the Abisko and Sidensjö chromosome races of Sorex araneus in Sweden

Six chromosome races of the common shrew occur in Sweden, each with its characteristic arm combination of metacentric chromosomes. G-banded karyotypes were analysed from 201 common shrews in 14 localities of the northern hybrid zone in Sweden. Analyses from another 64 shrews from seven localities outside the hybrid zone w ere included for comparison. The shrews were classified with respect to karyotype into any of five categories: (1) Abisko race, (2) Sidensjö race, (3) hybrids between the parental races, (4) pseudohybrids (a type of hybrid), and (5) AT with all race-specific chromosomes (h, i, n, o, p, r) present as telocentrics. Hybrids occurred at a frequency close to Hardy-Weinberg expectation in the centre of the hybrid zone. Chromosome polymorphism of Robertsonian type was common and 43 different karyotypes were found among the specimens studied. The polymorphism involved six metacentric pairs in the Abisko and three in the Sidensjö race. The frequency of the Sidensjö race-specific metacentric hi decreased and the frequency of the Abisko race-specific hn increased from south-west to north-east along a transect across the hybrid zone. The number of race-specific telocentrics reached a peak 13 km north-east of the hi-hn cline centre. The estimated standardized cline width for chromosomes hi and hn was 16.0 km. The extension of the Sidensjö race is comparatively narrow [c. 50 km in the region of the investigation), and it is regarded to be a 'hybrid race' between the Uppsala race, which colonized Sweden from the south-west, and the Abisko race which arrived from the north-east after the most recent glaciation. The origin of the Sidensjö race is thus less than 10 000 years old, because earlier this area was covered by glacial ice.     

Morphometric variation of the common shrew (Sorex araneus) in Britain, in relation to karyotype and geography

A multivariate study of variation in mandible dimensions was conducted to determine whether common shrews of different karyotypic race (Aberdeen, Oxford, Hermitage) in Britain differ in morphology. Differences between samples from north and south Britain suggest that geography is more important than karyotype as a morphological determinant. However, the distinctiveness of hybrids in the 'Oxford-Hermitage' hybrid zone raises the possibility that there are genetic differences between the races.     

Cytogenetic control of a hybrid zone of between two Sorex araneus chromosome races before breeding season

Two chromosome races of common shrew, Moscow and Seliger, differ in the arm combination in 11 diagnostic chromosomes (Robertsonian metacentrics/acrocentrics). Homozygotes of both pure races, simple Robertsonian heterozygotes of Seliger race, and complex heterozygotes (FI hybrids) were detected in the found earlier between hybrid zone of these races, in the spring before the breeding seasonbreeding season. The g/oheterozygote was first discovered in race Seliger, whose chromosome formula typically contains acrocentrics g and o. The m/q heterozygote was recorded for the second time. Meiosis was studied in 16 males representing five detected karyotypic categories. No abnormal in pairing of homologs in either sex trivalent common for the species (XY1Y2) or autosome trivalents (g/o and m/q) was detected at diakinesis--metaphase I. Two hybrids displayed a theoretically expected and unimpaired meiotic configuration in a form of a very long chain comprising 11 monobrachial homologs (g/gm/mq/qp/pr/rk/ki/ih/hn/no/o). The results are discussed in terms of hypotheses on fertility of complex heterozygotes and limited gene flow in hybrid zone.     

Cytogenetic control of a hybrid zone between two <Emphasis Type="Italic">Sorex araneus</Emphasis> chromosome races before breeding season

Two chromosome races of common shrew, Moscow and Seliger, differ in the arm combination in 11 diagnostic chromosomes (Robertsonian metacentrics/acrocentrics). Homozygotes of both pure races, simple Robertsonian heterozygotes of Seliger race, and complex heterozygotes (F₁ hybrids) were detected in the found earlier hybrid zone of these races, in the spring before the breeding season. The g/o heterozygote was first discovered in race Seliger, whose chromosome formula typically contains acrocentrics g and o. The m/q heterozygote was recorded for the second time. Meiosis was studied in 16 males representing five detected karyotypic categories. No abnormal in pairing of homologs in either sex trivalent common for the species (XY1Y2) or autosome trivalents (g/o and m/q) was detected at diakinesis-metaphase I. Two hybrids displayed a theoretically expected and unimpaired meiotic configuration in a form of a very long chain comprising 11 monobrachial homologs (g/gm/mq/qp/pr/rk/ki/ih/hn/no/o). The results are discussed in terms of hypotheses on fertility of complex heterozygotes and limited gene flow in hybrid zone.     

Meiotic studies of Robertsonian heterozygotes from natural populations of the common shrew, Sorex araneus L

Adult male common shrews, both Robertsonian heterozygotes and homozygotes, were collected from Oxford and elsewhere in Britain. In both simple Robertsonian heterozygotes and Robertsonian heterozygotes with monobrachial homology, regular chain configurations were observed at meiosis I; only 1-2% were incomplete such that univalents were observed. On the average, there was one chiasma per chromosome arm among those that displayed Robertsonian variation, including both chain configurations and bivalents. According to one hypothesis, a single chiasma per chromosome arm may facilitate proper disjunction of chain trivalents of simple Robertsonian heterozygotes. Based on metaphase II counts, anaphase I nondisjunction frequency can be estimated as 1.0% per heterozygous individual and 0.7% per heterozygous arm combination.     

High diversity of centric fusions with monobrachial homology in an area of chromosomal polymorphism of Mus musculus domesticus

One of the simplest models of chromosomal speciation is speciation by monobrachial centric fusion. This model is based on the assumption that a sterility barrier can develop between populations, in which fixed centric fusions show monobrachial homology, i.e. share only one chromosome arm. However, studies aimed at delineating intermediate stages of transition to reproductive isolation are lacking. In this paper, we describe a new area of chromosomal polymorphism in the house mouse, Mus musculus domesticus Schwarz and Schwarx, 1943, in Sicily (Italy). We trapped 79 mice at eighteen localities in an area of approximately 500 Km² surrounding the largest active European volcano, Mount Etna. Combining G‐banding and chromosome painting we identified twelve different Robertsonian (Rb) metacentrics. Considering the high number of Rb fusions, some of them shared with other documented areas, the presently studied area of chromosomal polymorphism is very likely to represent a mixture of allochthonous and autochthonous Rb fusions. The Rb(9.16) is the most widespread metacentric (overall frequency 0.80). Two Rb metacentrics, Rb(4.10) and Rb(5.6), have similar overall frequency, 0.29 and 0.37, respectively, and are narrowly co‐distributed in ten populations. Nine fusions – Rb(2.13), Rb(1.3), Rb(12.17), Rb(8.17), Rb(2.14), Rb(10.14), Rb(11.17), Rb(3.15), and Rb(11.14) – show a low frequency (0.04–0.01) and mostly non‐overlapping localization, but each of them shares monobrachial homology with at least one other metacentric. The overall geographical distribution of different Rb fusions seems to match an early stage of race formation. The eventual role of the presently studied hybrid zone in the context of chromosomal speciation by monobrachial centric fusions is discussed. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 722–731.     

GENETIC DIFFERENTIATION OF POLISH POPULATIONS OF SOREX ARANEUS L. III. INTERCHROMOSOMAL RECOMBINATION IN A HYBRID ZONE

Two parapatric chromosomal races of the common shrew (Sorex araneus) in Poland differ in their complement of metacentric arm combinations: hk, io, gr, nm (race IV), and hi, ko, gm, np (race II). In hybrids, these eight race-diagnostic metacentrics form two randomly segregating complexes. The first complex (C₁) occurs in the form of a ring configuration ok/kh/hi/io, or a chain o/ok/kh/hi/i (when there is Robertsonian polymorphism of the element io). The second complex (C₂) always takes the form of a six-element chain configuration r/rg/gm/mn/np/p. The C₂ complex may be shortened to five or even four elements, when acrocentrics g, m and n are present. In the contact zone we found shrews of pure races (race II or IV), as well as hybrids with C₁ or C₂ complexes, and recombinants hi, ko, gr, nm. Complex heterozygotes are likely to suffer reduced fertility due to malsegregation at meiosis. However, the C₁ hybrids with ring configurations occur with a high frequency throughout the contact zone. This suggest that their fitness is only slightly lowered relative to pure race individuals, in contrast to the hybrids with C₁ or C₂ chain configurations, which presumably have a more heavily reduced fertility. On the other hand, at the center of the zone there is a high proportion of recombinants, which, being chromosomal homozygotes, should display normal meiotic segregation. Furthermore, the high frequencies of recombinants within the contact zone should facilitate gene flow between the races. The occurrence of recombinants plays a similar role as the appearance of the maximum frequencies of acrocentric homozygotes described in several contact zones of S. araneus.     

NewSorex araneus karyotypes from Germany and the postglacial recolonization of central Europe

New G-banded karyotypes from populations of the common shrew Sorex araneus Linnaeus, 1758 provide a clearer picture of the distribution of chromosome races in central Europe. As expected according to their occurrence in neighbouring countries, the Jutland (kq, no), Laska (k/o) and Drnholec (ko, nr) races are also found in Germany. A new chromosome race “Rügen” (kq) is described from this Baltic Island. Together with the previously recorded races Ulm and Mooswald (kr), six chromosome races are now known from Germany. The resulting distribution pattern is characterized by high frequencies of different race-specific metacentrics at the periphery of the country and clines with decreasing frequencies towards the centre which is occupied by the Ulm race. This race is acrocentric for all chromosome arms involved in the observed race-specific fusions and represents a buffer between the surrounding, more metacentric races. According to the present distribution of these metacentrics, a scenario for the postglacial recolonization of central Europe by S.araneus populations on three different routes is proposed: from the east along the northern slopes of the Carpathian Arc, from the south-east along the Danube Valley and from the south-west through the Upper Rhine Valley.     

Meiotic drive favors Robertsonian metacentric chromosomes in the common shrew (Sorex araneus, Insectivora, mammalia)

Meiotic drive has attracted much interest because it concerns the robustness of Mendelian segregation and its genetic and evolutionary stability. We studied chromosomal meiotic drive in the common shrew (Sorex araneus, Insectivora, Mammalia), which exhibits one of the most remarkable chromosomal polymorphisms within mammalian species. The open question of the evolutionary success of metacentric chromosomes (Robertsonian fusions) versus acrocentrics in the common shrew prompted us to test whether a segregation distortion in favor of metacentrics is present in female and/or male meiosis. Performing crosses under controlled laboratory conditions with animals from natural populations, we found a clear trend toward a segregation distortion in favor of metacentrics during male meiosis, two chromosome combinations (gm and jl) being significantly preferred over their acrocentric homologs. Apart for one Robertsonian fusion (hi), this trend was absent in female meiosis. We propose a model based on recombination events between twin acrocentrics to explain the difference in transmission ratios of the same metacentric in different sexes and unequal drive of particular metacentrics in the same sex. Pooled data for female and male meiosis revealed a trend toward stronger segregation distortion for larger metacentrics. This is partially in agreement with the frequency of metacentrics occurring in natural populations of a chromosome race showing a high degree of chromosomal polymorphism.     

A hybrid zone between the Kirillov and Petchora chromosomal races of the common shrew (Sorex araneus L., 1758) in northeastern European Russia: a preliminary description

Karyotypes of the Petchora and Kirillov chromosomal races of the common shrew differ by six Robertsonian metacentrics with monobrachial homology, such that interracial F₁ hybrids produce a ring-of-six configuration at meiosis I and are expected to suffer infertility. Mapping of 52 karyotyped individuals by using a unique global positioning system (GPS) revealed that the Kirillov-Petchora hybrid zone is positioned close to the river Mezen, which separated these races, and so may limit the migration of shrews across the contact zone. Although the population density of shrews was found to be markedly different with respect to habitats, the zone runs through a mosaic of habitats that are similar for both the Petchora and the Kirillov sides. This is one of the narrowest chromosomal hybrid zones among those studied in Sorex araneus with a standard cline width of about 1 km. The center of the cline is located on a bank occupied by the Petchora race at a distance of 0.4 km away from a riverine barrier. Interestingly, both the Kirillov race and hybrid individuals were found on a small island in the middle of a river fully flooded each spring. The frequencies of karyotypic variants allow us to consider the zone as an example of a bimodal zone. New Robertsonian and de novo whole-arm reciprocal translocations (WART) chromosomal variants found in the zone could be regarded as evidences of current evolutionary process in chromosomal hybrid zones.     

Nondisjunction frequencies in Robertsonian heterozygotes from natural populations of the common shrew, Sorex araneus L

Pregnant female common shrews were collected from an area of Robertsonian polymorphism, involving five different arm combinations, around Oxford (England). The females and their fetuses were karyotyped, and the karyotypes of the sires were deduced. Ten pregnancies where at least one parent was known to be either a single or double Robertsonian heterozygote were available for analysis. From these pregnancies, upper and lower estimates of anaphase I nondisjunction arising from Robertsonian heterozygosity were calculated to be 1.0-2.5% per heterozygous arm combination and 1.5-3.7% per heterozygous parent. One trisomic fetus with retarded development was identified. This trisomy can be attributed to anaphase I nondisjunction of a trivalent in a female Robertsonian heterozygote.     

Natural hybridization between extremely divergent chromosomal races of the common shrew (Sorex araneus, Soricidae, Soricomorpha): hybrid zone in European Russia

The Moscow and Seliger chromosomal races of the common shrew differ by Robertsonian fusions and possibly whole‐arm reciprocal translocations (WARTs) such that their F₁ hybrids produce a chain‐of‐eleven configuration at meiosis I and are expected to suffer substantial infertility. Of numerous hybrid zones that have been described in the common shrew, those between the Moscow and Seliger races involve the greatest chromosomal difference. We collected 211 individuals from this zone to generate a total dataset of 298 individuals from 187 unique global positioning system (GPS) locations within the vicinity of interracial contact. We used a geographic information system (GIS) to map the location of the hybrid zone, which follows a direct route between two lakes, as would be anticipated from tension zone theory. Even within the central area of the hybrid zone, there is a much higher frequency of pure race individuals than hybrid, making this a clear example of a bimodal zone in the sense of Jiggins & Mallet (2000) . The zone runs through good habitat for common shrews, but nevertheless it is very narrow (standard cline widths: 3–4 km), as would be anticipated from low hybrid fitness. There is clear potential for an interruption to gene flow and build‐up of reproductive isolation. As found in some other hybrid zones, there is a high frequency of novel genetic variants, in this case, new chromosomal rearrangements. Here, we report a de novo Robertsonian fission and a de novo reciprocal translocation, both for the first time in the common shrew. There is an extraordinarily high frequency of de novo mutations recorded in F₁ hybrids in the zone and we discuss how chromosomal instability may be associated with such hybrids. The occurrence of a de novo Robertsonian fission is of considerable significance because it provides missing evidence that fissions are the basis of the novel acrocentric forms found and apparently selected for in certain common shrew hybrid zones.     

The role of chromosome rearrangements in evolution of mole voles of genus Ellobius (Rodentia, Mammalia)

Modern mole voles of the genus Ellobius are characterized by species-specific features of autosomes and sex chromosomes. Owing to the use of the Zoo-FISH method, the nomenclature of chromosomes was refined and nonhomologous Robertsonian translocations indistinguishable by G-staining were identified for Ellobius tancrei, which is a species with a wide chromosome variation of the Robertsonian type. The electron-microscopic analysis of synaptonemal complexes in F1 hybrids of forms with 2n = 50 and 2n = 48 revealed the formation of a closed SC-pentavalent composed of three metacentrics with monobrachial homology and two acrocentrics. Segregation of chromosomes of such complex systems is impeded by disturbances in the nucleus architecture leding to the formation of unbalanced gametes and to a dramatic reduction in fertility of hybrids. Our data support the hypothesis that the formation of monobrachial homologous metacentric chromosomes can be considered as a way of chromosomal speciation.     

B chromosomes and Robertsonian fusions of Dichroplus pratensis (Acrididae): intraspecific support for the centromeric drive theory

We tested the centromeric drive theory of karyotypic evolution in the grasshopper Dichroplus pratensis, which is simultaneously polymorphic for eight Robertsonian fusions and two classes of B chromosomes. A logistic regression analysis performed on 53 natural populations from Argentina revealed that B chromosomes are more probably found in populations with a higher proportion of acrocentric chromosomes, as the theory predicts. Furthermore, frequencies of B-carrying individuals are significantly negatively correlated with the mean frequency of different Robertsonian fusions per individual. No significant correlations between presence/absence or frequency of Bs, and latitude or altitude of the sampled populations, were found. We thus provide the first intraspecific evidence supporting the centromeric drive theory in relation to the establishment of B chromosomes in natural populations.     

The role of chromosome rearrangements in the evolution of mole voles of the genus Ellobius (Rodentia,Mammalia)

Modern mole voles of the genus Ellobius are characterized by species-specific features of autosomes and sex chromosomes. Owing to the use of the Zoo-FISH method, the nomenclature of chromosomes was refined and nonhomologous Robertsonian translocations indistinguishable by G-staining were identified for Ellobius tancrei, which is a species with a wide chromosome variation of the Robertsonian type. The electron-microscopic analysis of synaptonemal complexes in F₁ hybrids of forms with 2n = 50 and 2n = 48 revealed the formation of a closed SC-pentavalent composed of three metacentrics with monobrachial homology and two acrocentrics. Segregation of chromosomes of such complex systems is impeded by disturbances in the nucleus architecture leading to the formation of unbalanced gametes and to a dramatic reduction in fertility of hybrids. Our data support the hypothesis that the formation of monobrachial homologous metacentric chromosomes can be considered as a way of chromosomal speciation.     

Chromosomal introgression in house mice from the hybrid zone between M. m. domesticus and M. m. musculus in Denmark

The recent discovery of Robertsonian (Rb) translocations in Danish mice from the hybrid zone between Mus musculus musculus and M. m. domesticus stimulated the chromosomal analysis of populations along a north-south transect through this zone. G-Banding identified the Rb fusions as Rb(3.8), Rb(2.5) and Rb(6.9). The cytogenetic results show that there is a gradual decrease in the number of fusions as one proceeds north, the translocations abruptly ending in populations from the centre of the hybrid zone determined by seven diagnostic allozymic markers. These results indicate that Rb fusions are present only in domesticus or predominantly domesticus-genotype mice and that they do not introgress into M. m. musculus . To test if genie incompatibilities between the musculus genetic background and Rb fusions were involved in the systematic elimination of the latter, predominantly musculus mice from the hybrid zone were crossed with Rb domesticus mice carrying Rb(3.8). The karyotypic analysis of the progeny showed no distortion of the transmission ratio of this fusion.
The chromosomal and allozymic analysis of these mice further indicates that (i) recombination is not suppressed between metacentrics and their acrocentric homologues and (ii) specific domesticus chromosomal segments are tolerated in the musculus genomes whereas the Rb centromeres are not.     

Chromosome polymorphism and C-banding variation of the brachypterous grasshopper Podisma sapporensis Shir. (Orthoptera, Acrididae) in Hokkaido, northern Japan

The grasshopper Podisma sapporensis consists of two main chromosome races in Hokkaido. The western group of populations of P. sapporensis, belonging to the XO race, has a diploid number of chromosomes 2n = 23 in the male and 2n = 24 in the female (sex determination XO male/XX female). The eastern group of populations of this species, belonging to the XY race, differs from the western one as a result of Robertsonian translocation between the originally acrocentric X chromosome and M5 autosome in homozygous state, having resulted in the forming of chromosome sex determination neo-XY male/neo-XX female (2n = 22). These races are geographically isolated by the mountainous system consisting of the Mts Daisetsu and Hidaka range, occupying the central part of the island. The hybrid zones between the races have not so far been discovered. Various levels of polymorphism for the pericentric inversions and C-banding variation exist in different chromosomes throughout populations in both chromosome races. In some solitary populations (the population at the summit of Mt Yotei, populations in the vicinity of Naganuma, Oketo, and Tanno) pericentric inversions are fixed in some pairs of chromosomes, which enables marking of the discrete karyomorphes. In the Mt Daisengen population all chromosomes are two-armed as a result of fixing the pericentric inversions. These facts contradict karyotypical conservatism of the tribe Podismini. The level of diversity of P. sapporensis karyotypes could provide a new perspective on the evolutionary process of different karyotype in Orthoptera. The considerable occurrence of polymorphism in chromosomes suggests that karyotypic diversification is undergoing in P. sapporensis. The authors also proposed that P. sapporensis would be divided into four chromosome subraces in the XO chromosome race and two chromosome subraces in the XY race, on the basis of karyotypic features. These races may have been established by fundamental climatic changes during the glacial epoch.     

Restricted gene flow at specific parts of the shrew genome in chromosomal hybrid zones

The species and races of the shrews of the Sorex araneus group exhibit a broad range of chromosomal polymorphisms. European taxa of this group are parapatric and form contact or hybrid zones that span an extraordinary variety of situations, ranging from absolute genetic isolation to almost free gene flow. This variety seems to depend for a large part on the chromosome composition of populations, which are primarily differentiated by various Robertsonian fusions of a subset of acrocentric chromosomes. Previous studies suggested that chromosomal rearrangements play a causative role in the speciation process. In such models, gene flow should be more restricted for markers on chromosomes involved in rearrangements than on chromosomes common in both parent species. In the present study, we address the possibility of such differential gene flow in the context of two genetically very similar but karyotypically different hybrid zones between species of the S. araneus group using microsatellite loci mapped to the chromosome arm level. Interspecific genetic structure across rearranged chromosomes was in general larger than across common chromosomes. However, the difference between the two classes of chromosomes was only significant in the hybrid zone where the complexity of hybrids is expected to be larger. These differences did not distinguish populations within species. Therefore, the rearranged chromosomes appear to affect the reproductive barrier between karyotypic species, although the strength of this effect depends on the complexity of the hybrids produced.