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.     

Distribution of genetic variability in populations of two chromosomal races of Dichroplus pratensis (Melanoplinae, Acrididae) and their hybrid zone

We examined, through allozyme electrophoresis, the genetic structure of populations of the acridid grasshopper Dichroplus pratensis from two chromosomal races (Northern and Southern) and their hybrid zone in Argentina. No fixed alleles for any particular race were found, although genetic differentiation among parental races was significant (0 = 0.044, 95% CI: 0.004-0.068). Hybrid populations are genetically more similar to the Southern race (0 = 0.008, 95% CI: -0.005-0.018) than to Northern ones (0 = 0.018, 95% CI: 0.002-0.030). Differential viability or fertility of hybrids, or asymmetry in mating preferences in favour of one particular cross would cause a higher proportion of matings between hybrid individuals and those from the Southern race. This would explain the high genetic similarity between those groups, in spite of their geographical vicinity with northern race populations.     

Studies of mitochondrial DNA,allozyme and morphometric variation in a house mouse hybrid zone

An unusual chromosomal hybrid zone of the house mouse, Mus musculus domesticus, exists in Upper Valtellina, Northern Italy, consisting of four Robertsonian (Rb) races and the standard (all-acrocentric, or 2n = 40) race, all hybridizing freely within 10 km2. The hybrid zone in Valtellina provides an excellent opportunity to study the role of Rb fusions in reproductive isolation and speciation. This hybrid zone has already been well studied for the distribution of Rb fusions and the fertility of hybrids, but in order to understand the dynamics of the zone, a basic understanding of the origin and genetic similarity of the chromosomal races is necessary. This paper presents the results of three different methods of measuring genetic differentiation: multivariate analysis of morphological traits and analyses of allozyme variation and mitochondrial DNA sequences. The standard race is clearly distinguishable from the three Rb races by all three methods, but the Rb races are not distinguishable from one another. This provides strong evidence for our previous suggestions that the well-established Rb races in Valtellina are closely related, and that the standard race was introduced into the valley more recently from a distant source. The fact that the Rb races are indistinguishable is also consistent with our hypothesis that a within-village speciation event involving two of the races (Hauffe & Searle, 1992) was a recent occurrence. The low level of allozyme heterozygosity among the Rb races suggests that these populations are the products of at least one bottleneck. The present article substantially extends earlier studies and provides the first detailed morphological and molecular analysis of this complex hybrid zone.     

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.     

REDUCED GENE FLOW AT PERICENTROMERIC LOCI IN A HYBRID ZONE INVOLVING CHROMOSOMAL RACES OF THE HOUSE MOUSE MUS MUSCULUS DOMESTICUS

The West European house mouse, Mus musculus domesticus, is a particularly suitable model to investigate the role of chromosomal rearrangements in reproductive isolation. In fact, it exhibits a broad range of chromosomal polymorphism due to Robertsonian (Rb) fusions leading to various types of contact zones between different chromosomal races. In the present study, we analyzed a parapatric contact in central Italy between the Cittaducale chromosomal race (CD: 2n= 22) and the surrounding populations with standard karyotype (2n= 40) to understand if Rb fusions play a causative role in speciation. One hundred forty‐seven mice from 17 localities were genotyped by means of 12 microsatellite loci. A telomeric and a pericentromeric locus situated on six chromosome arms (four Rbs and one telocentric) were selected to detect differences in the amount of gene flow for each locus in different chromosomal positions. The analyses performed on the two subsets of loci show differences in the level of gene flow, which is more restricted near the centromeres of Rb chromosomes. This effect is less pronounced in the homozygotes populations settled at the border of the hybrid zone. We discuss the possible cause of the differential porosity of gene flow in Rbs considering “hybrid dysfunctions” and “suppressed recombination” models.     

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.     

Spatio-temporal variation in the structure of a chromosomal polymorphism zone in the house mouse

Several long-term temporal analyses of the structure of Robertsonian (Rb) hybrid zones in the western house mouse, Mus musculus domesticus, have been performed. Nevertheless, the detection of gradual or very rapid variations in a zone may be overlooked when the time elapsed between periods of study is too long. The Barcelona chromosomal polymorphism zone of the house mouse covers about 5000, km(2) around the city of Barcelona and is surrounded by 40 chromosome telocentric populations. Seven different metacentrics and mice with diploid numbers between 27 and 40 chromosomes and several fusions in heterozygous state (from one to seven) have been reported. We compare the present (period 2008-2010) and past (period 1996-2000) structure of this zone before examining its dynamics in more detail. Results indicate that there is not a Rb race in this area, which is consistent with the proposal that this zone was probably originated in situ, under a primary intergradation scenario. The lack of individuals with more than five metacentrics in heterozygous state in the current period suggests that selection acted against such mice. By contrast, this situation did not occur for mice with fewer than five fusions in heterozygous condition. Changes in human activity may affect the dynamics of gene flow between subpopulations, thus altering the chromosomal composition of certain sites. Although these local variations may have modified the clinal trend for certain metacentrics, the general staggered structure of the zone has not varied significantly in a decade.     

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.     

Staggered clines in a hybrid zone between two chromosome races of the harvestman Gagrellopsis nodulifera (Arachnida: Opiliones)

We analyzed a hybrid zone between two chromosome races (2n = 16 and 2n = 22) of a Japanese harvestman, Gagrellopsis nodulifera Sato and Suzuki (Arachnida: Opiliones: Phalangiidae). The hybrid zone is located in the eastern part of Tottori Prefecture, western Honshu. The width of the zone is approximately 5 to 15 km. Three independent tandem fusions/fissions seem to be the main cause of the karyotypic differences between the parental races. Ten karyotypic variants were found in the hybrid zone. They differed by numbers of diploid chromosomes and trivalents detected in meiosis. In most of the collecting sites, karyotypic heterozygotes were less common than expected. A positive correlation was found between number of trivalents in a karyotype and its deficiency rate. In some sites, the deficit of heterozygous individuals was accompanied by an excess of the intermediate homozygotes. One of the three transects across the zone was studied in detail. We found that three types of single heterozygotes (2n = 17, 2n = 19 and 2n = 21) formed a series of successive, spatially separated peaks along the transect. Two types of intermediate homozygotes (2n = 18 and 2n = 20) were also spatially separated. The most parsimonious explanation of such a structure is the staggering of clines of three tandem (or Robertsonian) fusion/fission variants that differentiate the parental races caused by selection against multiple heterozygotes. Analysis of nondisjunction in single heterozygotes demonstrated that there was a strong interindividual variation in nondisjunction rate. The mean frequency of aneuploid MII in single heterozygotes was 0.10 +/- 0.03. Crossover exchanges in some critical regions of trivalents result in abnormal chromosomal configurations: chromosomes with unequal chromatids and dicentric chromosomes. Frequency of crossover-induced chromosomal abnormalities was low in single heterozygotes (approximately equal to 4%), and was unexpectedly high in the double heterozygotes (approximately equal to 15%). Selection against karyotypic heterozygotes is considered as a main evolutionary force responsible for the structuring of the hybrid zone. A positive association between diploid chromosome number and altitude was found. The race 2n = 16 tended to occupy lower altitudes than the 2n = 22 parental race. Differences in ecological preferences may be a result of previous adaptations to different environments in allopatry. A hypothesis concerning the origin and evolution of the hybrid zone is proposed.     

Does divergence from normal patterns of integration increase as chromosomal fusions increase in number? A test on a house mouse hybrid zone

Chromosomal evolution is widely considered an important driver of speciation because it can promote the establishment of reproductive barriers. Karyotypic reorganization is also expected to affect the mean phenotype, as well as its development and patterns of phenotypic integration, through processes such as variation in genetic linkage between quantitative trait loci or between regulatory regions and their targets. Here we explore the relationship between chromosomal evolution and phenotypic integration by analyzing a well-known house mouse parapatric contact zone between a highly derived Robertsonian (Rb) race (2n = 22) and populations with standard karyotype (2n = 40). Populations with hybrid karyotypes are scattered throughout the hybrid zone connecting the two parental races. Using mandible shape data and geometric morphometrics, we test the hypothesis that patterns of integration progressively diverge from the “normal” integration pattern observed in the standard race as they accumulate Rb fusions. We find that the main pattern of integration observed between the posterior and anterior part of the mandible can be largely attributed to allometry. We find no support for a gradual increase in divergence from normal patterns of integration as fusions accumulate. Surprisingly, however, we find that the derived Rb race (2n = 22) has a distinct allometric trajectory compared with the standard race. Our results suggest that either individual fusions disproportionately affect patterns of integration or that there are mechanisms which “purge” extreme variants in hybrids (e.g. reduced fitness of hybrid shape).     

Rb(7.17), a rare Robertsonian fusion in wild populations of the house mouse

Robertsonian (Rb) translocation is the largest source of chromosomal diversity in the western European house mouse (Mus musculus domesticus). Recently, the fusion Rb(7.17) was found in the chromosomal polymorphic zone of this subspecies in the north-east of the Iberian Peninsula. This fusion has not been reported in any other European population. Here we give data on the distribution and frequency of this mutation in this region. Results revealed that Rb(7.17) is restricted to a small geographic area, and that, in comparison with other fusions in this polymorphic zone, it occurs at low frequencies. We suggest some possible explanations for the distribution of this translocation.     

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.     

Fixation of metacentric chromosomes in eastern Europe populations of the common shrew <Emphasis Type="Italic">Sorex araneus</Emphasis> L.

In this review, we discuss the processes of fixation of Robertsonian chromosome fusions in populations of the common shrew Sorex araneus L. Various Robertsonian fusions, accumulating in populations, create an illusion of large chromosomal rearrangements, reciprocal translocations of complete chromosome arms. The use of these rearrangements for phylogenetic reconstructions results in false conclusions. Robertsonian fusions accumulate in populations at such stages of the species evolution, when large open or subdivided populations prevail (populations of warm periods of Pleistocene and many present-day populations) and are fixed in small isolated populations and glacial refugia. The formation of monomorphic chromosome races requires a long time, several glaciation epochs during the whole Pleistocene.     

Genetic analysis of a chromosomal hybrid zone in the Australian morabine grasshoppers (Vandiemenella, viatica species group)

Whether chromosomal rearrangements promote speciation by providing barriers to gene exchange between populations is one of the long-standing debates in evolutionary biology. This question can be addressed by studying patterns of gene flow and selection in hybrid zones between chromosomally diverse taxa. Here we present results of the first study of the genetic structure of a hybrid zone between chromosomal races of morabine grasshoppers Vandiemenella viatica , P24(XY) and viatica 17, on Kangaroo Island, Australia. Chromosomal and 11 nuclear markers revealed a narrow hybrid zone with strong linkage disequilibrium and heterozygote deficits, most likely maintained by a balance between dispersal and selection. Widths and positions of clines for these markers are concordant and coincident, suggesting that selection is unlikely to be concentrated on a few chromosomes. In contrast, a mitochondrial marker showed a significantly wider cline with centre offset toward the P24(XY) side. We argue that the discordance between the mitochondrial and nuclear/chromosomal clines and overall asymmetry of the clines suggest a secondary origin of the contact zone and potential movement of the zone after contact. Genome-wide scans using many genetic markers and chromosomal mapping of these markers are needed to investigate whether chromosomal differences directly reduce gene flow after secondary contact.     

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

Chromosomal races of the common shrew differ in sets of metacentric chromosomes and on contact may produce hybrids with extraordinarily complex configurations at meiosis I that are associated with reduced fertility. There is an expectation that these may be some of the most extreme tension zones available for study and therefore are of interest as potential sites for reproductive isolation. Here, we analyse one of these zones, between the Novosibirsk race (characterized by metacentrics go, hn, ik, jl, mp and qr) and the Tomsk race (metacentrics gk, hi, jl and mn and acrocentrics o, p, q and r), which form hybrids with a chain-of-nine (CIX) and a chain-of-three (CIII) configuration at meiosis I. At the Novosibirsk-Tomsk hybrid zone, the CIX chromosomes form clines of 8.53 km standardized width on average, whereas the cline for the CIII chromosomes was 52.83 km wide. The difference in these cline widths fits with the difference in meiotic errors expected with the CIX and CIII configuration, and we produce estimates of selection against hybrids with these types of configurations, which we relate to dispersal and age of the hybrid zone. The hybrid zone is located at the isocline at 200 m altitude above sea level; this relationship between the races and altitude is suggested at both coarse and fine scales. This indicates adaptive differences between the races that may in turn have been promoted by the chromosome differences. Thus, the extreme chromosomal divergence between the Novosibirsk and Tomsk may be associated with genic differentiation, but it is still striking that, despite the large chromosomal differences, reproductive isolation between the Novosibirsk and Tomsk races has not occurred.     

UNDERSTANDING THE BASIS OF DIMINISHED GENE FLOW BETWEEN HYBRIDIZING CHROMOSOME RACES OF THE HOUSE MOUSE

Speciation may be promoted in hybrid zones if there is an interruption to gene flow between the hybridizing forms. For hybridizing chromosome races of the house mouse in Valtellina (Italy), distinguished by whole‐arm chromosomal rearrangements, previous studies have shown that there is greater interruption to gene flow at the centromeres of chromosomes that differ between the races than at distal regions of the same chromosome or at the centromeres of other chromosomes. Here, by increasing the number of markers along race‐specific chromosomes, we reveal a decay in between‐race genetic differentiation from the centromere to the distal telomere. For the first time, we use simulation models to investigate the possible role of recombination suppression and hybrid breakdown in generating this pattern. We also consider epistasis and selective sweeps as explanations for isolated chromosomal regions away from the centromere showing differentiation between the races. Hybrid breakdown alone is the simplest explanation for the decay in genetic differentiation with distance from the centromere. Robertsonian fusions/whole‐arm reciprocal translocations are common chromosomal rearrangements characterizing both closely related species and races within species, and this fine‐scale empirical analysis suggests that the unfitness associated with these rearrangements in the heterozygous state may contribute to the speciation process.     

Genetic differentiation and habitat partition of Robertsonian house mouse populations (Mus musculus domesticus) of Tunisia

The karyological analysis of Tunisian populations of house mice revealed the existence of a Robertsonian (Rb) chromosomal race carrying nine pairs of metacentric chromosomes in central Tunisia. Divergence estimates showed that they are genetically differentiated from local all-acrocentric populations and have a reduced level of genic variability. The Rb populations are restricted to urban habitats, whereas all-acrocentric populations occur in rural areas. Contact zones between these two types of habitat yield chromosomally polymorphic populations. Analysis of gene flow indicates that it is reduced and limited to populations bordering the contact areas. The reduced genic variability and patchy distribution exhibited by the Tunisian Rb mice do not agree with results from previous studies of the European Rb populations. Two hypotheses are presented to account for this discrepancy based on local differentiation versus introduction of the Tunisian Rb race.     

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.     

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.