Fixation of metacentric chromosomes in populations of the common shrew Sorex araneus L. from populations of Eastern Europe

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.     

Limited Introgression between Rock-Wallabies with Extensive Chromosomal Rearrangements

Chromosome rearrangements can result in the rapid evolution of hybrid incompatibilities. Robertsonian fusions, particularly those with monobrachial homology, can drive reproductive isolation amongst recently diverged taxa. The recent radiation of rock-wallabies (genus Petrogale) is an important model to explore the role of Robertsonian fusions in speciation. Here, we pursue that goal using an extensive sampling of populations and genomes of Petrogale from north-eastern Australia. In contrast to previous assessments using mitochondrial DNA or nuclear microsatellite loci, genomic data are able to separate the most closely related species and to resolve their divergence histories. Both phylogenetic and population genetic analyses indicate introgression between two species that differ by a single Robertsonian fusion. Based on the available data, there is also evidence for introgression between two species which share complex chromosomal rearrangements. However, the remaining results show no consistent signature of introgression amongst species pairs and where evident, indicate generally low introgression overall. X-linked loci have elevated divergence compared with autosomal loci indicating a potential role for genic evolution to produce reproductive isolation in concert with chromosome change. Our results highlight the value of genome scale data in evaluating the role of Robertsonian fusions and structural variation in divergence, speciation, and patterns of molecular evolution.     

Identification of a novel WART-like chromosome rearrangement in complex heterozygotes in an interracial hybrid zone of the common shrew Sorex araneus L.

Karyotypes uncharacteristic of pure races or hybrids were identified in the interracial hybrid zones of the common shrew Sorex araneus L. that were recently discovered in the European part of Russia. This suggests the actual existence in natural populations of WART-like rearrangements (whole-arm reciprocal trans-ocations) along with Robertsonian fusions of acrocentrics. Demonstration of new and still rare chromosome variants is the aim of this communication.     

The non-random occurrence of Robertsonian fusion in the house mouse

Chromosomal rearrangements such as Robertsonian (Rb) fusions constitute a major phenomenon in the evolution of genome organization in a wide range of organisms. Although proximate mechanisms for the formation of Rb fusion are now well identified, the evolutionary forces that drive chromosomal evolution remain poorly understood. In the house mouse, numerous chromosomal races occur in nature, each defined by a unique combination of Rb fusions. Among the 106 different Rb fusions that were reported from natural populations, the low involvement of chromosome 19 in Rb fusions is striking, prompting the question of the randomness of chromosomal involvement in Rb fusions. We uncover a significant quadratic relationship between chromosome size and probability of fusing, which has never previously been in this species. It appears that fusions involving chromosome 19 are not particularly infrequent, given the expected low fusion probability associated with the chromosome's size. The results are discussed, assessing selective processes or constraints that may operate on chromosome size.     

Identification of a novel WART-like chromosome rearrangement in complex heterozygotes in an interracial hybrid zone of the common shrew Sorex araneus L

Karyotypes uncharacteristic of pure races or hybrids were identified in the interracial hybrid zones of the common shrew Sorex araneus L. that were recently discovered in the European part of Russia. This suggests the actual existence in natural populations of WART-like rearrangements (whole-arm reciprocal translocations) along with Robertsonian fusions of acrocentrics. Demonstration of new and still rare chromosome variants is the aim of this communication.     

Gene flow despite complex Robertsonian fusions among rock-wallaby (Petrogale) species

Complex Robertsonian rearrangements, with shared arms in different fusions, are expected to prevent gene flow between hybrids through missegregation during meiosis. Here, we estimate gene flow between recently diverged and chromosomally diverse rock-wallabies (Petrogale) to test for this form of chromosomal speciation. Contrary to expectations, we observe relatively high admixture among species with complex fusions. Our results reinforce the need to consider alternative roles of chromosome change, together with genic divergence, in driving speciation.     

Chromosomal evolution in Cervidae

On the basis of chromosome data obtained on 30 species and 20 subspecies of Cervidae, a report is submitted on the karyosystematics of this family. The primitive karyotype of Cervidae may be inferred to be composed of 35 acrocentric pairs (2n = 70 FN = 70). During the phyletic evolution of this family different types of chromosome rearrangements were probably selected and the group may have differentiated karyologically into three branches: (1) the Cervinae that fixed a centric fusion resulting in a metacentric pair of autosomes (2n = 68, FN = 70), as shown by the basic karyotype of Cervus elaphus, and where Robertsonian fusions are the preeminent type of chromosome rearrangement; (2) the Odocoileinae, in which pericentric inversions and Robertsonian fusions were favored, yielding first a submetacentric X and then a submetacentric autosome pair. The most representative karyotype is 2n = 70, FN = 74--as in Odocoileus hemionus; and (3) the Muntiacinae, in which centric and tandem fusions were the most common chromosome rearrangements. While Muntiacus reevesi has a karyotype 2n = 46, FN = 46, the chromosome number drops down to 2n = 6 in the females of the M. muntjak vaginalis subspecies group and M. rooseveltorum. Therefore, while the karyotypes are conserved within the subfamilies Cervinae and Odocoileinae; the subfamily Muntiacinae appears to be the most chromosomally diversified group. The few karyological data on the Moschus berezovskii suggest that the Moschinae should be placed in a separate family, the Moschidae.     

Synapsis in Robertsonian heterozygotes and homozygotes of Dichroplus pratensis (Melanoplinae, Acrididae) and its relationship with chiasma patterns

Dichroplus pratensis has a complex system of Robertsonian rearrangements with central-marginal distribution; marginal populations are standard telocentric. Standard bivalents show a proximal-distal chiasma pattern in both sexes. In Robertsonian individuals a redistribution of chiasmata occurs: proximal chiasmata are suppressed in fusion trivalents and bivalents which usually display a single distal chiasma per chromosome arm. In this paper we studied the synaptic patterns of homologous chromosomes at prophase I of different Robertsonian status in order to find a mechanistic explanation for the observed phenomenon of redistribution of chiasmata. Synaptonemal complexes of males with different karyotypes were analysed by transmission electron microscopy in surface-spread preparations. The study of zygotene and early pachytene nuclei revealed that in the former, pericentromeric regions are the last to synapse in Robertsonian trivalents and bivalents and normally remain asynaptic at pachytene in the case of trivalents, but complete pairing in bivalents. Telocentric (standard) bivalents usually show complete synapsis at pachytene, but different degrees of interstitial asynapsis during zygotene, suggesting that synapsis starts in opposite (centromeric and distal) ends. The sequential nature of synapsis in the three types of configuration is directly related to their patterns of chiasma localisation at diplotene-metaphase I, and strongly supports our previous idea that Rb fusions instantly produce a redistribution of chiasmata towards chromosome ends by reducing the early pairing regions (which pair first, remain paired longer and thus would have a higher probability of forming chiasmata) from four to two (independently of the heterozygous or homozygous status of the fusion). Pericentromeric regions would pair the last, thus chiasma formation is strongly reduced in these areas contrary to what occurs in telocentric bivalents.     

The role of the Robertsonian rearrangements in the origin of the XX/XY1Y2 sex chromosome system and in the chromosomal differentiation in Harttia species (Siluriformes, Loricariidae)

Harttia is a genus of the subfamily Loricariinae that posses a broad chromosomal variation. In addition to interspecific karyotype diversity within this group, a multiple sex chromosome system, XX/XY₁Y₂, has been described for Harttia carvalhoi. Thus, this study aimed to determine the role of chromosomal rearrangements in karyotype differentiation in Harttia by classical and molecular cytogenetic procedures. The results show that Robertsonian rearrangements have a prominent role in the chromosomal diversification of the species analysed, which initially leads to hypothesize a diploid number reduction in Harttia torrenticola and H. carvalhoi. The metacentric chromosome 1, shared between H. torrenticola and H. carvalhoi, could have originated from centric fusions from the ancestral karyotype. A centric fission event associated with the first metacentric pair allowed for the origination of a multiple sex chromosome system XX/XY₁Y₂, specific to H. carvalhoi. This study highlights the relevance of Robertsonian rearrangements in karyotypic differentiation of the species studied and demonstrates that the occurrence of a centric fission, as opposed to a previously hypothesised chromosome fusion, is directly implicated in the origin of the sex chromosome system of H. carvalhoi.     

Identification of uniparental disomy following prenatal detection of Robertsonian translocations and isochromosomes

Rearrangements of the acrocentric chromosomes (Robertsonian translocations and isochromosomes) are associated with an increased risk of aneuploidy. Given this, and the large number of reported cases of uniparental disomy (UPD) associated with an acrocentric rearrangement, carriers are presumed to be at risk for UPD. However, an accurate risk estimate for UPD associated with these rearrangements is lacking. A total of 174 prenatally identified acrocentric rearrangements, including both Robertsonian translocations and isochromosomes, were studied prospectively to identify UPD for the chromosomes involved in the rearrangements. The overall goal of the study was to provide an estimate of the risk of UPD associated with nonhomologous Robertsonian translocations and homologous acrocentric rearrangements. Of the 168 nonhomologous Robertsonian translocations studied, one showed UPD for chromosome 13, providing a risk estimate of 0.6%. Four of the six homologous acrocentric rearrangements showed UPD, providing a risk estimate of 66%. These cases have also allowed delineation of the mechanisms involved in producing UPD unique to Robertsonian translocations. Given the relatively high risk for UPD in prenatally identified Robertsonian translocations and isochromosomes, UPD testing should be considered, especially for cases involving the acrocentric chromosomes 14 and 15, in which UPD is associated with adverse clinical outcomes.     

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.     

Comparative cytogenetics of six Indo‐Pacific moray eels (Anguilliformes: Muraenidae) by chromosomal banding and fluorescence in situ hybridization

A comparative cytogenetic analysis, using both conventional staining techniques and fluorescence in situ hybridization, of six Indo‐Pacific moray eels from three different genera (Gymnothorax fimbriatus, Gymnothorax flavimarginatus, Gymnothorax javanicus, Gymnothorax undulatus, Echidna nebulosa and Gymnomuraena zebra), was carried out to investigate the chromosomal differentiation in the family Muraenidae. Four species displayed a diploid chromosome number 2n = 42, which is common among the Muraenidae. Two other species, G. javanicus and G. flavimarginatus, were characterized by different chromosome numbers (2n = 40 and 2n = 36). For most species, a large amount of constitutive heterochromatin was detected in the chromosomes, with species‐specific C‐banding patterns that enabled pairing of the homologous chromosomes. In all species, the major ribosomal genes were localized in the guanine‐cytosine‐rich region of one chromosome pair, but in different chromosomal locations. The (TTAGGG)_n telomeric sequences were mapped onto chromosomal ends in all muraenid species studied. The comparison of the results derived from this study with those available in the literature confirms a substantial conservation of the diploid chromosome number in the Muraenidae and supports the hypothesis that rearrangements have occurred that have diversified their karyotypes. Furthermore, the finding of two species with different diploid chromosome numbers suggests that additional chromosomal rearrangements, such as Robertsonian fusions, have occurred in the karyotype evolution of the Muraenidae.     

Autosomal rearrangements in Graomys griseoflavus (Rodentia): a model of non-random Robertsonian divergence

The south American rodent Graomys griseoflavus exhibits a remarkable chromosome polymorphism as a consequence of four Robertsonian fusions. Focusing on the genetic analysis of the taxon, genome organization of all karyomorphs was studied at chromosome and molecular organization level. Cytogenetic (G, NOR and Re banding) and molecular (satellite and mitochondrial DNAs) events accompanying chromosome divergence allowed tracing a phylogenetic relationship among all karyomorphs. Available data led to propose that chromosome evolution of G. griseoflavus occurred in a non-random sequence of centric fusions, supporting the hypothesis of single origin for Robertsonian karyomorphs.     

Relationship between the study of DNA reassociation kinetics of various chromosomal forms of Ellobius and questions concerning the pathways of chromosome rearrangement during evolution

Fifteen chromosome forms of Ellobius talpinus (from 2n = 31 to 2n = 54) were found in the small area in the Pamirs. Low-chromosome karyotypes evolved from 54-chromosomal ancestral form by Robertsonia centric fusions. The DNA reassociation kinetics of 34- and 54-chromosome forms of E. talpinus have been studied. For comparison DNA of E. lutescens (2n = 17) the karyotype of which seems to have arisen from 54-chromosome ancestor by Robertsonian and other types rearrangements was examined. Reassociation profiles of Ellobius DNA suggest the existence of several repeated sequences families with different frequences of repetitions. The reassociation curves of DNA from 34- and 54-chromosome forms were identical. These data indicate absence of changes in DNA molecular organization during the evolution of E. talpinus karyotypes by Robertsonian fusions. Comparative analysis of DNA reassociation kinetics of E. talpinus and E. lutescens showed identical characteristics of highly repeated sequences and of one from the three intermediate fractions, however Cot 1/2, complexity and repetitive frequencies of two intermediate fractions of E. talpinus and E. lutescens were different. It is possible that non-robertsonian rearrangements of E. lutescens karyotype affected only intermediate repetitions. The alternative explanation of these data is a simple divergence of repeated sequences during the evolution of E. lutescens DNA.     

A new case of rob(14;17) in cattle

Robertsonian translocations, also called centric fusions, represent the most frequent chromosome anomalies in cattle, and rob(1;29) is the most widespread. However, centric fusions involving other chromosomes have been discovered in different cattle breeds. Here we report the appearance of a new case of rob(14;17) in an Italian cattle breed more than ten years after the first and only case had been observed, and we demonstrate the independent origin of this anomaly from the previous case.     

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.     

Mutation rates of structural chromosome rearrangements in man.

The gametic mutation rates of human structural chromosome rearrangements have been estimated from rearrangements ascertained from systematic surveys of live births and spontaneous abortions. The mutation rates for rearrangements that survive long enough to give rise to clinically recognized pregnancies are 2.20 X 10(-4) for balanced rearrangements, 3.54 X 10(-4) for unbalanced Robertsonian translocations, and 3.42 X 10(-4) for unbalanced non-Robertsonian rearrangements. These estimates give a mutation rate for all detectable structural chromosome rearrangements of approximately 1 X 10(-3). The most common single rearrangement, the Robertsonian translocation involving chromosomes 13 and 14, has a mutation rate of 1.5 X 10(-4).     

Genic differentiation and origin of Robertsonian populations of the house mouse (Mus musculus domesticus Rutty)

This paper examines the relation between chromosomal and nuclear-gene divergence in 28 wild populations of the house mouse semi-species, Mus musculus domesticus, in Western Europe and North Africa. Besides describing the karyotypes of 15 of these populations and comparing them to those of 13 populations for which such information was already known, it reports the results of an electrophoretic survey of proteins encoded by 34 nuclear loci in all 28 populations. Karyotypic variation in this taxon involves only centric (or Robertsonian) fusions which often differ in arm combination and number between chromosomal races. The electrophoretic analysis showed that the amount of genic variation within Robertsonian (Rb) populations was similar to that for all-acrocentric populations, i.e. bearing the standard karyotype. Moreover, divergence between the two types of populations was extremely low. These results imply that centric fusions in mice have not modified either the level or the nature of genic variability. The genetic similarity between Rb and all-acrocentric populations is not attributed to the persistence of gene flow, since multiple fusions cause marked reproductive isolation. Rather, we attribute this extreme similarity to the very recent origin of chromosomal races in Europe. Furthermore, genic diversity measures suggest that geographically separated Rb populations have in situ and independent origins. Thus, Rb translocations are probably not unique events, but originated repeatedly. Two models are presented to explain how the rapid fixation of a series of chromosomal rearrangements can occur in a population without lowering variability in the nuclear genes. The first model assumes that chromosomal mutation rates are between 10(-3) and 10(-4) and that populations underwent a series of transient bottlenecks in which the effective population size did not fall below 35. In the second model, genic variability is restored following severe bottlenecks, through gene flow and recombination.     

Karyotype differentiation in Chromaphyosemion killifishes (Cyprinodontiformes, Nothobranchiidae). II: cytogenetic and mitochondrial DNA analyses demonstrate karyotype differentiation and its evolutionary direction in C. riggenbachi

African killifishes of the genus Chromaphyosemion show a high degree of phenotypic and karyotypic diversity. The latter is especially pronounced in C. riggenbachi, a morphologically defined species restricted to a small distribution area in Cameroon. This study presents a detailed reconstruction of karyotype differentiation within C. riggenbachi using conventional Giemsa staining and sequential chromosome banding as well as a phylogenetic analysis based on part of the mitochondrial (mt) cytochrome b gene from eleven populations. The cytogenetic analysis revealed differences in chromosome morphology, banding patterns and/or diploid chromosome number (2n) among all populations examined. Diploid number ranged from 2n = 20 to 2n = 36 and varied mainly among populations, while C-banding patterns and NOR phenotypes showed fixed differences among populations as well as some variability within populations. The mtDNA analysis disclosed five clearly differentiated haplotype groups. Mapping the karyotype data onto the mtDNA dendrogram revealed a decrease in 2n from the most basal to the most derived groups, thus demonstrating a reduction of 2n during their evolutionary history. Our results indicate that karyotype differentiation involved Robertsonian fusions as well as non-Robertsonian processes. Causes of the high karyotypic variability may include an elevated chromosomal mutation rate as well as certain features of the ecology and mating system that could facilitate the fixation of chromosomal rearrangements. The pattern of karyotype and haplotype differentiation and the results of previous crossing experiments suggest incipient speciation in C. riggenbachi.     

Robertsonian polymorphism in plaice, Pleuronectes platessa L., and cod, Gadus morhua L., (Pisces Pleuronectiformes and Gadiformes)

Karyotypic analysis of plaice, Pleuronectes platessa L., and cod, Gadus morhua L., revealed that the chromosome numbers in both species vary but that chromosome arm numbers (NF) stay constant. The C-, Q- and R-banding patterns also confirmed that the population of plaice studied shows Robertsonian polymorphism. The tendency of reduction in chromosome number in fishes suggests that Robertsonian fusions play a role in karyotype evolution in fishes.