Monobrachial Homology Research Articles

Natural male hybrid common shrews with a very long chromosomal multivalent at meiosis appear not to be completely sterile.

Among 36 known chromosomal hybrid zones of the common shrew Sorex araneus, the Moscow-Seliger hybrid zone is of special interest because inter-racial complex heterozygotes (F1 hybrids) produce the longest meiotic configuration, consisting of 11 chromosomes with monobrachial homology (undecavalent or chain-of-eleven: CXI). Different studies suggest that such a multivalent may negatively affect meiotic progression and in general should significantly reduce fertility of hybrids. In this work, by immunocytochemical and electron microscopy methods, we investigated for the first time chromosome synapsis, recombination and meiotic silencing in pachytene spermatocytes of natural inter-racial heterozygous shrew males carrying CXI configurations. Despite some abnormalities detected in spermatocytes, such as associations of chromosomes, stretched centromeres, and the absence of recombination nodules in some arms of the multivalent, a large number of morphologically normal spermatozoa were observed. Possible low stringency of pachytene checkpoints may mean that even very long meiotic configurations do not cause complete sterility of such complex inter-racial heterozygotes.

Сhannelized Karyotype Evolution of the Common Shrew <i>Sorex araneus</i> (Mammalia)

A model of channelized evolution of the S. araneus L. karyotype in the processes of replacement of ten pairs of acrocentric chromosomes by five pairs of metacentric chromosomes has been proposed. The channelized evolution of the karyotype arises due to the inability of Rb fusions with incomplete (monobrachial) homology to spread in the same population. Therefore, an Rb fusion, due to some random event first appearing in a population, largely determines the further evolution of the karyotype of that population. After the third replacement of acrocentric chromosomes by metacentric ones, the replacement of the remaining 6 pairs of acrocentrics allows the formation of no more than three karyotypes with five diagnostic metacentrics, which can be predicted, regardless of which rearrangements result in metacentric chromosomes (Rb fusion or WART). The channelized karyotypic evolution greatly increases the likelihood of parallel karyotype formation, in cases where evolution begins with identical metacentrics in geographically distant populations. An example of parallel evolution that began with the gk metacentric is the identical karyotypes of the new Mogilev race from Belarus and the Tomsk race from Western Siberia. The evolution of Eastern European chromosomal races shows hybrid fusion processes between the karyotypes of the East European karyotypic group (EEKG) and the West European karyotypic group (WEKG).

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.

Notable homologous variation in chromosomal races of the common shrew.

This paper is a review of the rare phenomenon of chromosome intraspecies variation manifested in monobrachial homology series in the comprehensively investigated karyotype of the common shrew Sorex araneus Linnaeus, 1758 (Eulipotyphla, Mammalia). The detailed dataset on the account of this mammalian species was drawn from the recently published monograph by Searle et al. (2019) “Shrews, Chromosomes and Speciation”. The parallels to the law of homologous series in variation by Nikolai Vavilov are discussed.

Chromosome Translocations as a Driver of Diversification in Mole Voles Ellobius (Rodentia, Mammalia).

The involvement of chromosome changes in the initial steps of speciation is controversial. Here we examine diversification trends within the mole voles Ellobius, a group of subterranean rodents. The first description of their chromosome variability was published almost 40 years ago. Studying the G-band structure of chromosomes in numerous individuals revealed subsequent homologous, step-by-step, Robertsonian translocations, which changed diploid numbers from 54 to 30. Here we used a molecular cytogenetic strategy which demonstrates that chromosomal translocations are not always homologous; consequently, karyotypes with the same diploid number can carry different combinations of metacentrics. We further showed that at least three chromosomal forms with 2n = 34 and distinct metacentrics inhabit the Pamir-Alay mountains. Each of these forms independently hybridized with E. tancrei, 2n = 54, forming separate hybrid zones. The chromosomal variations correlate slightly with geographic barriers. Additionally, we confirmed that the emergence of partial or monobrachial homology appeared to be a strong barrier for hybridization in nature, in contradistinction to experiments which we reported earlier. We discuss the possibility of whole arm reciprocal translocations for mole voles. Our findings suggest that chromosomal translocations lead to diversification and speciation.

Hybrid Zone between the Sok and Serov Chromosomal Races of the Common Shrew Sorex araneus (Lipotyphla, Mammalia) in European Russia

Analysis of the frequencies of karyotypic variants in the hybrid zone between the Sok and Serov chromosomal races of the common shrew Sorex araneus revealed that the zone has a complex configuration. A large part of the contact zone is located in a monotonous mid taiga zone, where there are no significant barriers to limit dispersion of shrews. Another part of the zone runs along the Pechora River (Komi Republic). Analysis of distribution of the diagnostic chromosomes on a transect along the Pechora River showed that the hybrid zone could be described by opposing metacentric clines. Individuals of both pure Sok and Serov races, as well as F1 hybrids, were found only on the left bank of the Pechora River. The right bank was occupied only by the Serov race, and F1 hybrids were rare there. The observed number of interracial hybrids in the center of the zone does not differ from that expected in the case of random breeding. This allows us to define this zone as unimodal. The standard width of the zone is about 40 km. This is considerably higher than all known cases of hybrid zones with the same level of karyotypic differences between parental races: two pairs of diagnostic metacentric chromosomes with monobrachial homology. We discuss possible causes of this phenomenon.

Chromosome Synapsis and Recombination in Male Hybrids between Two Chromosome Races of the Common Shrew (Sorex araneus L., Soricidae, Eulipotyphla).

Hybrid zones between chromosome races of the common shrew (Sorex araneus) provide exceptional models to study the potential role of chromosome rearrangements in the initial steps of speciation. The Novosibirsk and Tomsk races differ by a series of Robertsonian fusions with monobrachial homology. They form a narrow hybrid zone and generate hybrids with both simple (chain of three chromosomes) and complex (chain of eight or nine) synaptic configurations. Using immunolocalisation of the meiotic proteins, we examined chromosome pairing and recombination in males from the hybrid zone. Homozygotes and simple heterozygotes for Robertsonian fusions showed a low frequency of synaptic aberrations (<10%). The carriers of complex synaptic configurations showed multiple pairing abnormalities, which might lead to reduced fertility. The recombination frequency in the proximal regions of most chromosomes of all karyotypes was much lower than in the other regions. The strong suppression of recombination in the pericentromeric regions and co-segregation of race specific chromosomes involved in the long chains would be expected to lead to linkage disequilibrium between genes located there. Genic differentiation, together with the high frequency of pairing aberrations in male carriers of the long chains, might contribute to maintenance of the narrow hybrid zone.

Analysis of meiotic chromosome structure and behavior in Robertsonian heterozygotes of Ellobius tancrei (Rodentia, Cricetidae): a case of monobrachial homology.

Synaptonemal complex (SC) chains were revealed in semisterile intraspecific F1 hybrids of Ellobius tancrei Blasius, 1884 (2n = 49, NF=56 and 2n=50, NF=56), heterozygous for Robertsonian (Rb) translocations. Chains were formed by Rb submetacentrics with monobrachial homology. Chromosome synapsis in spermatocytes of these hybrids was disturbed, apparently because of the problematic release of the chromosomes from the SC chains. These hybrids suffer from low fertility, and our data support the opinion that this is because a formation of Rb metacentrics with monobrachial homology within different races of the same species might be an initial event for the divergence of chromosomal forms.

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.

Synaptonemal complex analysis of interracial hybrids between the Moscow and Neroosa chromosomal races of the common shrew Sorex araneus showing regular formation of a complex meiotic configuration (ring-of-four).

Immunocytochemical and electron microscopic analysis of synaptonemal complexes (SCs) was carried out for the first time in homozygotes and complex Robertsonian heterozygotes (hybrids) of the common shrew, Sorex araneus Linnaeus, 1758, from a newly discovered hybrid zone between the Moscow and the Neroosa chromosomal races. These races differ in four monobrachial homologous metacentrics, and closed SC tetravalent is expected to be formed in meiosis of a hybrid. Indeed, such a multivalent was found at meiotic prophase I in hybrids. Interactions between multivalent and both autosomes and/or the sex chromosomes were observed. For the first time we have used immunocytochemical techniques to analyse asynapsis in Sorex araneus and show that the multivalent pairs in an orderly fashion with complete synapsis. Despite some signs of spermatocytes arrested in the meiotic prophase I, hybrids had large number of active sperm. Thus, Moscow – Neroosa hybrid males that form a ring-of-four meiotic configuration are most likely not sterile. Our results support previous demonstrations that monobrachial homology of metacentrics of the common shrew does not lead to complete reproductive isolation between parapatric chromosomal races of the species.

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 Km 2 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. ADDITIONAL KEYWORDS: chromosomal speciation – chromosome races – Mus musculus domesticus – population cytogenetics – Robertsonian metacentrics – structural heterozygotes.

New data on the evolution of the Cretan spiny mouse, Acomys minous (Rodentia: Murinae), shed light on the phylogenetic relationships in the cahirinus group

The karyotype of the Cretan spiny mouse Acomys minous was examined with chromosome banding techniques in 53 individuals from 12 localities of Crete, aiming to gain a more detailed knowledge on the chromosomal constitution and variability of its natural populations. We found that it consists of three Robertsonian (Rb) populations with 2n = 38, 2n = 40 and 2n = 42, respectively, the last one being reported for the first time, and with stable fundamental number (FNa = 66, FN = 68). The G-banding pattern proves that the Rb populations are closely linked phylogenetically by the many common Rb fusions and the lack of monobrachial homologies. In addition, they appear to freely mate at their contact areas, producing viable and fertile hybrids. No other type of chromosomal rearrangement appears to have played part in the chromosomal evolution of this species, at least in the recent past, as indicated also by the study of the telomeric sequences. Heterochromatin appears to be restricted to the pericentromeric position of all acrocentric and most biarmed autosomes, as well as of the X chromosome, whereas the Y chromosome is uniformly, yet faintly heterochromatic. Chromosome banding comparison of the karyotypes in A. minous with those of the other species in the cahirinus group (i.e. Acomys cahirinus, Acomys cilicicus, and Acomys nesiotes) proves their very close phylogenetic relationship, further reinforced by the study of the cytochrome b sequences, and that A. minous possesses the ancestral karyotype of the group. It is suggested that at least two of the karyotypes that characterize A. minous today, pre-existed in North Africa before it colonized Crete and that the specific status of the four members in the cahirinus group may need to be revisited. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102, 498–509.

Morphological, Genetic, and Chromosomal Variation at a Small Spatial Scale within a Mosaic Hybrid Zone of the Grasshopper Dichroplus pratensis Bruner (Acrididae)

Hybrid zones are regions where genetically different populations meet and mate, resulting in offspring of mixed characteristics. In organisms with limited dispersal, such as melanopline grasshoppers, hybrid zones can occur at small spatial scales (i.e., <500 m). We assessed levels of morphological, chromosomal, and molecular variability in adult males of the grasshopper Dichroplus pratensis Bruner (N = 137 males, 188 females) collected at 12 sites within a mosaic hybrid zone in a heterogeneous environment in Sierra de la Ventana, Argentina. In this hybrid zone, 2 Robertsonian chromosomal races, polymorphic for different centric fusions, meet (the "Northern race" at low altitudes and the "Southern race" at higher altitudes), forming hybrids that show monobrachial homologies during meiosis. High morphometric variation in 6 traits was revealed among grasshoppers of both sexes, with male body size positively and significantly correlated with increasing altitude. Frequency of Robertsonian fusions characteristic of the Southern race increased significantly with altitude. Moreover, fusion frequencies covaried between samples. Considerable genetic variation was revealed by random amplification of polymorphic DNA markers, with heterozygosity ranging from 0.3477 to 0.3745. Insects from low-altitude and high-altitude populations showed significant genetic differentiation, as indicated by F(ST) values. The proposed model for D. pratensis, involving the generation and maintenance by chromosomal fusions, of gene complexes adaptive in different environments, could explain the observed clinal patterns within the contact zone.

Selection against Robertsonian fusions involving housekeeping genes in the house mouse: integrating data from gene expression arrays and chromosome evolution

Monobrachial homology resulting from Robertsonian (Rb) fusions is thought to contribute to chromosomal speciation through underdominance. Given the karyotypic diversity characterizing wild house mouse populations [Mus musculus domesticus, (MMU)], variation that results almost exclusively from Rb fusions (diploid numbers range from 22 to 40) and possibly whole arm reciprocal translocations (WARTs), this organism represents an excellent model for testing hypotheses of chromosomal evolution. Previous studies of chromosome size and recombination rates have failed to explain the bias for certain chromosomes to be involved more frequently than others in these rearrangements. Here, we show that the pericentromeric region of one such chromosome, MMU19, which is infrequently encountered as a fusion partner in wild populations, is significantly enriched for housekeeping genes when compared to other chromosomes in the genome. These data suggest that there is selection against breakpoints in the pericentromeric region and provide new insights into factors that constrain chromosomal reorganizations in house mice. Given the anticipated increase in vertebrate whole genome sequences, the examination of gene content and expression profiles of the pericentromeric regions of other mammalian lineages characterized by Rb fusions (i.e., other rodents, bats, and bovids, among others) is both achievable and crucial to developing broadly applicable models of chromosome evolution.

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 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.

Spermatogenesis in house mouse in a Robertsonian polymorphism zone

Robertsonian (Rb) translocations can be important in speciation as a mechanism of postzygotic isolation between populations. Meiotic non-disjunction, gametogenic impairment, and association of impaired autosomal segments with sex chromosomes have been postulated as mechanisms responsible for reducing fertility in Rb mice. Quantitative histological studies needed to understand the role of Rb fusions in gametogenic impairment are scarce. Most research on Rb mice has analyzed meiotic non-disjunction of laboratory and wild-derived strains, which have complex or simple structural heterozygosity with large numbers of fusions. Using histological multilevel sampling, we examined spermatogenesis in mice from the Rb polymorphism area of Barcelona. We studied four chromosomal groups having: a) one Rb heterozygote fusion and 2n=39, b) one Rb heterozygote fusion and 2n=31, c) three Rb heterozygote fusions without monobrachial homology and with diploid number ranging from 2n=29 to 2n=37, and d) only Rb homozygote fusions with diploid number ranging from 2n=28 to 2n=30. Standard mice from the area surrounding the Rb zone were used as control. We analyzed morphological variables of the testes, relative frequency of stages in the seminiferous epithelium cycle, the 'round spermatids:primary spermatocytes' ratio, and other derived parameters. Our results reveal that structural homozygote mice and simple heterozygote mice having as few as one to three Rb fusions undergo greater germ cell death (GCD) than standard mice, suggesting that Rb fusions are related to increased GCD (in both the heterozygous and homozygous state) and may be the main cause of decreased gene flow between mice populations from this area.

Possible involvement of whole-arm reciprocal translocations (WARTs) in the evolution of a Mus musculus domesticus Robertsonian system from Greece

The evolution of the Robertsonian (Rb) system of the house mouse (Mus musculus domesticus) located in Peloponnisos (Greece) is examined, under the possibility of whole arm reciprocal translocation (WART) involvement in the formation process of two of its Rb races with 2n = 24 and 2n = 28, respectively, characterized by monobrachial homology. Our contribution reinforces the opinion that WARTs may have been more actively involved in the formation of Rb races in this subspecies than previously thought. Moreover, the consideration of WARTs, when studying complex Rb systems permits the suggestion of more sensible and parsimonial pathways for their phylogenetic history than when WARTs are excluded.

How did the platypus get its sex chromosome chain? A comparison of meiotic multiples and sex chromosomes in plants and animals

The duck-billed platypus is an extraordinary mammal. Its chromosome complement is no less extraordinary, for it includes a system in which ten sex chromosomes form an extensive meiotic chain in males. Such meiotic multiples are unprecedented in vertebrates but occur sporadically in plant and invertebrate species. In this paper, we review the evolution and formation of meiotic multiples in plants and invertebrates to try to gain insights into the origin of the platypus meiotic multiple. We describe the meiotic hurdles that translocated mammalian chromosomes face, which make longer chains disadvantageous in mammals, and we discuss how sex chromosomes and dosage compensation might have affected the evolution of sex-linked meiotic multiples. We conclude that the evolutionary conservation of the chain in monotremes, the structural properties of the translocated chromosomes and the highly accurate segregation at meiosis make the platypus system remarkably different from meiotic multiples in other species. We discuss alternative evolutionary models, which fall broadly into two categories: either the chain is the result of a sequence of translocation events from an ancestral pair of sex chromosomes (Model I) or the entire chain came into being at once by hybridization of two populations with different chromosomal rearrangements sharing monobrachial homology (Model II).

EPISODIC CHROMOSOMAL EVOLUTION IN PLANIPAPILLUS (ONYCHOPHORA: PERIPATOPSIDAE): A PHYLOGENETIC APPROACH TO EVOLUTIONARY DYNAMICS AND SPECIATION

Planipapillus, a clade of onychophorans from southeastern Australia, exhibits substantial chromosomal variation. In the context of a robust phylogeny based on nuclear and mitochondrial sequence data, we evaluate models of chromosomal evolution and speciation that differ in the roles assigned to selection, mutation, and drift. Permutation tests suggest that all chromosome rearrangements in the clade have been centric fusions and, on the basis of parsimony and maximum-likelihood methods with independent estimates of branch lengths, we conclude that at least 31 centric fusions have been fixed in Planipapillus. A likelihood-ratio test approach, which is independent of our point estimates of ancestral states, rejects an evolutionary model in which the mutation rate is constant and centric fusions are effectively neutral. In contrast to the nucleotide sequence data, which are consistent with neutrality and rate constancy, centric fusions in Planipapillus are underdominant, spontaneous fusion rates vary among lineages, or both. We predict an inverse relationship between rates of chromosomal evolution and historical population size. Chromosomal evolution may play a role in speciation in Planipapillus, both by interactions between centric fusions with monobrachial homology and by the accumulation of multiple weakly underdominant fusions.

EPISODIC CHROMOSOMAL EVOLUTION IN PLANIPAPILLUS (ONYCHOPHORA: PERIPATOPSIDAE): A PHYLOGENETIC APPROACH TO EVOLUTIONARY DYNAMICS AND SPECIATION

Planipapillus, a clade of onychophorans from southeastern Australia, exhibits substantial chromosomal variation. In the context of a robust phylogeny based on nuclear and mitochondrial sequence data, we evaluate models of chromosomal evolution and speciation that differ in the roles assigned to selection, mutation, and drift. Permutation tests suggest that all chromosome rearrangements in the clade have been centric fusions and, on the basis of parsimony and maximum-likelihood methods with independent estimates of branch lengths, we conclude that at least 31 centric fusions have been fixed in Planipapillus. A likelihood-ratio test approach, which is independent of our point estimates of ancestral states, rejects an evolutionary model in which the mutation rate is constant and centric fusions are effectively neutral. In contrast to the nucleotide sequence data, which are consistent with neutrality and rate constancy, centric fusions in Planipapillus are underdominant, spontaneous fusion rates vary among lineages, or both. We predict an inverse relationship between rates of chromosomal evolution and historical population size. Chromosomal evolution may play a role in speciation in Planipapillus, both by interactions between centric fusions with monobrachial homology and by the accumulation of multiple weakly underdominant fusions.Corresponding Editor: J. Huelsenbeck