Non-Sciuromorph rodent karyotypes in evolution.

Rodents are, taxonomically, the most species-rich mammalian order. They display a series of special genomic features including the highest karyotypic diversity, frequent occurrence of complex intraspecies chromosome variability, and a variety of unusual chromosomal sex determination mechanisms not encountered in other mammalian taxa. Rodents also have an abundance of cytochemically heterogeneous heterochromatin. There are also instances of extremely rapid karyotype reorganization and speciation not accompanied by significant genetic differentiation. All these peculiarities make it clear that a detailed study of rodent genomic evolution is indispensable to understand the mode and tempo of mammalian evolution. The aim of this review is to update the data obtained by classical and molecular cytogenetics as well as comparative genomics in order to outline the range of old and emerging problems that remain to be resolved.

Karyotype reorganisation in the subtilis group of birch mice (Rodentia, Dipodidae, Sicista): unexpected taxonomic diversity within a limited distribution.

Conventional cytogenetic studies of Sicista subtilis and S. severtzovi (Dipodidae, Sicistinae), both attributable to the subtilis group of birch mice, revealed extensive karyotype diversity with 2n = 16-26 and NFa values of 26-46 indicating the overwhelming non-Robertsonian nature of chromosomal reorganization in these species. The numerical and structural chromosome variability was principally found in specimens located within a confined region of the East European (Russian) Plain. The approximately 135,000-km(2) area occurs in the vicinity of the Don River bend between 49°13'N/43°46'E and 51°32'N/36°16'E. The detection of cytotypes sharing similar 2n and NF values, but having morphologically distinct chromosomes, suggests that these may result from polymorphisms present both within recognized species and in cryptic taxa not hitherto described. We conducted a comprehensive, comparative chromosome banding analysis of 52 birch mice (21 localities) referable to the subtilis group and report the presence of 5 distinct karyotypes, each characterized by a combination of stable, variable, and partly overlapping 2n/NFa values. These karyotypes differed from each other by 10-29 structural chromosomal rearrangements (18.1 ± 6.3) that comprised Rb fusions/fissions (42.2%), pericentric inversions (31.1%), and tandem translocations (22.2%). The composition, and the high numbers of these chromosomal changes, is likely to provide an effective means of post-mating isolation, suggesting that taxonomic diversity within the subtilis group is larger than currently accepted. Additionally, we report the frequent fixation of tandem translocations in sample populations, one of which was found in a polymorphic state representing, as far as we are aware, the first case of an in statu nascendi tandem fusion in wild populations. Moreover, our data revealed that bi-armed chromosomes were involved in fusions detected in some of the subtilis taxa. In each instance, however, fusions were preceded by pericentric inversions that transform one or both bi-armed chromosomes into acrocentrics resulting in either centromere-telomere or Robertsonian translocations. Finally, a phylogenetic scenario inferred from a cladistic analysis of the chromosomal data suggests that the extensive karyotypic diversification within the subtilis group in the south-east region of the Russian Plain most likely results from fragmentation of a continuously distributed, ancestral population. It is thought that this occurred at the last glacial maximum (18,000-14,000 years B.P.), and that the process of isolation has been exacerbated by increasing human activity in the region in modern times.

Karyotype evolution of eulipotyphla (insectivora): the genome homology of seven sorex species revealed by comparative chromosome painting and banding data.

The genus Sorex is one of the most successful genera of Eulipotyphla. Species of this genus are characterized by a striking chromosome variability including XY1Y2 sex chromosome systems and exceptional chromosomal polymorphisms within and between populations. To study chromosomal evolution of the genus in detail, we performed cross-species chromosome painting of 7 Sorex species with S. granarius and S. araneus whole-chromosome probes and found that the tundra shrew S. tundrensis has the most rearranged karyotype among these. We reconstructed robust phylogeny of the genus Sorex based on revealed conserved chromosomal segments and syntenic associations. About 16 rearrangements led to formation of 2 major Palearctic groups after their divergence from the common ancestor: the S. araneus group (10 fusions and 1 fission) and the S. minutus group (5 fusions). Further chromosomal evolution of the 12 species inside the groups, including 5 previously investigated species, was accompanied by multiple reshuffling events: 39 fusions, 20 centromere shifts and 10 fissions. The rate of chromosomal exchanges upon formation of the genus was close to the average rate for eutherians, but increased during recent (about 6-3 million years ago) speciation within Sorex. We propose that a plausible ancestral Sorex karyotype consists of 56 elements. It underwent 20 chromosome rearrangements from the boreoeutherian ancestor, with 14 chromosomes retaining the conserved state. The set of genus-specific chromosome signatures was drawn from the human (HSA)-shrew comparative map (HSA3/12/22, 8/19/3/21, 2/13, 3/18, 11/17, 12/15 and 1/12/22). The syntenic association HSA4/20, that was previously proposed as a common trait of all Eulipotyphla species, is shown here to be an apomorphic trait of S. araneus.

Cross-species chromosome painting corroborates microchromosome fusion during karyotype evolution of birds.

The stone curlew, also known as thick-knee (Burhinus oedicnemus, BOE), represents a phylogenetically young species of the shorebirds (Charadriiformes) that exhibits one of the most atypical genome organizations known within the class of Aves, due to an extremely low diploid number (2n = 42) and only 6 pairs of microchromosomes in its complement. This distinct deviation from the 'typical' avian karyotype is attributed to repeated fusions of ancestral microchromosomes. In order to compare different species with this atypical avian karyotype and to investigate the chromosome rearrangement patterns, chromosome-specific painting probes representing the whole genome of the stone curlew were used to delineate chromosome homology between BOE and 5 species belonging to 5 different avian orders: herring gull (Charadriiformes), cockatiel (Psittaciformes), rock pigeon (Columbiformes), great gray owl (Strigiformes) and Eurasian coot (Gruiformes). Paints derived from the 20 BOE autosomes delimited 28 to 33 evolutionarily conserved segments in the karyotypes of the 5 species, similar to the number recognized by BOE paints in such a basal lineage as the chicken (28 conserved segments). This suggests a high degree of conservation in genome organization in birds. BOE paints also revealed some species-specific rearrangements. In particular, chromosomes BOE1-4 and 14, as well as to a large extent BOE5 and 6, showed conserved synteny with macrochromosomes, whereas homologous regions for BOE7-13 are found to be largely distributed on microchromosomes in the species investigated. Interestingly, the 6 pairs of BOE microchromosomes 15-20 appear to have undergone very few rearrangements in the 5 lineages investigated. Although the arrangements of BOE homologous segments on some chromosomes can be explained by complex fusions and inversions, the occurrence of homologous regions at multiple sites may point to fission of ancestral chromosomes in the karyotypes of the species investigated. However, the present results demonstrate that the ancestral microchromosomes most likely experienced fusion in the stone curlew lineage forming the medium-sized BOE chromosomes, while they have been conserved as microchromosomes in the other neoavian lineages.

Phylogenetic position of the saola (Pseudoryx nghetinhensis) inferred from cytogenetic analysis of eleven species of Bovidae.

Previous morphological and molecular analyses failed to resolve the phylogenetic position of the critically endangered saola (Pseudoryx nghetinhensis) with respect to its placement in Bovina (cattle, bison, and yak) or Bubalina (Asian and African buffaloes). In the present study, G- and C-banding, Ag-staining and FISH with 28S and telomeric probes was undertaken for 17 bovid species. An analysis of these data allowed us to identify 49 structural rearrangements that included autosomes, gonosomes and 17 different NOR sites. The combined data set was subjected to a cladistic analysis aimed at: (i) providing new insights on phylogenetic relationships of the saola and other species within the subfamily Bovinae, and (ii) testing the suitability of different classes of chromosomal characters for phylogenetic reconstruction of the family Bovidae. The study revealed that nucleolar organizing regions (NORs) are phylogenetically informative. It was shown that at least one, or sometimes two of these characters punctuate divergences that include nodes that are the most basal in the tree, to those that are the most recent. In this context, the shared presence of three NORs in saola and species of Syncerus and Bubalus strongly suggests the saola's placement within the subtribe Bubalina. This contrasts with Robertsonian rearrangements which are informative only at the generic level. These findings suggest that NORs are an important and frequently overlooked source of additional phylogenetic information within the Bovidae that may also have applicability at higher taxonomic levels, possibly even for Pecora.

Systematics and phylogeny of West African gerbils of the genus Gerbilliscus (Muridae: Gerbillinae) inferred from comparative G- and C-banding chromosomal analyses.

Comparative analysis of the G- and C-banding patterns in six morphologically similar species of the genus Gerbilliscus(G. gambianus, G. guineae, G. kempi, Gerbilliscus sp., G. robustus and G. leucogaster) and one belonging to the genus Gerbillurus (G. tytonis) from 27 West, East and South African localities was carried out. Our study revealed that 17 rearrangements comprising seven fissions, five translocations and five inversions occurred in the evolution of this group, with 1-13 rearrangements differentiating the various species. In addition the unusually large sex chromosomes appear to be species-specific as judged by size and morphology reflecting structural rearrangements as well as the variable presence of a large amount of C-heterochromatin found in each species at a particular chromosomal location. These karyotypic features allow us to recognize five distinct species in West Africa (compared to the two recognized in recent taxonomic lists) and to roughly delimit their geographical distributions. The pattern of phylogenetic relationships inferred from a cladistic analysis of the chromosomal data is in good agreement with recent molecular phylogenetic studies that recognize a West African species group within the genus Gerbilliscus, and the monophyly of both Gerbilliscus and Gerbillurus.

Unusually extensive karyotype reorganization in four congeneric Gerbillus species (Muridae: Gerbillinae).

Comparative analysis of the G- and C-banding patterns in four morphologically poorly differentiated Gerbillus species (G. pyramidum, G. perpallidus, G. tarabuli and G. occiduus) was carried out. These gerbils have similar karyotype morphology with 2n and NF equal to 38/76, 40/76, 40/78 and 40/80, respectively. Our study revealed that possibly 70 Robertsonian (Rb) fusions, two pericentric inversions, one tandem translocation and at least 13 non-identified rearrangements have occurred during the karyotypic evolution of these species. The number of chromosomal changes by which any of these species differ from each other ranges from 33 to 49. One Rb fusion was common to two of the species, with only a single autosome-gonosome translocation shared by all four, suggesting a monophyletic origin of these karyotypically highly divergent species. Based on the chromosomal data obtained here, the systematic and geographic implications for these North African species are also discussed.

Extensive gross genomic rearrangements between chicken and Old World vultures (Falconiformes: Accipitridae).

The karyotypes of most birds consist of a small number of macrochromosomes and numerous microchromosomes. Intriguingly, most accipitrids which include hawks, eagles, kites, and Old World vultures (Falconiformes) show a sharp contrast to this basic avian karyotype. They exhibit strikingly few microchromosomes and appear to have been drastically restructured during evolution. Chromosome paints specific to the chicken (GGA) macrochromosomes 1-10 were hybridized to metaphase spreads of three species of Old World vultures (Gyps rueppelli, Gyps fulvus, Gypaetus barbatus). Paints of GGA chromosomes 6-10 hybridize only to single chromosomes or large chromosome segments, illustrating the existence of high chromosome homology. In contrast, paints of the large macrochromosomes 1-5 show split hybridization signals on the chromosomes of the accipitrids, disclosing excessive chromosome rearrangements which is in clear contrast to the high degree of chromosome conservation substantiated from comparative chromosome painting in other birds. Furthermore, the GGA chromosome paint hybridization patterns reveal remarkable interchromosomal conservation among the two species of the genus Gyps.

Evolution of rRNA gene clusters and telomeric repeats during explosive genome repatterning in TATERILLUS X (Rodentia, Gerbillinae).

A survey of 28S and 5S rRNA gene clusters, and telomeric repeats was performed using single and double FISH in the Taterillus genus (Rodentia, Muridae, Gerbillinae). Taterillus was previously demonstrated to have undergone a very recent and extensive chromosomal evolution. Our FISH results demonstrate that rRNA genes can vary in location and number irrespective of the phylogenetic relationships. Telomeric repeats were detected in pericentromeric and interstitial regions of several chromosomes, thus providing nonambiguous evolutionary footprints of Robertsonian and tandem translocation events. These footprints are discussed in reference to the molecular process of these karyotypical changes. Also, examples of colocation of rDNA clusters and telomeric repeats lend support to their possible involvement in nucleolus formation. Finally, the presence of rRNA genes, and the extensive amplification of telomeric repeats at specific loci within a double X-autosome translocated element which were not observed on the homologous Y1 and Y2, served as basis for an epigenomic hypothesis on X-autosome translocation viability in mammals.

Recent radiation in West African Taterillus (Rodentia, Gerbillinae): the concerted role of chromosome and climatic changes.

West African gerbils of the genus Taterillus constitute a complex of seven sibling species distributed from sudano-guinean to saharo-sahelian regions. They display radically rearranged karyotypes despite low genic divergence and a very recent differentiation, that is, within the last 0.4 Myr for the six most derived species. We here provide a comparison of the seven specific karyotypes and perform a cladistic analysis using chromosomal rearrangements character states. When a posteriori polarized mutations were mapped onto the phylogenetic tree, 38 rearrangements were identified as fixed during the evolution of these rodents. This makes Taterillus one of the most striking examples of accelerated chromosomal evolution within placental mammals. Taking into account the types of chromosomal changes involved, divergence times between lineages, genetic distances, as well as reassessed geographic distributions, we suggest that (1) speciation in West African Taterillus was driven by chromosomal changes, and (2) the paleoclimatic oscillations of the Sahara desert have played a major role in their evolution. In particular, elevated plasticity of the Taterillus genome, as suggested by the patterns observed for some repetitive elements, would have led to a higher probability of mutation. We hypothesize that the process underpinning cladogenesis most probably involved highly underdominant genomic rearrangements that were fixed following pronounced populational bottlenecks resulting from drastic climatic and subsequent environmental changes. Major African rivers formed significant barriers to dispersal, limiting expansion during the more moist and so favorable periods. This scenario would explain the current parapatric species distributions and their relationship to the West African hydrographic features.

Low rate of genomic repatterning in Xenarthra inferred from chromosome painting data.

Comparative cytogenetic studies on Xenarthra, one of the most basal mammalian clades in the Placentalia, are virtually absent, being restricted largely to descriptions of conventional karyotypes and diploid numbers. We present a molecular cytogenetic comparison of chromosomes from the two-toed (Choloepus didactylus, 2n = 65) and three-toed sloth species (Bradypus tridactylus, 2n = 52), an anteater (Tamandua tetradactyla, 2n = 54) which, together with some data on the six-banded armadillo (Euphractus sexcinctus, 2n = 58), collectively represent all the major xenarthran lineages. Our results, based on interspecific chromosome painting using flow-sorted two-toed sloth chromosomes as painting probes, show the sloth species to be karyotypically closely related but markedly different from the anteater. We also test the synteny disruptions and segmental associations identified within Pilosa (anteaters and sloths) against the chromosomes of the six-banded armadillo as outgroup taxon. We could thus polarize the 35 non-ambiguously identified chromosomal changes characterizing the evolution of the anteater and sloth genomes and map these to a published sequence-based phylogeny for the group. These data suggest a low rate of genomic repatterning when placed in the context of divergence estimates based on molecular and fossil data. Finally, our results provide a glimpse of a likely ancestral karyotype for the extant Xenarthra, a pivotal group for understanding eutherian genome evolution.

Cytogenetic repartition of chicken CR1 sequences evidenced by PRINS in Galliformes and some other birds.

Chicken repeat 1 (CR1) belongs to the non-long repeat class of retrotransposons. Nearly 100000 repeats interspersed in the chicken genome are subdivided into at least six distinct subfamilies, each 300 bp long and all sharing substantial sequence similarity. CR1-like elements were found in genomes from invertebrates to mammals, suggesting their importance for genome structure and/or function. Moreover, numerous data support the hypothesis of their implication in regulation of gene expression. So, the chromosomal distribution of these CR1 sequences in vertebrates is of great interest to improve our knowledge about the genome structure, function and evolution. A comparison of the cytogenetic distribution of CR1 sequences was performed by PRINS using consensus chicken primers on the chromosomes of chicken and species of several bird orders: Galliformes, Anseriformes, Passeriformes and Falconiformes. The study revealed that CR1 repeats are spread over nearly all chicken chromosomes with a higher density on the macrochromosomes and in particular with hot spots on subtelomeric regions of chromosome 1, 2, 3q, 4q, 5q. Their distribution on the macrochromosomes forms a kind of banding pattern, which was not systematically matched with R- or G-banding. This banding pattern appears to be conserved on the chromosomes of the Galliformes studied, irrespective of their karyotypes, rearranged or not. CR1 primers also show similar signals on the chromosomes of birds phylogenetically more distant (Anseriformes, Passeriformes and Falconiformes). This fact confirms the importance of these sequences at the large scale of bird evolution and in the chromosomal structure. The location of CR1 sequences, and in particular of the hot spots, mainly within the richest CG areas are in conformity with the data on an epigenetic role of these highly conserved sequences.

A finding of the XX/XY1Y2 sex-chromosome system in Taterillus arenarius (Gerbillinae, Rodentia) and its phylogenetic implications.

A chromosome banding study (R- and C-bands) of a male Taterillus arenarius (Rodentia, Gerbillinae) specimen from Mauritania revealed the presence of an XX/XY1Y2 sex-chromosome system in the karyotype, as found previously in three other congeneric species. This finding allowed us to resolve the phylogenetic affinities of this species within the genus and to propose an evolutionary scenario leading to the formation of the species with an XX/XY1Y2 sex-chromosome system. A review of chromosome data in Taterillus suggests that there may be more species in the genus than hitherto recognized.

Presumptive sex chromosomes of a unisexual homomorphic species of lizards, Lepidodactylus lugubris.

Incorporation of 5-bromo-2'-deoxyuridine (BrdU) in prometaphasic chromosomes allows active from inactivated X chromosomes in female mammalian cells to be distinguished. We have applied the technique to the all-female, chromosomally homomorphic gecko Lepidodactylus lugubris. Similar differences to those obtained between the two female sex chromosomes of mammals are observed in the patterns of chromosome pair 1. It is argued that this is more likely to reflect incipient ZW heterogamety than female (XX) homogamety.

Explosive chromosome evolution and speciation in the gerbil genus Taterillus (Rodentia, Gerbillinae): a case of two new cryptic species.

The five morphologically sibling gerbil species of the genus Taterillus in West Africa were first identified from karyotypes. These species possess an XX/XY(1)Y(2) sex-chromosome system and are characterized by significant karyotypic reorganization, thus making them a suitable model for studying the role of chromosomal rearrangements in the speciation process. We present here a description of two new cytotypes, Taterillus sp. 1 and Taterillus sp. 2, from the Lake Chad area, the former having a 2n = 22/23, NFa = 40, and the latter 2n = 24/25, NFa = 44. Comparison of their G- and C- banding patterns with those of T. pygargus (2n = 22/23, NFa = 38/40), examined in an earlier paper, revealed that all three species differ from each other by 7 to 11 chromosomal rearrangements, comprising tandem translocations, pericentric inversions, and Robertsonian metacentrics displaying monobrachial homology. Meiotic configurations formed in potential hybrids among any of these three forms would consist of complex rings and chains, alone or in combination, resulting, as expected, in a significant disruption of gametogenesis. These results provide support for assigning Taterillus sp. 1 and Taterillus sp. 2 to two different biological species, which, as demonstrated by our preliminary molecular studies, would have emerged recently. Possible factors responsible for the rapid karyotypic evolution and speciation in this West African gerbil complex are discussed.

Comparative chromosome banding of two South-American species of rice rats of the genus Oligoryzomys (Rodentia, Sigmodontinae).

Comparative analysis of G- and C-banding patterns in two species of pygmy rice rats, namely Oligoryzomys microtis from Peru (Ucayali and Loreto departments) and O. flavescens from Bolivia (Tarija department) established that the diploid number of the former species is 64 (NFa = 66), whereas, in the latter, it varies between 64 and 66 (NFa = 66-68) due to the presence of 0-2 heterochromatic supernumerary or B chromosomes. The G-banding pattern of the euchromatic part of their karyotypes is similar in spite of differences in morphology of the largest and smallest autosomal pairs caused by a centromeric shift and the presence of heterochromatic arms, respectively. In addition, the total quantity of C-heterochromatin is smaller in the karyotype of O. microtis than in that of O. flavescens, resulting in differences in the number and size of chromosome pairs (including sex chromosomes) bearing C-blocks. It follows from present and previous data that these karyotypic features are stable in each of these species and thus may be used as species-specific markers.

Comparative chromosome banding analysis of three South American species of rice rats of the genus Oryzomys (Rodentia, Sigmodontinae).

Comparative G- and C-banding analysis in three species of rice rats, namely Oryzomys megacephalus from Peru and French Guiana, O. yunganus (Peru) and O. nitidus (Bolivia) was carried out. It revealed that Peruvian O. megacephalus (2N = 52, NFa = 62) and that from French Guiana (2N = 54, NFa = 64) differ from each other by one Rb translocation and one heterochromatic arm addition/deletion. Three further Rb translocations separate them from O. yunganus (2N = 58, NFa = 62). Only 16 out of 39 autosomal pairs of O. nitidus (2N = 80, NFa = 86) shared homologous banding patterns with O. yunganus, 4 of which were involved in tandem translocations to form the larger chromosomes in two other taxa. The study suggests that O. megacephalus, O. yunganus and O. laticeps studied previously form a monophyletic group in good agreement with earlier molecular and morphological data. By contrast, the limited homologous banding patterns found between them and O. nitidus cast doubt on its belonging to the same phylogenetic lineage. In the light of available chromosomal and molecular data, the significance of intra- and interspecies karyotypic variability within Oryzomys and its relevance to systematics and phylogeny of the genus are discussed.

A molecular perspective on the systematics and evolution of the genus Arvicanthis (Rodentia, Muridae): inferences from complete cytochrome b gene sequences.

Systematics of the genus Arvicanthis, the African unstriped grass rat, are somewhat controversial. Most recent taxonomic revisions list five to six species but the definition of some of these (Arvicanthis dembeensis, Arvicanthis nairobae, and Arvicanthis niloticus) is uncertain. The complete mitochondrial cytochrome b gene (1140 bp) was sequenced for 20 specimens from throughout the range of the genus to determine the intrageneric genetic structure, construct a molecular phylogeny, and evaluate classical taxonomies. Neighbor-joining and maximum parsimony analyses yielded identical phylogenetic trees that identify two major lineages: the first one (1) is composed of specimens usually referred to A. niloticus but representing several distinct species, and the other (2) is a complex including "true" A. niloticus from Egypt and northern West Africa as well as Arvicanthis abyssinicus, Arvicanthis dembeensis, and Arvicanthis somalicus. An analysis on a 357-bp fragment of the cytochrome b including published data on A. nairobae indicates that this taxon is part of clade (1). Calibration of the number of 3rd position transversion changes with the murid fossil record suggests that clades (1) and (2) diverged approximately 5 Myr ago. Arvicanthis niloticus as currently recognized is a paraphyletic association and this name should be restricted to the Egyptian and northern West African sample. We also suggest referring to A. dembeensis as A. niloticus, as our cytochrome b data do not support its recognition as a distinct species. Clade (1) is subdivided in three lineages, geographically corresponding to southern West, Central, and East Africa. The high genetic divergence detected between the Central African lineage and the other two lineages suggests that they probably represent separate species. Clade (2) experienced rapid cladogenetic events during the late Pliocene, with the A. somalicus lineage being the first to emerge, followed by the ancestor of A. abyssinicus and A. blicki. This period was characterized by significant climatic and environmental changes, such as the extension of open habitats, which might have provided a stimulus for speciation in this savanna-dwelling genus. Confrontation of our molecular results with chromosomal data shows a high degree of congruence between the two datasets.

Chromosomal evidence for a hybrid origin of diploid parthenogenetic females from the unisexual-bisexual Lepidodactylus lugubris complex (Reptilia, Gekkonidae).

Chromosome banding analysis of seven diploid parthenogenetic females from Polynesian and Southeast Asian populations of the unisexual-bisexual Lepidodactylus lugubris complex (Reptilia, Gekkonidae) showed that the unisexual karyotype consists of two different haploid sets. Similar analysis of an L. lugubris male from a bisexually reproducing population revealed two identical chromosome complements, the banding pattern generally matching that of the females, although many chromosomes were obviously different. These observations suggest that the gonochoristic males belong to a taxon related to the parthenogenetic female taxon but are not a direct ancestor of the latter. The data also offer strong evidence for a hybrid origin of diploid parthenogenetic females in L. lugubris and suggest that a high degree of chromosomal heterogeneity may be the leading reason for the evolutionary selection of a modified meiotic process in this species, allowing production of unreduced oocytes and, consequently, of a unisexual mode of reproduction.

Viability of X-autosome translocations in mammals: an epigenomic hypothesis from a rodent case-study.

X-autosome translocations are highly deleterious chromosomal rearrangements due to meiotic disruption, the effects of X-inactivation on the autosome, and the necessity of maintaining different replication timing patterns between the two segments. In spite of this, X-autosome translocations are not uncommon. We here focus on the genus Taterillus (Rodentia, Gerbillinae) which provides two sister lineages differing by two autosome-gonosome translocations. Despite the recent and dramatic chromosomal repatterning characterising these lineages, the X-autosome translocated species all display intercalary heterochromatic blocks (IHBs) between the autosomal and the ancestral sexual segments. These blocks, composed of highly amplified telomeric repeats and rDNA clusters, are not observed on the chromosomes of the non-translocated species, nor the Y1 and Y2 of the translocated species. Such IHBs are found in all mammals documented for X-autosome translocation. We propose an epigenomic hypothesis which explains the viability of X-autosome translocations in mammals. This posits that constitutive heterochromatin is probably selected for in X-autosome translocations since it may (1) prevent facultative heterochromatinization of the inactivated X from spreading to the autosomal part, and (2) allow for the independent regulation of replication timing of the sex and autosomal segments.