The B chromosomes of the grasshopper Eyprepocnemis plorans and the intragenomic conflict

The grasshopper Eyprepocnemis plorans harbours an extremely widespread polymorphism for supernumerary (B) chromosomes, which is found in almost all circum-Mediterranean and Caucasian populations hitherto analysed. B chromosomes in this species have been shown to evolve through several stages of parasitic and near-neutral nature, presumably because of an arms race between the standard (A) and B chromosomes. This intragenomic conflict can either be solved with the extinction of the neutralised B chromosome or, more interestingly, with the replacement of the neutralised B by a mutant version being parasitic again and thus prolonging B chromosome life. This species thus provides a complete view of the long-term life-cycle of parasitic B chromosomes.     

Selfish DNA and breeding system in flowering plants

In many species, some individuals carry one or more B chromosomes: extra, or supernumerary chromosomes not part of the normal complement. In most well-studied cases, Bs lower the fitness of their carrier and persist in populations only because of accumulation mechanisms analogous to meiotic drive. It has been suggested that such genomic parasites are expected to persist only in outcrossed sexual species, in which uninfected lines of descent can be continuously reinfected; in inbred or asexual species, all selection is between lines of descent, and the genomic parasites are either lost or must evolve into commensals or mutualists. Here we present a simple population genetic model of the effect of outcrossing rate on the frequency of B chromosomes, and find that outcrossing facilitates the spread of parasitic Bs, but inhibits the spread of mutualists. Data compiled from the literature on breeding system and B chromosomes of British plants indicate that Bs are much more likely to be reported from obligately outcrossed species than inbred species. These results support the ideas that most B chromosomes are parasitic, and that breeding systems play a central role in the biology of selfish genes.     

Comportement des chromosomes surnuméraires et relation avec le taux de mortalité dans une population africaine de Locusta migratoria migratorioides

Transmission of supernumerary chromosomes is studied in adults and embryos of an African population of Locusta migratoria migratorioides; 34% of the animals show one or two B chromosomes (24% one, 10% two). This percentage is the same in both sexes. During mitosis, B chromosomes are very stable. At meiosis, in some cases they show pairing, in other cases they enter as univalents. The eventuality of synapsis or association is discussed. These two kinds of behaviour could not be explained by the presence of two different B chromosomes as is shown from the study of parthenogenetic progeny. Repartition of B chromosomes in the progeny is different depending on whether the male or the female parent supplies them; so the behaviour of these supernumerary should be conditioned, not by their own structure, but by a connection with the cell. — One B chromosome apparently is neutral. When there are two B chromosomes, in case of synapsis, the number of animals with two B in the progeny is slightly lower than previous; in case of asynapsis, there is a higher lethality of individuals and oocytes with two B chromosomes.     

Temporal frequency stability and absence of effects on mating behaviour for an autosomal supernumerary segment in two natural populations of the grasshopper Eyprepocnemis plorans.

Interannual evolution of a polymorphism for a supernumerary segment in the smallest autosome of the grasshopper Eyprepocnemis plorans has been analysed in two natural populations. The polymorphism seemed to be stable in both populations, despite its undertransmission through heterozygous females carrying B chromosomes. Analyses of the effects of the extra segment on mating behaviour failed to show differential mating success in any sex or consistent effects on mating pattern. These results are discussed in relation to the maintenance of this polymorphism in natural populations.     

Supernumerary chromosomes and their behaviour in meiosis of the holocentric Cuscuta babylonica Ghoisy

A supernumerary chromosome and its behaviour during meiosis is described in the parasitic herb Cuscuta babylonica Choisy (2n = 8 + 1B). This species is characterized by holocentric chromosome behaviour, and the occurrence of a supernumerary here is considered noteworthy.     

Distortional meiotic segregation of a supernumerary chromosome producing differential frequencies in the sexes in the short-horned grasshopper Phaulacridium vittatum

Samples of males reveal the presence of a large, mitotically stable supernumerary chromosome in five populations examined. A stable frequency (11.22±0.3%) of male carriers has been observed over nine years in one population. The supernumerary follows closely the condensation cycle and behaviour of the sex chromosome in spermatogonial mitosis and meiosis. A structure simulating a terminalized chiasma frequently joins the precocious sex and supernumerary chromosomes during meiotic prophase; these two chromosomes move preferentially (70%) to opposite poles during the subsequent stages producing a differential transmission of the supernumerary to the two sexes. It is possible that the stable frequency in the population is maintained by a conserved balance between the two sexes without the need of an elimination system. The evidence supports the interpretation that the supernumerary chromosome is partially homologous with the sex chromosome. The possibility that the supernumerary might evolve into a neo-Y chromosome is suggested.     

Meiotic drive against an autosomal supernumerary segment promoted by the presence of a B chromosome in females of the grasshopper Eyprepocnemis plorans

Twenty-seven out of 50 progeny analyses performed with specimens of the grasshopper Eyprepocnemis plorans were informative about the transmission of a supernumerary heterochromatic chromosome segment. The simultaneous presence of a B chromosome in some of the parents involved in the crosses permitted us to test the relationship between both types of supernumerary heterochromatin with respect to their transmission. The results demonstrated that the supernumerary segment is partly eliminated through females possessing B chromosomes. The implications of this in relation to the occurrence of the extra segment in natural populations are discussed.by S.A. Gerbi     

PSR (paternal sex ratio) chromosomes: the ultimate selfish genetic elements

PSR (paternal sex ratio) chromosomes are a type of supernumerary (or B) chromosomes that occur in haplodiploid arthropods. They are transmitted through sperm but then cause loss of the paternal chromosomes (except themselves) early in development. As a result, PSR chromosomes convert diploid fertilized eggs (which would normally develop into females) into haploid males that carry a PSR chromosome. Because they act by completely eliminating the haploid genome of their hosts, PSR chromosomes are the most extreme form of selfish or parasitic DNA known. PSR was originally described in the parasitic wasp Nasonia vitripennis (Pteromalidae). A second PSR chromosome has been found in Trichogramma kaykai, an egg parasitoid from a different family of Hymenoptera (Trichogrammatidae). We argue that PSR chromosomes are likely to be widespread in haplodiploid organisms, but have so far gone under reported due to a paucity of population genetic studies in haplodiploids. We describe the two known PSR systems and related phenomena, and models indicating the conditions conducive to increase of PSR like chromosomes in haplodiploids.     

Post-meiotic B chromosome expulsion,during spermiogenesis,in two grasshopper species

Most supernumerary (B) chromosomes are parasitic elements carrying out an evolutionary arms race with the standard (A) chromosomes. A variety of weapons for attack and defense have evolved in both contending elements, the most conspicuous being B chromosome drive and A chromosome drive suppression. Here, we show for the first time that most microspermatids formed during spermiogenesis in two grasshopper species contain expulsed B chromosomes. By using DNA probes for B-specific satellite DNAs in Eumigus monticola and Eyprepocnemis plorans, and also 18S rDNA in the latter species, we were able to count the number of B chromosomes in standard spermatids submitted to fluorescence in situ hybridization, as well as visualizing B chromosomes inside most microspermatids. In E. plorans, the presence of B-carrying microspermatids in 1B males was associated with a significant decrease in the proportion of B-carrying standard spermatids. The fact that this decrease was apparent in elongating spermatids but not in round ones demonstrates that meiosis yields 1:1 proportions of 0B and 1B spermatids and hence that B elimination takes place post-meiotically, i.e., during spermiogenesis, implying a 5–25% decrease in B transmission rate. In E. monticola, the B chromosome is mitotically unstable and B number varies between cells within a same individual. A comparison of B frequency between round and elongating spermatids of a same individual revealed a significant 12.3% decrease. We conclude that B chromosome elimination during spermiogenesis is a defense weapon of the host genome to get rid of parasitic chromosomes.     

B chromosomes: an update about their occurrence in freshwater Neotropical fishes (Teleostei)

In freshwater Neotropical fishes, supernumerary chromosomes or B chromosomes have been found in 61 species so far, distributed in 16 families of seven different orders and in distinct hydrographic basins. The order Characiformes is the one that possesses the most species with these chromosomes, including 31 species from six different families. The order Siluriformes has 21 species from five families, with Rhamdia , of the family Heptapteridae, being the most common genus where these chromosomes are found. The order Perciformes has five species with B chromosomes in only one family, Cichlidae, and the orders Beloniformes, Cyprinodontiformes, Gymnotiformes and Synbranchiformes contain only one species each with extra chromosomes. They are found as microchromosomes in Schizodon , Astyanax , Moenkhausia , Cyphocharax , Steindachnerina , Prochilodus , Rhamdia , Iheringichthys and Loricaria , among others, up to supernumerary macrochromosomes as in Astyanax , varying in morphology as well as number, showing evidence of the wide diversity of B chromosomes in Neotropical fishes.     

Double fertilization in maize: the two male gametes from a pollen grain have the ability to fuse with egg cells

In flowering plants, two male gametes from a single pollen grain fuse with two female gametes, the egg and central cells, to form the embryo and endosperm, respectively. The question then arises whether the two male gametes fuse randomly with the egg and central cells. We investigated this question using two nearly isogenic maize lines with supernumerary B chromosomes (TB10L18) or without (r-tester). B chromosomes regularly undergo non-disjunction at the second pollen mitosis, producing one sperm cell with zero B chromosomes and one with two. We first confirmed earlier studies showing an excess of transmission of the B chromosomes to the embryo rather than to the endosperm. We then tested the possibility of a directed fertilization. For TB10L18 pollen, we could demonstrate the existence of a size dimorphism between the two sperm cells, correlated to the content in B chromosomes, as detected by fluorescence in situ hybridization (FISH). However, no directed fusion of B chromosome containing sperm to egg cells could be detected when using in vitro fertilization. The absence of directed fusion in vitro could also be demonstrated for control lines. We conclude that both male gametes have the capacity to fuse with the egg cell in maize, although sexual reproduction results in a preferential transmission of supernumerary B chromosomes.     

One gene determines maize B chromosome accumulation by preferential fertilisation; another gene(s) determines their meiotic loss

Genotypes of high (H(m)) and low (L(m)) male B transmission rate (B-TR) were obtained. B-TR segregation in the F2 is reported, showing that the H(m) and L(m) lines differ in a single locus we call mBt (male B transmission), controlling B preferential fertilisation in maize. The egg cells control which one of the sperm nuclei is going to fertilise them, mBt(h) egg cells being preferentially fertilised by the sperm nucleus carrying the supernumerary B chromosomes (Bs). It is hypothesised that the mBt gene is involved in the normal fertilisation of maize but the parasitic Bs take advantage of the mBt(h) allele to increase their own transmission. Selection was also carried out when the Bs were transmitted on the female side (H(f) and L(f) lines). The F1 hybrids show that the gene(s) that we call fBt (female B transmission), controlling female B-TR, is located on the A chromosomes acting at diploid level, the fBt(l) allele(s) for low transmission being dominant. This allele causes the loss of Bs at meiosis, which is shown using a specific B molecular probe to determine B presence/absence in microspores of both lines and hybrids. Maize Bs are a nice example of intragenome conflict, because the mBt and fBt loci are a polymorphic system of attack and defence between A and B chromosomes.     

Maintenance of a "Parasitic" B Chromosome in the Grasshopper MELANOPLUS FEMUR-RUBRUM

About 10-15% of the males and females of the grasshopper Melanoplus femur-rubrum collected near Rochester, New York, possessed a supernumerary B chromosome. The frequency of the B chromosome remained fairly constant during the years 1971-1974. The B chromosome was shown previously to be transmitted at a rate of about 0.5 and 0.8 by 1B males and females, respectively. This study was designed to determine the forces preventing the B chromosome from increasing in frequency due to the high rate of transmission by the females. Eighty inseminated females collected in the wild were analyzed cytologically together with their embryos (10-20 per female). Ten of the 80 females had a B chromosome, and they transmitted it at a rate of about 0.75. Among the 983 embryos analyzed, 0.141 had one B, 0.007 had two, and the mean number of B chromosomes per embryo was 0.155. The frequency of the B chromosome in the sperm pool (0.061) was consistent with a 0.5 rate of transmission. Individuals with two B chromosomes apparently have low viability, because about six were expected, but none was found among 851 adult males and females examined. The data suggest that the viability of the 1B individuals was only about 0.86 that of the OB individuals. There was no evidence that the B chromosome increased the fecundity of either the 1B males or females. It was concluded, therefore, that the B chromosome reduced the fitness of all the individuals carrying it and was thus "parasitic," and that it was maintained in the population only because of its high transmission rate. The maintenance of other B chromosomes with high transmission rates is reviewed.     

Undertransmission of a supernumerary chromosome segment through heterozygous females possessing B chromosomes in the grasshopper Eyprepocnemis plorans.

The transmission ratio (ks) for a supernumerary chromosome segment was studied in a total of 54 heterozygous females collected from two Spanish natural populations of the grasshopper Eyprepocnemis plorans. Our analysis clearly demonstrated that ks is negatively dependent on the number of B chromosomes in the female. The possible mechanisms by which B chromosomes may cause undertransmission of the supernumerary segment, and the implications of this phenomenon for the maintenance of this extra chromosome segment, are discussed.     

The supernumerary B chromosome of maize: drive and genomic conflict

The supernumerary B chromosome of maize is dispensable, containing no vital genes, and thus is variable in number and presence in lines of maize. In order to be maintained in populations, it has a drive mechanism consisting of nondisjunction at the pollen mitosis that produces the two sperm cells, and then the sperm with the two B chromosomes has a preference for fertilizing the egg as opposed to the central cell in the process of double fertilization. The sequence of the B chromosome coupled with B chromosomal aberrations has localized features involved with nondisjunction and preferential fertilization, which are present at the centromeric region. The predicted genes from the sequence have paralogues dispersed across all A chromosomes and have widely different divergence times suggesting that they have transposed to the B chromosome over evolutionary time followed by degradation or have been co-opted for the selfish functions of the supernumerary chromosome.     

Mapping of paternal-sex-ratio deletion chromosomes localizes multiple regions involved in expression and transmission

The paternal-sex-ratio (PSR) chromosome in the parasitic wasp Nasonia vitripennis is a submetacentric supernumerary (B chromosome). Males transmit PSR, but after fertilization it causes the loss of the paternal autosomes. Paternal genome loss caused by PSR results in the conversion of a female (diploid) zygote into a male (haploid) under haplodiploid sex determination. In this study, site-specific markers were developed to assay deletion derivatives of PSR. Both polymerase chain reaction and Southern hybridization were used to detect the presence/absence of 16 single-site markers on a set of 20 functional and nine nonfunctional deletion chromosomes. Based on the pattern of marker loss on the deletion chromosomes, the basic organization of PSR was revealed. Two sets of markers were deleted independently, apparently representing the two arms of the submetacentric chromosome. The presence or absence of specific regions was examined in relation to phenotypic characteristics of the deletion chromosomes; ability to cause paternal genome loss, and stability in mitotic cell divisions. Rather than identifying a single region on PSR as being responsible for PSR function, the results suggest that the retention of one of two chromosomal regions is sufficient for causing paternal genome loss. Furthermore, a region was identified that is tightly correlated with mitotic stability, as measured from chromosomal transmission rates. Functional chromosomes with short-arm deletions had high (approximately 100%) transmission rates, whereas functional chromosomes with long-arm deletions had low (approximately 85%) transmission rates.     

THE GENUS COLLINSIA. XVI. SUPERNUMERARY CHROMOSOMES

Dhillon , T. S., and E. D. Garber . (U. Chicago, Chicago, Ill.) The genus Collinsia. XVI. Supernumerary chromosomes. Amer. Jour. Bot. 49 (2) : 168–170. 1962.—The pairing and transmission of supernumerary chromosomes in Collinsia solitaria and in hybrids between C. sparsiflora subsp. arvensis and C. bruceae were studied. Two supernumerary chromosomes usually formed a bivalent with 1 chiasma at metaphase I; 4 supernumerary chromosomes occasionally yielded a trivalent and univalent at this stage. Plants with 2–4 supernumerary chromosomes were fertile and plants with 5–8, sterile. Plants with a given number of supernumerary chromosomes when used as seed or pollen parent gave gametes with a higher number of such chromosomes.     

Multiple supernumerary chromosomes in the pseudogamous parthenogenetic flatworm Polycelis nigra: lineage markers or remnants of genetic leakage?

Polycelis nigra is a free-living simultaneous hermaphroditic flatworm that has amphimictic and pseudogamous parthenogenetic biotypes. Sexual individuals are always diploid (2n = 16) and pseudogamous parthenogens are polyploid (usually triploid). Two types of supernumerary chromosomes are found in parthenogens, those resembling autosomes ("A-like") and typical B chromosomes, both of which reach frequencies in populations of close to 100%. Experiments measuring the transmission rates of the B chromosomes indicated that they are potentially inherited via the male line, escaping expulsion by pseudogamous parthenogenesis. This study used the C-banding technique to demonstrate (i) that there is a single morphologically distinct B chromosome (B1) and (ii) that there are two "A-like" chromosomes that can be considered B chromosomes (B2 and B3) and which are not simple polysomics of one of the eight autosomes. As there is no genetic exchange between pseudogamous parthenogenetic lineages, two different individuals carrying a similar B morph must either have received it through common ancestry (a lineage marker) or have acquired it horizontally from another parthenogenetic lineage (leakage). C-banding further revealed intra-individual heteromorphy for band regions on chromosomes 5 and 8. This supports the karyotypic observation that oogenesis is preceded by premeiotic chromosome doubling followed by pairing of replicate homologues.     

THE INTERSPECIFIC ORIGIN OF B CHROMOSOMES: EXPERIMENTAL EVIDENCE

Abstract.— A centric fragment was generated during the introgression of a chromosome region from Nasonia giraulti into N. vitripennis. This neo B chromosome carries the N. giraulti or 123⁺ gene for wild‐type eye color. Using this phenotypic effect, the transmission of this chromosome was analyzed. The supernumerary chromosome showed less than Mendelian segregation rate in meiosis and some mitotic instability manifested as mosaic phenotype for eye color. However, transmission rate and mitotic stability increased over successive generations. The transmission rate through male gametogenesis was nearly 100%. These results support the interspecific hybridization model for B chromosome origin and reveal that problems in chromosome stability can persist for several generations after “foreign chromosomes” are introduced into a different species. We suggest that hybrid zones should be investigated as possible sites for neo‐B chromosome generation.     

Human supernumeraries: are they B chromosomes?

In humans, the presence of supernumerary chromosomes is an unusual phenomenon, which is often associated with developmental abnormalities and malformations. In contrast to most animal and plant species, the extensive knowledge of the human genome and the ample set of molecular and cytogenetic tools available have permitted to ascertain not only that most human supernumerary chromosomes (HSCs) derive from the A chromosome set, but also the specific A chromosome from which most of them arose. These extra chromosomes are classified into six types on the basis of morphology and size. There are both heterochromatic and euchromatic HSCs, the latter being more detrimental. Most are mitotically stable, except some producing individual mosaicism. No information is available on the HSC transmission rate since extensive familial studies are not usually performed generally because of death of the relatives or lack of cooperation. The main B chromosome property failing in HSCs seems to be their population spread as polymorphisms, since most HSCs seem to correspond to extra A chromosomes or centric fragments spontaneously arisen in the analysed individual or one of his/her parents. However, we cannot rule out at this moment, that more intensive studies on population distribution and frequency of those HSCs most closely resembling B chromosomes (i.e. those heterochromatic and thus less detrimental) would reveal possible HSCs polymorphisms. Although HSCs cannot be considered B chromosomes, some of them might be a source for future B chromosomes. The best candidates would be heterochromatic HSCs, which might manage to drive in either sex. To ascertain this possibility, research on inheritance and population studies would be very helpful in combination with the powerful cytogenetic and molecular tools available for our species.