Automictic reproduction in interspecific hybrids of poeciliid fish

Automixis, the process whereby the fusion of meiotic products restores the diploid state of the egg, is a common mode of reproduction in plants but has also been described in invertebrate animals. In vertebrates, however, automixis has so far only been discussed as one of several explanations for isolated cases of facultative parthenogenesis. Analyzing oocyte formation in F1 hybrids derived from Poecilia mexicana limantouri and P. latipinna crosses (the cross that led to the formation of the gynogenetic Poecilia formosa), we found molecular evidence for automictic oocyte production. The mechanism involves the random fusion of meiotic products after the second meiotic division. The fertilization of diploid oocytes gives rise to fully viable triploid offspring. Although the automictic production of diploid oocytes as seen in these F1 hybrids clearly represents a preadaptation to parthenogenetic reproduction, it is also a powerful intrinsic postzygotic isolation mechanism because the resulting next generation triploids were always sterile. The mechanism described here can explain facultative parthenogenesis, as well as varying ploidy levels reported in different animal groups. Most importantly, at least some of the reported cases of triploidy in humans can now be traced back to automixis.     

Meiotic restitution in amphihaploids in the tribe Triticeae

In haploid and diploid organisms of the plant kingdom, meiotic division of diploid cells proceeds in two consecutive stages, with DNA replicating only once. In amphihaploids (interspecific or intergeneric hybrids), where homologs are absent, the reduction of the chromosome number does not occur, meiosis is abnormal, and the plants are sterile. Gamete viability in F₁ hybrids is ensured by a single division when chromosomes are separated into sister chromatids in either the first or the second division. Such gametes ensure partial fertility of amphihaploids, thereby facilitating their survival and stabilization of the polygenome. The frequency of the formation of viable gametes varies from a few cases to 98.8% in different anthers of the hybrids. Here, studies on the cytological mechanisms and genetic control of chromosome unreduction or restitution in different amphihaploids of the tribe Triticeae are reviewed. The current notions on the control of formation of restitution nuclei based on the principles of a prolonged metaphase I and different types of meiocytes. The main terms used for systematization of restitution mechanisms are first-division restitution (FDR), single-division meiosis (SDM), and unreductional meiotic cell division (UMCD). It has been assumed that archesporial cells of wide hybrids may have two cell division programs, the meiotic and the mitoyic ones The possible approaches to the analysis of the genetic control of chromosome restitution in amphihaploids are discussed.     

Dimorphic mating-type chromosomes in the fungus Microbotryum violaceum

Fungi often mate as haploids, and sex chromosomes (i.e., mating-type chromosomes) that are dimorphic for their size or overall DNA content have never been reported in this kingdom. Using electrophoretic techniques for karyotype analysis, a highly dimorphic chromosome pair that determines mating compatibility is shown to occur in populations of the fungus Microbotryum violaceum. This substantiates the evolution of such dimorphism as a general feature associated with haploid determination of mating compatibility, which previously had been known only in haplodioecious plants (mosses and liverworts). Size-dimorphic sex chromosomes are present in a lineage of M. violaceum native to Europe, as well as a lineage native to North America. However, they are very different in size between these lineages, indicating either independent evolution of the dimorphism or a large degree of divergence since their isolation. Several DNA sequences that show sequence similarity to transposons were isolated from these sex chromosomes.     

Meiotic recombination dramatically decreased in thelytokous queens of the little fire ant and their sexually produced workers

The little fire ant, Wasmannia auropunctata, displays a peculiar breeding system polymorphism. Classical haplo-diploid sexual reproduction between reproductive individuals occurs in some populations, whereas, in others, queens and males reproduce clonally. Workers are produced sexually and are sterile in both clonal and sexual populations. The evolutionary fate of the clonal lineages depends strongly on the underlying mechanisms allowing reproductive individuals to transmit their genomes to subsequent generations. We used several queen-offspring data sets to estimate the rate of transition from heterozygosity to homozygosity associated with recombination events at 33 microsatellite loci in thelytokous parthenogenetic queen lineages and compared these rates with theoretical expectations under various parthenogenesis mechanisms. We then used sexually produced worker families to define linkage groups for these 33 loci and to compare meiotic recombination rates in sexual and parthenogenetic queens. Our results demonstrate that queens from clonal populations reproduce by automictic parthenogenesis with central fusion. These same parthenogenetic queens produce normally segregating meiotic oocytes for workers, which display much lower rates of recombination (by a factor of 45) than workers produced by sexual queens. These low recombination rates also concern the parthenogenetic production of queen offspring, as indicated by the very low rates of transition from heterozygosity to homozygosity observed (from 0% to 2.8%). We suggest that the combination of automixis with central fusion and a major decrease in recombination rates allows clonal queens to benefit from thelytoky while avoiding the potential inbreeding depression resulting from the loss of heterozygosity during automixis. In sterile workers, the strong decrease of recombination rates may also facilitate the conservation over time of some coadapted allelic interactions within chromosomes that might confer an adaptive advantage in habitats disturbed by human activity, where clonal populations of W. auropunctata are mostly found.     

Suppressed recombination and a pairing anomaly on the mating-type chromosome of Neurospora tetrasperma

Neurospora crassa and related heterothallic ascomycetes produce eight homokaryotic self-sterile ascospores per ascus. In contrast, asci of N. tetrasperma contain four self-fertile ascospores each with nuclei of both mating types (matA and mata). The self-fertile ascospores of N. tetrasperma result from first-division segregation of mating type and nuclear spindle overlap at the second meiotic division and at a subsequent mitotic division. Recently, Merino et al. presented population-genetic evidence that crossing over is suppressed on the mating-type chromosome of N. tetrasperma, thereby preventing second-division segregation of mating type and the formation of self-sterile ascospores. The present study experimentally confirmed suppressed crossing over for a large segment of the mating-type chromosome by examining segregation of markers in crosses of wild strains. Surprisingly, our study also revealed a region on the far left arm where recombination is obligatory. In cytological studies, we demonstrated that suppressed recombination correlates with an extensive unpaired region at pachytene. Taken together, these results suggest an unpaired region adjacent to one or more paired regions, analogous to the nonpairing and pseudoautosomal regions of animal sex chromosomes. The observed pairing and obligate crossover likely reflect mechanisms to ensure chromosome disjunction.     

Structural heterozygosity and aneuploidy in the parthenogenetic stick insect Carausius morosus Br. (Phasmatodea: Phasmatidae)

The female chromosome complement of the thelytokous stick insect Carausius morosus Br. consists of three metacentric sex chromosomes, four metacentric and 57 acrocentric autosomes. The rare impaternate males have two sex chromosomes. The spermatogenesis is highly aberrant which is evident from the various numbers of univalents, homomorphic and unequal bivalents, and multivalents during first metaphase, and from abnormal segregation patterns during first and second anaphase. The abnormalities are due to aneuploidy and structural heterozygosity. The heterozygosity is maintained by the endomeiotic chromosome duplication in females. Translocations resulting from chiasmata in unequal associations are not formed during female meiosis. It has been discussed that the heterozygosity in males, and consequently in females, is caused by either chromosomal mutations, as indicated by at least ten interchanges and three inversions, or hybridization, indicated by allotriploidy.     

Regional Bivalent-Univalent Pairing versus Trivalent Pairing of a Trisomic Chromosome in Saccharomyces Cerevisiae

In meiosis I, homologous chromosomes pair, recombine and segregate to opposite poles. These events and subsequent meiosis II ensure that each of the four meiotic products has one complete set of chromosomes. In this study, the meiotic pairing and segregation of a trisomic chromosome in a diploid (2n + 1) yeast strain was examined. We find that trivalent pairing and segregation is the favored arrangement. However, insertions near the centromere in one of the trisomic chromosomes leads to preferential pairing and segregation of the ``like' centromeres of the remaining two chromosomes, suggesting that bivalent-univalent pairing and segregation is favored for this region.     

Putative origin of clonal lineages of Amylostereum areolatum, the fungal symbiont associated with Sirex noctilio, retrieved from Pinus sylvestris, in eastern Canada

The Eurasian Sirex noctilio-Amylostereum areolatum complex was discovered and has become established close to the North American Great Lakes in the 2000s. This invasive forest insect pest represents a very high risk to native and exotic pines in North America. We investigated the geographical origin of clonal lineages of the fungal symbiont A. areolatum in the recently pest-colonized eastern Canadian region by analyzing mitochondrial and nuclear sequence variations and comparing the genetic diversity of a worldwide collection of fungal symbionts among six countries where the Sirex complex is native and four countries from which the insect-fungal complex has been introduced. In total, 102 isolates were analyzed. While 12 multilocus genotypes (MLGs) are observed in the areas where S. noctilio is native, only two MLGs are retrieved from areas where S. noctilio is not native, indicating the wide spread of clonal lineages in the introduced fungal symbiont of S. noctilio. MLG2 comprises 26% of the Canadian isolates and is also observed in Chile and South Africa, where the insect-fungal complex has also been introduced. MLG3 comprises 74% of the Canadian isolates and is also observed in the USA, but nowhere else in our worldwide collection. Thus, at least one of the Canadian clonal lineages shares a common origin with A.?areolatum isolates from the Southern Hemisphere. The source of the second clonal lineage is still unknown, but phylogenetic analyses show that MLG3 is isolated. More extended sampling is necessary to determine the origin of this fungal clonal lineage and investigate its probable symbiotic association with native North American Sirex.     

A large-scale screen in S. pombe identifies seven novel genes required for critical meiotic events

Meiosis is a specialized form of cell division by which sexually reproducing diploid organisms generate haploid gametes. During a long prophase, telomeres cluster into the bouquet configuration to aid chromosome pairing, and DNA replication is followed by high levels of recombination between homologous chromosomes (homologs). This recombination is important for the reductional segregation of homologs at the first meiotic division; without further replication, a second meiotic division yields haploid nuclei. In the fission yeast Schizosaccharomyces pombe, we have deleted 175 meiotically upregulated genes and found seven genes not previously reported to be critical for meiotic events. Three mutants (rec24, rec25, and rec27) had strongly reduced meiosis-specific DNA double-strand breakage and recombination. One mutant (tht2) was deficient in karyogamy, and two (bqt1 and bqt2) were deficient in telomere clustering, explaining their defects in recombination and segregation. The moa1 mutant was delayed in premeiotic S phase progression and nuclear divisions. Further analysis of these mutants will help elucidate the complex machinery governing the special behavior of meiotic chromosomes.     

Puzzling chromosome behavior in triploid females of Drosophila melanogaster

Based on a particular formation of the chromocenter and trivalents in triploid Drosophila females, as well as on asynapsis in pericentromeric regions (which is a result of trivalent competition), an explanation for the increased frequency of crossing over and nonrandom segregation of the X chromosomes and autosomes in the first meiotic division is suggested. It is proposed that a delay in pairing of the pericentromeric heterochromatic chromosome regions combined into a single chromocenter leads to the following: (1) formation of the heteroduplex structures (X structures) takes more time and, consequently, their number and the frequency of crossing over in the paired chromosome regions increases; (2) in nonhomologous chromosomes, the chromocentral connections, which normally degrade in prometaphase, are retained to fulfill a function of coorientation during the first meiotic division.     

Soft selection reduces loss of heterozygosity in asexual reproduction

The adaptive value of sexual reproduction is still debated in evolutionary theory. It has been proposed that the advantage of sexual reproduction over asexual reproduction is to promote genetic diversity, to prevent the accumulation of harmful mutations or to preserve heterozygosity. Since these hypothetical advantages depend on the type of asexual reproduction, understanding how selection affects the taxonomic distribution of each type could help us discriminate between existing hypotheses. Here, I argue that soft selection, competition among embryos or offspring in selection arenas prior to the hard selection of the adult phase, reduces loss of heterozygosity in certain types of asexual reproduction. Since loss of heterozygosity leads to the unmasking of recessive deleterious mutations in the progeny of asexual individuals, soft selection facilitates the evolution of these types of asexual reproduction. Using a population genetics model, I calculate how loss of heterozygosity affects fitness for different types of apomixis and automixis, and I show that soft selection significantly reduces loss of heterozygosity, hence increases fitness, in apomixis with suppression of the first meiotic division and in automixis with central fusion, the most common types of asexual reproduction. Therefore, if sexual reproduction evolved to preserve heterozygosity, soft selection should be associated with these types of asexual reproduction. I discuss the evidence for this prediction and how this and other observations on the distribution of different types of asexual reproduction in nature is consistent with the heterozygosity hypothesis.     

Microsatellite-centromere mapping in the loach, Misgurnus anguillicaudatus

Primer sets for 15 polymorphic microsatellite loci were developed in the loach, Misgurnus anguillicaudatus (Cobitidae) by molecular cloning and sequencing techniques. Mendelian inheritance was confirmed for the 15 loci by examining the genotypic segregation produced with the primer sets in two full-sib families. The loci were mapped in relation to their centromere in four gynogenetic diploid lines, which were induced by inhibition of the second meiotic division after fertilization with genetically inert sperm. Microsatellite-centromere recombination rates ranged between 0.06 and 0.95 under the assumption of complete interference. Thus, these loci are distributed from the centromeres to the telomeres of their respective chromosomes. The success of mitotic gynogenesis, produced by suppression of the first cleavage, was verified by homozygosity at three diagnostic microsatellite loci that exhibited high gene-centromere meiotic recombination rates in the same family. The differences in heterozygosity levels observed with these markers were attributed to differences in the temporal application of heat shock following inert sperm activation.     

Intratetrad mating and its genetic and evolutionary consequences

Genetic characteristics of intratetrad mating, i.e., fusion of haploid products of one meiotic division, are considered. Upon intratetrad mating, the probability of homozygotization is lower than that upon self-fertilization, while heterozygosity at genes linked to the mating-type locus, which determines the possibility of cell fusion, is preserved. If the mating-type locus is linked to the centromere, the genome regions adjoining the centromeres of all chromosomes remain heterozygous. Intratetrad mating is characteristic of a number of fungi (Saccharomyces cerevisiae, Saccharomycodes ludwigii, Neurospora tetrasperma, Agaricus bisporus, Microbotryum violaceum, and others). Parthenogenetic reproduction in some insects also involves this type of fusion of nuclei. Intratetrad mating leads to the accumulation of haplolethals (i.e., lethals manifesting in haploid cells but not hindering their mating) in pericentric chromosome regions. Since heterozygosity increases viability of an organism, recombination has been suppressed during evolution in fungi characterized by intratetrad mating, which ensures heterozygosity of the most part of the genome.__________Translated from Genetika, Vol. 41, No. 4, 2005, pp. 508–519.Original Russian Text Copyright © 2005 by Zakharov.     

Puzzling Chromosome Behavior in Triploid Females of Drosophila melanogaster

Based on a particular formation of the chromocenter and trivalents in triploid Drosophila females, as well as on asynapsis in pericentromeric regions (which is a result of trivalent competition), an explanation for the increased frequency of crossing over and nonrandom segregation of the X chromosomes and autosomes in the first meiotic division is suggested. It is proposed that a delay in pairing of the pericentromeric heterochromatic chromosome regions combined into a single chromocenter leads to the following: (1) formation of the heteroduplex structures (X structures) takes more time and, consequently, their number and the frequency of crossing over in the paired chromosome regions increases; (2) in nonhomologous chromosomes, the chromocentral connections, which normally degrade in prometaphase, are retained to fulfill a function of coorientation during the first meiotic division.     

Diploid spermatids: a manifestation of spermatogenic impairment in XOSxr and T31H/+ male mice

Microdensitometry of Feulgen-stained spermatogenic cell preparations from six XOSxr and four T31H/+ male mice revealed large numbers of spermatids with a diploid amount of DNA. In XOSxr mice, where the diploid spermatids usually constituted the majority of the spermatid population, there were large differences from mouse to mouse in the proportion of diploid spermatids (range, 35%-94%). There were large losses of both haploid and diploid spermatids during spermiogenesis, and the later condensed spermatids of both types were grossly misshapen. It is suggested that the omission of one meiotic division, and the other spermiogenic anomalies may be manifestations of a meiotic "quality control" mechanism that destroys the products of those pachytene spermatocytes which have unsynapsed or incompletely synapsed chromosomes.     

Repetitive DNA in the automictic fungus <Emphasis Type="Italic">Microbotryum violaceum</Emphasis>

The small genomes of fungi are expected to have little repetitive content other than rDNA genes. Moreover, among asexual or highly selfing lineages, the diversity of repetitive elements is also expected to be very low. However, in the automictic fungus Microbotryum violaceum, a very large proportion of random DNA fragments from the autosomes and the fungal sex chromosomes are repetitive in nature, either as retrotransposon or helicase sequences. Among the retrotransposon sequences, examples were found from each major kind of elements, including copia, gypsy, and non-LTR sequences. The most numerous were copia-like elements, which are believed to be rare in fungi, particularly among basidiomycetes. The many helicase sequences appear to belong to the recently discovered Helitron type of transposable elements. Also, sequences that could not be identified as a known type of gene were also very repetitive within the database of random fragments from M. violaceum. The differentiated pair of fungal sex chromosomes and suppression of recombination may be the major forces determining the highly repetitive content in the small genome of M. violaceum.     

Un ménage à quatre: the molecular biology of chromosome segregation in meiosis

Sexually reproducing organisms rely on the precise reduction of chromosome number during a specialized cell division called meiosis. Whereas mitosis produces diploid daughter cells from diploid cells, meiosis generates haploid gametes from diploid precursors. The molecular mechanisms controlling chromosome transmission during both divisions have started to be delineated. This review focuses on the four fundamental differences between mitotic and meiotic chromosome segregation that allow the ordered reduction of chromosome number in meiosis: (1) reciprocal recombination and formation of chiasmata between homologous chromosomes, (2) suppression of sister kinetochore biorientation, (3) protection of centromeric cohesion, and (4) inhibition of DNA replication between the two meiotic divisions.     

What are the spermatocyte's requirements for successful meiotic division?

The consequences of error during meiotic division in spermatogenesis can be serious: aneuploid spermatozoa, embryonic lethality, and developmental abnormalities. Recombination between homologs is essential to ensure normal segregation; thus the spermatocyte must time division precisely so that it occurs after recombination between chromosomes and accumulation of the cell-cycle machinery necessary to ensure an accurate segregation of chromosomes. We use two systems to investigate meiotic division during spermatogenesis in the mouse: pharmacological induction of meiotic metaphase in cultured spermatocytes and transillumination-mediated dissection of stage XII seminiferous tubule segments to monitor progress through the division phase. By these approaches we can assess timing of acquisition of competence for the meiotic division phase and the temporal order of events as division proceeds. Competence for the meiotic division arises in the mid-pachytene stage of meiotic prophase, after chromosomes have synapsed and coincident with the accumulation of the cell-cycle regulatory protein CDC25C. The activity of both MPF and topoisomerase II are required. The earliest hallmarks of the division phase are nuclear envelope breakdown, followed by phosphorylation of histone H3 and chromosome condensation. These events are likely to be monitored by checkpoint mechanisms since checkpoint proteins can be localized in nuclei and DNA-damaging agents delay entry into the meiotic division phase. Understanding how the spermatocyte regulates its entry into the meiotic division phase can help clarify the natural mechanisms ensuring accurate chromosome segregation and preventing aneuploidy. J. Exp. Zool. (Mol. Dev. Evol.) 285:243-250, 1999.