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Schematic comparison of the chromosomal separation occurring during the first meiotic division in standard and inverted meiosis. https://doi.org/10.1371/journal.pgen.1008918.g002
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Holocentric chromosomes possess multiple kinetochores along their length rather than the single centromere typical of other chromosomes [1]. They have been described for the first time in cytogenetic experiments dating from 1935 and, since this first observation, the term holocentric chromosome has referred to chromosomes that: i. lack the primary...
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... observations, together with several further analyses, evidenced that canonical meiosis consists of a first division (called reductional division) that involves the segregation of chromosomal homologs resulting in the reduction of chromosome number and a second division (defined equational division) consisting in the separation of sister chromatids. A general rule for meiosis is therefore: first homologues, then sisters (see figure standard vs inverted meiosis) (Fig 2). Ironically, the understanding of the reductional division in meiosis of Ascaris sp. has been obtained studying the holocentric chromosomes which, in many other taxa, follow a reverse order of meiotic division [12]. ...
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... If this degradation is insufficient, chromosomes that cannot be resolved will be retained, and a part of the chromosome could be translocated to the nucleus, possibly resulting in increased genome size and chromosome numbers. In addition, zygnematophycean algae are suggested to have holocentric chromosomes (Mandrioli & Manicardi, 2020), which may stabilize chromosomal fragments and tolerate karyotype rearrangements because of their diffuse kinetochores. Other factors, such as transference of retrotransposons, which was observed in Penium margaritaceum (Jiao et al., 2020), and extensive gene duplication may also be important to shape a large genome size variation in the C. psl. ...
The evolutionary transitions of mating systems between outcrossing and self‐fertilization are often suggested to associate with the cytological and genomic changes, but the empirical reports are limited in multicellular organisms. Here we used the unicellular zygnematophycean algae, the Closterium peracerosum–strigosum–littorale ( C. psl. ) complex, to address whether genomic properties such as genome sizes and chromosome numbers are associated with mating system transitions between homothallism (self‐fertility) and heterothallism (self‐sterility). Phylogenetic analysis revealed the polyphyly of homothallic strains, suggesting multiple transitions between homothallism and heterothallism in the C. psl. complex. Flow cytometry analysis identified a more than 2‐fold genome size variation, ranging from 0.53 to 1.42 Gbp, which was positively correlated with chromosome number variation between strains. Although we did not find consistent trends in genome size change and mating system transitions, the mean chromosome sizes tend to be smaller in homothallic strains than in their relative heterothallic strains. This result suggests that homothallic strains possibly have more fragmented chromosomes, which is consistent with the argument that self‐fertilizing populations may tolerate more chromosomal rearrangements.
... Our results also support the hypothesis that holocentric chromosomes evolved as an adaptive response to survive increased DNA damage, particularly in extreme environments 23 . More generally, our research highlights how chromosomal features and reproductive modes may contribute to genome plasticity, fostering diversification and adaptability. ...
Homologous recombination plays a fundamental role in the evolution of organisms. It serves as a DNA repair mechanism which, in sexual organisms, contributes to genetic diversity through the shuffling of alleles during meiosis. Here we investigate the two functions of homologous recombination in the bdelloid rotifer Adineta vaga, an ancient asexual species also known for its tolerance to extreme genotoxic stresses. Genomic analyses reveal that A. vaga retained meiotic recombination mechanisms, both for DNA repair and occurrence of spontaneous crossovers during oogenesis. Our study introduces a novel transgenerational DNA repair mechanism termed break-induced homologous extension repair (BIHER). BIHER operates on single DNA ends, enabling the repair of fragmented chromosomes. Our findings suggest that the BIHER mechanism, combined with a holocentric structure of chromosomes and a modified meiosis, constitutes a key adaptation for life in extreme environments. Identifying such a mechanism in bdelloid rotifers sheds a new light on the strategies that evolved to maintain genome structure in asexually reproducing species.
... ), with n = 21 as the ancestral haploid number with the highest likelihood (although, again, a large range of possible ancestral chromosome number was inferred)). Nevertheless, the high frequency of intraspecific numerical variation in this genus may introduce uncertainties in the reconstruction(Hipp et al. 2009).Chromosomal rearrangements are the main drivers of karyotypic asymmetry(Schubert and Lysak 2011;Bardella et al. 2014;Burchardt et al. 2020;Mandrioli and Manicardi 2020;Vimala et al. 2021). However, Cryptangieae diverges from this tendency, as its karyotypes exhibit symmetry. ...
Cryptangieae has recently been revised based on morphology and molecular phylogeny, but cytogenetic data is still scarce. We conducted this study with the aim of investigating the occurrence of holocentric chromosomes and pseudomonads, as well as understanding the mode of chromosomal evolution in the tribe. We performed analyses of meiotic behavior, chromosome counts, and reconstruction of the ancestral state for the haploid number. We present novel cytogenetic data for eight potentially holocentric species: Cryptangium verticillatum, Krenakia junciforme, K. minarum, Lagenocarpus bracteosus, L. griseus, L. inversus, L. rigidus, and L. tenuifolius. Meiotic abnormalities were observed, with parallel spindles being particularly noteworthy. Intra-specific variations in chromosome number were not found, which may indicate an efficient genetic control for the elimination of abnormal nuclei. The inferred ancestral haploid number was n = 16, with dysploidy being the main evolutionary mechanism. At least five chromosomal fissions occurred in Krenakia (n = 21), followed by a further ascending dysploidy event in Lagenocarpus (n = 17). As proposed for Cyperaceae, it is possible that cladogenesis events in Cryptangieae were marked by numerical and structural chromosomal changes.
... We noticed that most of the full-length LTRs were recently inserted, which may be because old LTRs were affected by genome instability, resulting in the loss of their intact structure and thus making them undetectable. Additionally, mitotic asexual reproduction and holocentromeres also contributes to the successful inheritance of fused chromosomes 70 . ...
The formation and consequences of polyploidization in animals with clonal reproduction remain largely unknown. Clade I root-knot nematodes (RKNs), characterized by parthenogenesis and allopolyploidy, show a widespread geographical distribution and extensive agricultural destruction. Here, we generated 4 unzipped polyploid RKN genomes and identified a putative novel alternative telomeric element. Then we reconstructed 4 chromosome-level assemblies and resolved their genome structures as AAB for triploid and AABB for tetraploid. The phylogeny of subgenomes revealed polyploid RKN origin patterns as hybridization between haploid and unreduced gametes. We also observed extensive chromosomal fusions and homologous gene expression decrease after polyploidization, which might offset the disadvantages of clonal reproduction and increase fitness in polyploid RKNs. Our results reveal a rare pathway of polyploidization in parthenogenic polyploid animals and provide a large number of high-precision genetic resources that could be used for RKN prevention and control.
... An alternative explanation for the high rate of autosomal rearrangements is the presence of holocentric chromosomes in aphids (Schubert and Lysak 2011;Mandrioli and Manicardi 2020). In plants, holocentric chromosomes can facilitate rearrangements, yielding variable karyotypes (Hofstatter et al. 2022), and elevated chromosomal evolution has been observed in some other groups with holocentric chromosomes (Höök et al. 2023;Ruckman et al. 2020;Fradin et al. 2017). ...
Genomes of aphids (family Aphididae) show several unusual evolutionary patterns. In particular, within the XO sex determination system of aphids, the X chromosome exhibits a lower rate of interchromosomal rearrangements, fewer highly expressed genes, and faster evolution at nonsynonymous sites compared to the autosomes. In contrast, other hemipteran lineages have similar rates of interchromosomal rearrangement for autosomes and X chromosomes. One possible explanation for these differences is the aphids life cycle of cyclical parthenogenesis, where multiple asexual generations alternate with one sexual generation. If true, we should see similar features in the genomes of Phylloxeridae, an outgroup of aphids which also undergoes cyclical parthenogenesis. To investigate this, we generated a chromosome-level assembly for the grape phylloxera, an agriculturally important species of Phylloxeridae, and identified its single X chromosome. We then performed synteny analysis using the phylloxerid genome and 30 high-quality genomes of aphids and other hemipteran species. Unexpectedly, we found that the phylloxera does not share aphids patterns of chromosome evolution. By estimating interchromosomal rearrangement rates on an absolute time scale, we found that rates are elevated for aphid autosomes compared to their X chromosomes, but this pattern does not extend to the phylloxera branch. Potentially, the conservation of X chromosome gene content is due to selection on XO males that appear in the sexual generation. We also examined gene duplication patterns across Hemiptera and uncovered horizontal gene transfer events contributing to phylloxera evolution.
... We first analyzed the color of chromatids in diakinesis oocytes in which homologous chromosomes form chiasmata, i.e., bivalents. The expected figures of crossover in holocentric chromosomes has been described in (24) and is depicted in Fig. 3A. From eight oocytes, we identified 26 bivalent chromosomes whose orientation allowed us to unambiguously distinguish the chromatids within the chiasma. ...
In asexual animals, female meiosis is modified to produce diploid oocytes. If meiosis still involves recombination, this is expected to lead to a rapid loss of heterozygosity, with adverse effects on fitness. Many asexuals, however, have a heterozygous genome, the underlying mechanisms being most often unknown. Cytological and population genomic analyses in the nematode Mesorhabditis belari revealed another case of recombining asexual being highly heterozygous genome-wide. We demonstrated that heterozygosity is maintained despite recombination because the recombinant chromatids of each chromosome pair cosegregate during the unique meiotic division. A theoretical model confirmed that this segregation bias is necessary to account for the observed pattern and likely to evolve under a wide range of conditions. Our study uncovers an unexpected type of non-Mendelian genetic inheritance involving cosegregation of recombinant chromatids.
... While most eukaryotes have chromosomes with centromeres, ∼20% of extant animals and plants are holocentric, with small centromere-like features dispersed along the entire length of their chromosomes rather than a single large centromeric region (Melters et al. 2012;Mandrioli and Manicardi 2020). Because rearranged segments do not depend on distant centromeres for meiotic segregation, segmental rearrangements may not cause the same segregation defects during cell divisions as in monocentric species (Lukhtanov et al. 2018). ...
Chromosomal rearrangements (CRs) have been known since almost the beginning of genetics. While an important role for CRs in speciation has been suggested, evidence primarily stems from theoretical and empirical studies focusing on the microevolutionary level (i.e., on taxon pairs where speciation is often incomplete). Although the role of CRs in eukaryotic speciation at a macroevolutionary level has been supported by associations between species diversity and rates of evolution of CRs across phylogenies, these findings are limited to a restricted range of CRs and taxa. Now that more broadly applicable and precise CR detection approaches have become available, we address the challenges in filling some of the conceptual and empirical gaps between micro- and macroevolutionary studies on the role of CRs in speciation. We synthesize what is known about the macroevolutionary impact of CRs and suggest new research avenues to overcome the pitfalls of previous studies to gain a more comprehensive understanding of the evolutionary significance of CRs in speciation across the tree of life.
... However, the centromeric activity can be distributed along a large portion of the so-called holocentric chromosomes (Mandrioli & Manicardi, 2020). Holocentricity has evolved independently at least 19 times in various clades across the tree of life including Lepidoptera (i.e. ...
Repetitive elements can cause large-scale chromosomal rearrangements, for example through ectopic recombination, potentially promoting reproductive isolation and speciation. Species with holocentric chromosomes, that lack a localized centromere, might be more likely to retain chromosomal rearrangements that lead to karyotype changes such as fusions and fissions. This is because chromosome segregation during cell division should be less affected than in organisms with a localized centromere. The relationships between repetitive elements and chromosomal rearrangements and how they may translate to patterns of speciation in holocentric organisms are though poorly understood. Here, we use a reference-free approach based on low-coverage short-read sequencing data to characterize the repeat landscape of two independently evolved holocentric groups: Erebia butterflies and Carex sedges. We consider both micro-and macro-evolutionary scales to investigate the repeat landscape differentiation between Erebia populations and the association between repeats and karyotype changes in a phylogenetic framework for both Erebia and Carex. At a micro-evolutionary scale, we found population differentiation in repeat landscape that increases with overall intraspecific genetic differentiation among four Erebia species. At a macro-evolutionary scale, we found indications for an association between repetitive elements and karyotype changes along both Erebia and Carex phylogenies. Altogether, our results suggest that repetitive elements are associated with the level of population differentiation and chromosomal rearrangements in holocentric clades and therefore likely play a role in adaptation and potentially species diversification.
... This evolutionary dynamics of large chromosomal rearrangements basically coincides with the theory that predicts a slow accumulation of underdominant chromosomal rearrangements (King 1993). The accumulation of chromosomal rearrangements in Lepidoptera can be facilitated by two of their genomic features: holocentricity of chromosomes (Mandrioli and Manicardi 2020) and a tendency to inverted meiosis (Archetti 2020). The first feature increases the probability that the rearranged chromosomes will retain normal kinetic activity (Mandrioli and Manicardi 2020). ...
... The accumulation of chromosomal rearrangements in Lepidoptera can be facilitated by two of their genomic features: holocentricity of chromosomes (Mandrioli and Manicardi 2020) and a tendency to inverted meiosis (Archetti 2020). The first feature increases the probability that the rearranged chromosomes will retain normal kinetic activity (Mandrioli and Manicardi 2020). The second feature contributes to the formation of balanced gametes in chromosomal heterozygotes (Lukhtanov et al. 2018). ...
In the evolution of many organisms, periods of slow genome reorganization (= chromosomal conservatism) are interrupted by bursts of numerous chromosomal changes (= chromosomal megaevolution). Using comparative analysis of chromosome-level genome assemblies, we investigated these processes in blue butterflies (Lycaenidae). We demonstrate that the phase of chromosome number conservatism is characterized by the stability of most autosomes and dynamic evolution of the sex chromosome Z, resulting in multiple variants of NeoZ chromosomes due to autosome-sex chromosome fusions. In contrast during the phase of rapid chromosomal evolution, the explosive increase in chromosome number occurs mainly through simple chromosomal fissions. We show that chromosomal megaevolution is a highly non-random canalized process, and in two phylogenetically independent Lysandra lineages, the drastic parallel increase in number of fragmented chromosomes was achieved, at least partially, through reuse of the same ancestral chromosomal breakpoints. In species showing chromosome number doubling, we found no blocks of duplicated sequences or duplicated chromosomes, thus refuting the hypothesis of polyploidy. In the studied taxa, long blocks of interstitial telomere sequences (ITSs) consist of (TTAGG)n arrays interspersed with telomere-specific retrotransposons. ITSs are sporadically present in rapidly evolving Lysandra karyotypes, but not in the species with ancestral chromosome number. Therefore, we hypothesize that the transposition of telomeric sequences may be triggers of the rapid chromosome number increase. Finally, we discuss the hypothetical genomic and population mechanisms of chromosomal megaevolution and argue that the disproportionally high evolutionary role of the Z sex chromosome can be additionally reinforced by sex chromosome—autosome fusions and Z-chromosome inversions.
... We first analyzed the color of chromatids in diakinesis oocytes, in which homologous chromosomes form chiasmata, i.e. bivalents. The expected figures of crossing-over in holocentric chromosomes has been described in (21) and is depicted in Figure 3A.From 8 oocytes, we identified 26 bivalent chromosomes whose orientation allowed us to unambiguously distinguish the chromatids within the chiasma. For 12 of them, the two opposed chromatids had the same color and could not be analyzed. ...
In asexual animals, female meiosis is modified to produce diploid oocytes. Associated with recombination, this is expected to lead to a rapid loss of heterozygosity, with adverse effects on fitness. Many asexuals, however, have a heterozygous genome, the underlying mechanisms being most often unknown. Cytological and population genomic analyses in the nematode Mesorhabditis belari revealed another case of recombining asexual being highly heterozygous genome-wide. We demonstrated that heterozygosity is maintained because the recombinant chromatids of each chromosome pair co-segregate during the unique meiotic division. A theoretical model confirmed that this segregation bias is necessary to account for the observed pattern and likely to evolve under a wide range of conditions. Our study uncovers a new type of cell division involving Directed Chromatid Assortment.
One sentence summary
Genome wide heterozygosity in the asexual nematode Mesorhabditis belari is achieved by directed assortment of recombinant chromatids during female meiosis
