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Article ; Online: Why Are X Autosome Rearrangements so Frequent in Beetles? A Study of 50 Cases.

Dutrillaux, Bernard / Dutrillaux, Anne-Marie

2023 Volume 14, Issue 1

Abstract: Amongst the 460 karyotypes of Polyphagan Coleoptera that we studied, 50 (10.8%) were carriers of an X autosome rearrangement. In addition to mitotic metaphase analysis, the correct diagnosis was performed on meiotic cells, principally at the pachytene ... ...

Abstract	Amongst the 460 karyotypes of Polyphagan Coleoptera that we studied, 50 (10.8%) were carriers of an X autosome rearrangement. In addition to mitotic metaphase analysis, the correct diagnosis was performed on meiotic cells, principally at the pachytene stage. The percentages of these inter-chromosomal rearrangements, principally fusions, varied in relation to the total diploid number of chromosomes: high (51%) below 19, null at 19, low (2.7%) at 20 (the ancestral and modal number), and slightly increasing from 7.1% to 16.7% from 22 to above 30. The involvement of the X in chromosome fusions appears to be more than seven-fold higher than expected for the average of the autosomes. Examples of karyotypes with X autosome rearrangements are shown, including insertion of the whole X in the autosome (ins(A;X)), which has never been reported before in animals. End-to-end fusions (Robertsonian translocations, terminal rearrangements, and pseudo-dicentrics) are the most frequent types of X autosome rearrangements. As in the 34 species with a 19,X formula, there was no trace of the Y chromosome in the 50 karyotypes with an X autosome rearrangement, which demonstrates the dispensability of this chromosome. In most instances, C-banded heterochromatin was present at the X autosome junction, which suggests that it insulates the gonosome from the autosome portions, whose genes are subjected to different levels of expression. Finally, it is proposed that the very preferential involvement of the X in inter-chromosome rearrangements is explained by: (1) the frequent acrocentric morphology of the X, thus the terminal position of constitutive heterochromatin, which can insulate the attached gonosomal and autosomal components; (2) the dispensability of the Y chromosome, which considerably minimizes the deleterious consequences of the heterozygous status in male meiosis, (3) following the rapid loss of the useless Y chromosome, the correct segregation of the X autosome-autosome trivalent, which ipso facto is ensured by a chiasma in its autosomal portion.
MeSH term(s)	Animals ; Male ; X Chromosome ; Heterochromatin/genetics ; Coleoptera/genetics ; Y Chromosome/genetics ; Sex Chromosomes
Chemical Substances	Heterochromatin
Language	English
Publishing date	2023-01-05
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2527218-4
ISSN	2073-4425 ; 2073-4425
ISSN (online)	2073-4425
ISSN	2073-4425
DOI	10.3390/genes14010150
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Why Are X Autosome Rearrangements so Frequent in Beetles? A Study of 50 Cases

Dutrillaux, Bernard / Dutrillaux, Anne-Marie

Genes (Basel). 2023 Jan. 05, v. 14, no. 1

2023

Abstract	Amongst the 460 karyotypes of Polyphagan Coleoptera that we studied, 50 (10.8%) were carriers of an X autosome rearrangement. In addition to mitotic metaphase analysis, the correct diagnosis was performed on meiotic cells, principally at the pachytene stage. The percentages of these inter-chromosomal rearrangements, principally fusions, varied in relation to the total diploid number of chromosomes: high (51%) below 19, null at 19, low (2.7%) at 20 (the ancestral and modal number), and slightly increasing from 7.1% to 16.7% from 22 to above 30. The involvement of the X in chromosome fusions appears to be more than seven-fold higher than expected for the average of the autosomes. Examples of karyotypes with X autosome rearrangements are shown, including insertion of the whole X in the autosome (ins(A;X)), which has never been reported before in animals. End-to-end fusions (Robertsonian translocations, terminal rearrangements, and pseudo-dicentrics) are the most frequent types of X autosome rearrangements. As in the 34 species with a 19,X formula, there was no trace of the Y chromosome in the 50 karyotypes with an X autosome rearrangement, which demonstrates the dispensability of this chromosome. In most instances, C-banded heterochromatin was present at the X autosome junction, which suggests that it insulates the gonosome from the autosome portions, whose genes are subjected to different levels of expression. Finally, it is proposed that the very preferential involvement of the X in inter-chromosome rearrangements is explained by: (1) the frequent acrocentric morphology of the X, thus the terminal position of constitutive heterochromatin, which can insulate the attached gonosomal and autosomal components; (2) the dispensability of the Y chromosome, which considerably minimizes the deleterious consequences of the heterozygous status in male meiosis, (3) following the rapid loss of the useless Y chromosome, the correct segregation of the X autosome–autosome trivalent, which ipso facto is ensured by a chiasma in its autosomal portion.
Keywords	Coleoptera ; Y chromosome ; autosomes ; diploidy ; heterochromatin ; heterozygosity ; karyotyping ; males ; meiosis ; metaphase ; mitosis ; pachytene stage
Language	English
Dates of publication	2023-0105
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article ; Online
ZDB-ID	2527218-4
ISSN	2073-4425
ISSN	2073-4425
DOI	10.3390/genes14010150
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Article ; Online: Multiple Chromosome Fissions, Including That of the X Chromosome, in

Dutrillaux, Bernard / Dutrillaux, Anne-Marie / Salazar, Karen / Boucher, Stéphane

Genes

2023 Volume 14, Issue 7

Abstract: The male karyotype ... ...

Abstract	The male karyotype of
MeSH term(s)	Animals ; Male ; Heterochromatin ; Coleoptera/genetics ; New Caledonia ; X Chromosome/genetics ; Karyotyping
Chemical Substances	Heterochromatin
Language	English
Publishing date	2023-07-21
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2527218-4
ISSN	2073-4425 ; 2073-4425
ISSN (online)	2073-4425
ISSN	2073-4425
DOI	10.3390/genes14071487
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Article ; Online: Multiple Chromosome Fissions, Including That of the X Chromosome, in Aulacocyclus tricuspis Kaup (Coleoptera, Passalidae) from New Caledonia: Characterization of a Rare but Recurrent Pathway of Chromosome Evolution in Animals

Dutrillaux, Bernard / Dutrillaux, Anne-Marie / Salazar, Karen / Boucher, Stéphane

Genes (Basel). 2023 July 21, v. 14, no. 7

2023

Abstract: The male karyotype of Aulacocyclus tricuspis Kaup 1868 (Coleoptera, Scarabaeoidea, Passalidae, Aulacocyclinae) from New Caledonia contains an exceptionally high number of chromosomes, almost all of which are acrocentric (53,X1X2Y). Unlike the karyotypes ... ...

Abstract	The male karyotype of Aulacocyclus tricuspis Kaup 1868 (Coleoptera, Scarabaeoidea, Passalidae, Aulacocyclinae) from New Caledonia contains an exceptionally high number of chromosomes, almost all of which are acrocentric (53,X1X2Y). Unlike the karyotypes of other species of the pantropical family Passalidae, which are principally composed of metacentric chromosomes, this karyotype is derived by fissions involving almost all the autosomes after breakage in their centromere region. This presupposes the duplication of the centromeres. More surprising is the X chromosome fragmentation. The rarity of X chromosome fission during evolution may be explained by the deleterious effects of alterations to the mechanisms of gene dosage compensation (resulting from the over-expression of the unique X chromosome in male insects). Herein, we propose that its occurrence and persistence were facilitated by (1) the presence of amplified heterochromatin in the X chromosome of Passalidae ancestor, and (2) the capacity of heterochromatin to modulate the regulation of gene expression. In A. tricuspis, we suggest that the portion containing the X proper genes and either a gene-free heterochromatin fragment or a fragment containing a few genes insulated from the peculiar regulation of the X by surrounding heterochromatin were separated by fission. Finally, we show that similar karyotypes with multiple acrocentric autosomes and unusual sex chromosomes rarely occur in species of Coleoptera belonging to the families Vesperidae, Tenebrionidae, and Chrysomelidae. Unlike classical Robertsonian evolution by centric fusion, this pathway of chromosome evolution involving the centric fission of autosomes has rarely been documented in animals.
Keywords	Chrysomelidae ; Passalidae ; Tenebrionidae ; ancestry ; autosomes ; centromeres ; evolution ; gene dosage ; gene expression regulation ; heterochromatin ; karyotyping ; males ; New Caledonia
Language	English
Dates of publication	2023-0721
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article ; Online
ZDB-ID	2527218-4
ISSN	2073-4425
ISSN	2073-4425
DOI	10.3390/genes14071487
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Article: Different behaviour of C-banded peri-centromeric heterochromatin between sex chromosomes and autosomes in Polyphagan beetles.

Dutrillaux, Anne-Marie / Dutrillaux, Bernard

Comparative cytogenetics

2019 Volume 13, Issue 2, Page(s) 179–192

Abstract: Heterochromatin variation was studied after C-banding of male karyotypes with a XY sex formula from 224 species belonging to most of the main families of Coleoptera. The karyotypes were classified in relation with the ratio heterochromatin/euchromatin ... ...

Abstract	Heterochromatin variation was studied after C-banding of male karyotypes with a XY sex formula from 224 species belonging to most of the main families of Coleoptera. The karyotypes were classified in relation with the ratio heterochromatin/euchromatin total amounts and the amounts of heterochromatin on autosomes and gonosomes were compared. The C-banded karyotypes of 19 species, representing characteristic profiles are presented. This analysis shows that there is a strong tendency for the homogenization of the size of the peri-centromeric C-banded heterochromatin on autosomes. The amount of heterochromatin on the X roughly follows the variations of autosomes. At contrast, the C-banded heterochromatin of the Y, most frequently absent or very small and rarely amplified, looks quite independent from that of other chromosomes. We conclude that the Xs and autosomes, but not the Y, possibly share some, but not all mechanisms of heterochromatin amplification/reduction. The theoretical models of heterochromatin expansion are discussed in the light of these data.
Language	English
Publishing date	2019-07-03
Publishing country	Bulgaria
Document type	Journal Article
ZDB-ID	2572457-5
ISSN	1993-078X ; 1993-0771
ISSN (online)	1993-078X
ISSN	1993-0771
DOI	10.3897/CompCytogen.v13i2.34746
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Article: Different behaviour of C-banded peri-centromeric heterochromatin between sex chromosomes and autosomes in Polyphagan beetles

Dutrillaux, Anne-Marie / Dutrillaux, Bernard

Comparative cytogenetics. 2019 July 03, v. 13, no. 2

2019

Abstract	Heterochromatin variation was studied after C-banding of male karyotypes with a XY sex formula from 224 species belonging to most of the main families of Coleoptera. The karyotypes were classified in relation with the ratio heterochromatin/euchromatin total amounts and the amounts of heterochromatin on autosomes and gonosomes were compared. The C-banded karyotypes of 19 species, representing characteristic profiles are presented. This analysis shows that there is a strong tendency for the homogenization of the size of the peri-centromeric C-banded heterochromatin on autosomes. The amount of heterochromatin on the X roughly follows the variations of autosomes. At contrast, the C-banded heterochromatin of the Y, most frequently absent or very small and rarely amplified, looks quite independent from that of other chromosomes. We conclude that the Xs and autosomes, but not the Y, possibly share some, but not all mechanisms of heterochromatin amplification/reduction. The theoretical models of heterochromatin expansion are discussed in the light of these data.
Keywords	Coleoptera ; autosomes ; chromosome banding ; heterochromatin ; homogenization ; karyotyping ; males
Language	English
Dates of publication	2019-0703
Size	p. 179-192.
Publishing place	Pensoft Publishers
Document type	Article
ZDB-ID	2572457-5
ISSN	1993-078X ; 1993-0771
ISSN (online)	1993-078X
ISSN	1993-0771
DOI	10.3897/CompCytogen.v13i2.34746
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Article: The chromosomes of Lepturinae (Coleoptera: Cerambycidae) II. A study of eight more species, with focus on Desmocerus palliatus

Dutrillaux, Anne-Marie / Dutrillaux, Bernard

Annales de la Société entomologique de France. 2019 July 4, v. 55, no. 4

2019

Abstract: Following the study of 28 species of Lepturinae (Coleoptera: Cerambycidae) the karyotypes of seven additional Palaearctic and one Nearctic species are established. The 19,X male karyotypes found in genera Stictoleptura (four species), Vadonia and Judolia ...

Abstract	Following the study of 28 species of Lepturinae (Coleoptera: Cerambycidae) the karyotypes of seven additional Palaearctic and one Nearctic species are established. The 19,X male karyotypes found in genera Stictoleptura (four species), Vadonia and Judolia (one species each) confirm the loss of Y chromosome in Lepturini. The 22,XY male karyotype of Cortodera humeralis is very close to that of some species of Rhagiini (genera Gaurotes, Acmaeops, Dinoptera, all 22,XY) and Grammoptera ruficornis (24,XY) recently reported. We propose that these taxa could form a monophyletic group within Rhagiini. The karyotype of the Nearctic species Desmocerus palliates (23,neoXneoXneoY) is quite different and characterized by the presence of many acrocentric chromosomes and a complex autosome–gonosome translocation. Its particular karyotype is compatible with its present classification within a separate tribe, the Desmocerini.
Keywords	acrocentric chromosomes ; Cerambycidae ; chromosome translocation ; karyotyping ; males ; monophyly ; Nearctic region ; Palearctic region ; Y chromosome
Language	English
Dates of publication	2019-0704
Size	p. 348-354.
Publishing place	Taylor & Francis
Document type	Article
ISSN	2168-6351
DOI	10.1080/00379271.2019.1637779
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Article ; Online: Improved Basic Cytogenetics Challenges Holocentricity of Butterfly Chromosomes.

Dutrillaux, Bernard / Dutrillaux, Anne-Marie / McClure, Mélanie / Gèze, Marc / Elias, Marianne / Bed'hom, Bertrand

Cytogenetic and genome research

2023 Volume 162, Issue 5, Page(s) 262–272

Abstract: Mitotic chromosomes of butterflies, which look like dots or short filaments in most published data, are generally considered to lack localised centromeres and thus to be holokinetic. This particularity, observed in a number of other invertebrates, is ... ...

Abstract	Mitotic chromosomes of butterflies, which look like dots or short filaments in most published data, are generally considered to lack localised centromeres and thus to be holokinetic. This particularity, observed in a number of other invertebrates, is associated with meiotic particularities known as "inverted meiosis," in which the first division is equational, i.e., centromere splitting-up and segregation of sister chromatids instead of homologous chromosomes. However, the accurate analysis of butterfly chromosomes is difficult because (1) their size is very small, equivalent to 2 bands of a mammalian metaphase chromosome, and (2) they lack satellite DNA/heterochromatin in putative centromere regions and therefore marked primary constrictions. Our improved conditions for basic chromosome preparations, here applied to 6 butterfly species belonging to families Nymphalidae and Pieridae challenges the holocentricity of their chromosomes: in spite of the absence of primary constrictions, sister chromatids are recurrently held together at definite positions during mitotic metaphase, which makes possible to establish karyotypes composed of acrocentric and submetacentric chromosomes. The total number of chromosomes per karyotype is roughly inversely proportional to that of non-acrocentric chromosomes, which suggests the occurrence of frequent robertsonian-like fusions or fissions during evolution. Furthermore, the behaviour and morphological changes of chromosomes along the various phases of meiosis do not seem to differ much from those of canonical meiosis. In particular, at metaphase II chromosomes clearly have 2 sister chromatids, which refutes that anaphase I was equational. Thus, we propose an alternative mechanism to holocentricity for explaining the large variations in chromosome numbers in butterflies: (1) in the ancestral karyotype, composed of about 62 mostly acrocentric chromosomes, the centromeres, devoid of centromeric heterochromatin/satellite DNA, were located at contact with telomeric heterochromatin; (2) the instability of telomeric heterochromatin largely contributed to drive the multiple rearrangements, principally chromosome fusions, which occurred during butterfly evolution.
MeSH term(s)	Humans ; Animals ; Butterflies/genetics ; Heterochromatin ; DNA, Satellite ; Chromosomes ; Centromere ; Meiosis ; Chromatids ; Karyotyping ; Mammals/genetics
Chemical Substances	Heterochromatin ; DNA, Satellite
Language	English
Publishing date	2023-01-23
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2087824-2
ISSN	1424-859X ; 1424-8581
ISSN (online)	1424-859X
ISSN	1424-8581
DOI	10.1159/000526034
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Article ; Online: Evolution of the Sex Chromosomes in Beetles. I. The Loss of the Y Chromosome.

Dutrillaux, Anne-Marie / Dutrillaux, Bernard

Cytogenetic and genome research

2017 Volume 152, Issue 2, Page(s) 97–104

Abstract: In the males of Coleoptera, the most frequent sex chromosome constitution is XY. At metaphase I of meiosis, the X and Y are linked by nucleolar proteins, forming the so-called parachute bivalent (Xyp), which is assumed to allow the non-synapsed X and Y ... ...

Abstract	In the males of Coleoptera, the most frequent sex chromosome constitution is XY. At metaphase I of meiosis, the X and Y are linked by nucleolar proteins, forming the so-called parachute bivalent (Xyp), which is assumed to allow the non-synapsed X and Y to segregate correctly at anaphase I. However, X0 males are not exceptional, and we explored the relationships between the X and nucleolar proteins in the absence of the Y chromosome in 6 species belonging to different families/subfamilies. Using C-banding and silver staining, we show that nucleolar proteins always remain in contact with the X until anaphase I. These proteins are generally more abundant than in the Xyp bivalent, may remain associated with the NOR during diakinesis, and frequently link the X to 1 or 2 autosomal bivalents, which seem to play the same role as the Y. This role may also be played by B chromosomes, which appear to be more frequent in X0 than in XY males. In conclusion, following Y chromosome loss, various strategies using nucleolar proteins have been developed to facilitate the migration of the unique X at meiotic anaphase I.
MeSH term(s)	Animals ; Biological Evolution ; Chromosome Banding ; Coleoptera/genetics ; Karyotype ; Male ; Sex Chromosomes/genetics ; Staining and Labeling ; Y Chromosome/genetics
Language	English
Publishing date	2017
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2087824-2
ISSN	1424-859X ; 1424-8581
ISSN (online)	1424-859X
ISSN	1424-8581
DOI	10.1159/000478075
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Article ; Online: Genome assembly of 3 Amazonian Morpho butterfly species reveals Z-chromosome rearrangements between closely related species living in sympatry.

Bastide, Héloïse / López-Villavicencio, Manuela / Ogereau, David / Lledo, Joanna / Dutrillaux, Anne-Marie / Debat, Vincent / Llaurens, Violaine

GigaScience

2023 Volume 12

Abstract: The genomic processes enabling speciation and species coexistence in sympatry are still largely unknown. Here we describe the whole-genome sequencing and assembly of 3 closely related species from the butterfly genus Morpho: Morpho achilles (Linnaeus, ... ...

Abstract	The genomic processes enabling speciation and species coexistence in sympatry are still largely unknown. Here we describe the whole-genome sequencing and assembly of 3 closely related species from the butterfly genus Morpho: Morpho achilles (Linnaeus, 1758), Morpho helenor (Cramer, 1776), and Morpho deidamia (Höbner, 1819). These large blue butterflies are emblematic species of the Amazonian rainforest. They live in sympatry in a wide range of their geographical distribution and display parallel diversification of dorsal wing color pattern, suggesting local mimicry. By sequencing, assembling, and annotating their genomes, we aim at uncovering prezygotic barriers preventing gene flow between these sympatric species. We found a genome size of 480 Mb for the 3 species and a chromosomal number ranging from 2n = 54 for M. deidamia to 2n = 56 for M. achilles and M. helenor. We also detected inversions on the sex chromosome Z that were differentially fixed between species, suggesting that chromosomal rearrangements may contribute to their reproductive isolation. The annotation of their genomes allowed us to recover in each species at least 12,000 protein-coding genes and to discover duplications of genes potentially involved in prezygotic isolation like genes controlling color discrimination (L-opsin). Altogether, the assembly and the annotation of these 3 new reference genomes open new research avenues into the genomic architecture of speciation and reinforcement in sympatry, establishing Morpho butterflies as a new eco-evolutionary model.
MeSH term(s)	Animals ; Sympatry ; Butterflies/genetics ; Biological Evolution ; Reproductive Isolation ; Sex Chromosomes
Language	English
Publishing date	2023-05-22
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2708999-X
ISSN	2047-217X ; 2047-217X
ISSN (online)	2047-217X
ISSN	2047-217X
DOI	10.1093/gigascience/giad033
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