New insights into sex chromosome evolution in anole lizards (Reptilia, Dactyloidae)

Giovannotti, Massimo; Trifonov, Vladimir A.; Paoletti, Alessio; Kichigin, Ilya G.; O’Brien, Patrícia C. M.; Kasai, Fumie; Giovagnoli, Giacomo; Ng, Bee Ling; Ruggeri, Paolo; Cerioni, Paola Nisi; Splendiani, Andrea; Pereira, Jorge C.; Olmo, Ettore; Rens, Willem; Barucchi, Vincenzo Caputo; Ferguson-Smith, Malcolm A.

doi:10.1007/s00412-016-0585-6

Cited by 33 publications

(65 citation statements)

References 32 publications

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“…This opened the opportunity to study the functional evolution of an amniote male heterogametic sex chromosome system outside of mammals. The distribution and karyotypic patterns of this XY system within the large Anolis genus and its presence in other (pleurodont) lizards has been established (Rovatsos et al 2014a,c;Giovannotti et al 2016), and a recent study made initial suggestions regarding the evolution of dosage compensation in this system based on expression data for green anole tail samples (Rupp et al 2017). However, a detailed genome-scale investigation of the origins and functional evolution of the Anolis XY system has been lacking.…”

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confidence: 99%

Convergent origination of aDrosophila-like dosage compensation mechanism in a reptile lineage

Cortez²,

et al. 2017

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Sex chromosomes differentiated from different ancestral autosomes in various vertebrate lineages. Here, we trace the functional evolution of the XY Chromosomes of the green anole lizard (Anolis carolinensis), on the basis of extensive high-throughput genome, transcriptome and histone modification sequencing data and revisit dosage compensation evolution in representative mammals and birds with substantial new expression data. Our analyses show that Anolis sex chromosomes represent an ancient XY system that originated at least ≈160 million years ago in the ancestor of Iguania lizards, shortly after the separation from the snake lineage. The age of this system approximately coincides with the ages of the avian and two mammalian sex chromosomes systems. To compensate for the almost complete Y Chromosome degeneration, X-linked genes have become twofold up-regulated, restoring ancestral expression levels. The highly efficient dosage compensation mechanism of Anolis represents the only vertebrate case identified so far to fully support Ohno's original dosage compensation hypothesis. Further analyses reveal that X up-regulation occurs only in males and is mediated by a male-specific chromatin machinery that leads to global hyperacetylation of histone H4 at lysine 16 specifically on the X Chromosome. The green anole dosage compensation mechanism is highly reminiscent of that of the fruit fly, Drosophila melanogaster. Altogether, our work unveils the convergent emergence of a Drosophila-like dosage compensation mechanism in an ancient reptilian sex chromosome system and highlights that the evolutionary pressures imposed by sex chromosome dosage reductions in different amniotes were resolved in fundamentally different ways.

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confidence: 99%

Convergent origination of aDrosophila-like dosage compensation mechanism in a reptile lineage

Cortez²,

et al. 2017

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“…In other anole species studied by Giovannotti et al [2016], the decrease in affinity affected only Y chromosomes, suggesting their independent degeneration in different lineages.…”

Section: Discussionmentioning

confidence: 99%

“…Morphological and genetic differentiation between their X and Y chromosomes remains understudied [Rovatsos et al, 2014a;Giovannotti et al, 2016]. Comparison of the sex chromosome structure in these distant anole species will provide information for the tentative reconstruction of the ancestral sex chromosomes in Dactyloidae including the intrachromosomal changes that occurred in different lineages.…”

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confidence: 99%

“…The sex chromosomes of the pleurodont iguanians vary in their degree of morphological differentiation [Gamble et al, 2014;Altmanová et al, 2016]. Giovannotti et al [2016] describe several chromosome fusions that appear in different lineages of anoles (Dactyloidae) leading to well-differentiated sex chromosomes and systems with multiple sex chromosomes (such as the X 1 X 2 X 1 X 2 /X 1 X 2 Y system in Ctenonotus pogus and C. sabanus and the XX/XY system in Norops). Fused with several ancestral autosomal microchromosomes, the sex chromosomes of these species became larger and can be considered as macrochromosomes, especially in Norops.…”

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Heteromorphism of “Homomorphic” Sex Chromosomes in Two Anole Species (Squamata, Dactyloidae) Revealed by Synaptonemal Complex Analysis

Lisachov

Trifonov

Giovannotti

et al. 2017

Cytogenet Genome Res

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Iguanians (Pleurodonta) are one of the reptile lineages that, like birds and mammals, have sex chromosomes of ancient origin. In most iguanians these are microchromosomes, making a distinction between the X and Y as well as between homeologous sex chromosomes in other species difficult. Meiotic chromosome analysis may be used to elucidate their differentiation, because meiotic prophase chromosomes are longer and less condensed than metaphase chromosomes, and the homologues are paired with each other, revealing minor heteromorphisms. Using electron and fluorescent microscopy of surface spread synaptonemal complexes (SCs) and immunolocalization of the proteins of the SC (SYCP3), the centromere, and recombination nodules (MLH1), we examined sex chromosome synapsis and recombination in 2 species of anoles (Dactyloidae), Anolis carolinensis and Deiroptyx coelestinus, in which the sex chromosomes represent the ancestral condition of iguanians. We detected clear differences in size between the anole X and Y microchromosomes and found an interspecies difference in the localization of the pseudoautosomal region. Our results show that the apparent homomorphy of certain reptile sex chromosome systems can hide a cryptic differentiation, which potentially may influence the evolution of sexual dimorphism and speciation.

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“…However, several large reptile groups possess ancient sex chromosome systems of common origin. The most known and best-studied of them are the higher snakes (Caenophidia) [Rovatsos et al, 2015], the pleurodont iguanian lizards (Pleurodonta; Iguanidae sensu lato) [Gamble et al, 2014;Rovatsos et al, 2014;Giovannotti et al, 2017], and the lacertid lizards [Rovatsos et al, 2016].…”

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Genetic Content of the Neo-Sex Chromosomes in Ctenonotus and Norops (Squamata, Dactyloidae) and Degeneration of the Y Chromosome as Revealed by High-Throughput Sequencing of Individual Chromosomes

Lisachov

Makunin

Giovannotti

et al. 2019

Cytogenet Genome Res

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Pleurodont lizards are characterized by an ancient system of sex chromosomes. Along with stability of the central component of the system (homologous to the X chromosome of Anolis carolinensis [Dactyloidae], ACAX), in some genera the ancestral sex chromosomes are fused with microautosomes, forming neo-sex chromosomes. The genus Ctenonotus (Dactyloidae) is characterized by multiple X₁X₁X₂X₂/X₁X₂Y sex chromosomes. According to cytogenetic data, the large neo-Y chromosome is formed by fusion of the ancestral Y chromosome with 2 microautosomes (homologous to ACA10 or ACA11 and ACA12), the X₁ chromosome is formed by fusion of the ancestral X chromosome with the autosome homologous to ACA10 or ACA11, and the X₂ chromosome is homologous to autosome ACA12. To determine more precisely the content and evolution of the Ctenonotus sex chromosomes, we sequenced flow-sorted chromosomes (both sex chromosomes and microautosomes as control) of 2 species with a similar system: C. pogus and C. sabanus. Our results indicate that the translocated part of the X₁ is homologous to ACA11, X₂ is homologous to ACA12, and the Y contains segments homologous to both ACA11 and ACA12. Molecular divergence estimates suggest that the ancestral X-derived part has completely degenerated in the Y of Ctenonotus, similar to the degeneration of the Norops sagrei Y chromosome (Dactyloidae). The newly added regions show loss of DNA content, but without degeneration of the conserved regions. We hypothesize that the translocation of autosomal blocks onto sex chromosomes facilitated rapid degeneration of the pseudoautosomal region on the ancestral Y.

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New insights into sex chromosome evolution in anole lizards (Reptilia, Dactyloidae)

Cited by 33 publications

References 32 publications

Convergent origination of aDrosophila-like dosage compensation mechanism in a reptile lineage

Convergent origination of aDrosophila-like dosage compensation mechanism in a reptile lineage

Heteromorphism of “Homomorphic” Sex Chromosomes in Two Anole Species (Squamata, Dactyloidae) Revealed by Synaptonemal Complex Analysis

Genetic Content of the Neo-Sex Chromosomes in <b><i>Ctenonotus</i></b> and <b><i>Norops</i></b> (Squamata, Dactyloidae) and Degeneration of the Y Chromosome as Revealed by High-Throughput Sequencing of Individual Chromosomes

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