Anchoring genome sequence to chromosomes of the central bearded dragon (Pogona vitticeps) enables reconstruction of ancestral squamate macrochromosomes and identifies sequence content of the Z chromosome

Abstract

BackgroundSquamates (lizards and snakes) are a speciose lineage of reptiles displaying considerable karyotypic diversity, particularly among lizards. Understanding the evolution of this diversity requires comparison of genome organisation between species. Although the genomes of several squamate species have now been sequenced, only the green anole lizard has any sequence anchored to chromosomes. There is only limited gene mapping data available for five other squamates. This makes it difficult to reconstruct the events that have led to extant squamate karyotypic diversity. The purpose of this study was to anchor the recently sequenced central bearded dragon (Pogona vitticeps) genome to chromosomes to trace the evolution of squamate chromosomes. Assigning sequence to sex chromosomes was of particular interest for identifying candidate sex determining genes.ResultsBy using two different approaches to map conserved blocks of genes, we were able to anchor approximately 42 % of the dragon genome sequence to chromosomes. We constructed detailed comparative maps between dragon, anole and chicken genomes, and where possible, made broader comparisons across Squamata using cytogenetic mapping information for five other species. We show that squamate macrochromosomes are relatively well conserved between species, supporting findings from previous molecular cytogenetic studies. Macrochromosome diversity between members of the Toxicofera clade has been generated by intrachromosomal, and a small number of interchromosomal, rearrangements. We reconstructed the ancestral squamate macrochromosomes by drawing upon comparative cytogenetic mapping data from seven squamate species and propose the events leading to the arrangements observed in representative species. In addition, we assigned over 8 Mbp of sequence containing 219 genes to the Z chromosome, providing a list of genes to begin testing as candidate sex determining genes.ConclusionsAnchoring of the dragon genome has provided substantial insight into the evolution of squamate genomes, enabling us to reconstruct ancestral macrochromosome arrangements at key positions in the squamate phylogeny, demonstrating that fusions between macrochromosomes or fusions of macrochromosomes and microchromosomes, have played an important role during the evolution of squamate genomes. Assigning sequence to the sex chromosomes has identified NR5A1 as a promising candidate sex determining gene in the dragon.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2774-3) contains supplementary material, which is available to authorized users.

Isolating Chromosomes of the Komodo Dragon: New Tools for Comparative Mapping and Sequence Assembly

“…Among reptiles, preliminary cytogenetic maps are currently available for the Japanese four-striped snake Elaphe quadrivirgata [Srikulnath et al, 2009] and 6 species of lizards, including the central bearded dragon Pogona vitticeps [Young et al, 2013], the water monitor lizard Varanus salvator macromaculatus , the savannah monitor lizard V. exanthematicus [Srikulnath et al, 2013], the butterfly lizard Leiolepis reevesii [Srikulnath et al, 2009], the sand lizard Lacerta agilis [Srikulnath et al, 2014], and the Hokou gecko Gekko hokouensis [Srikulnath et al, 2015]. Among them, the P. vitticeps map has recently been improved by the work of Deakin et al [2016] who anchored 42% of the genome sequences to chromosomes. Highquality chromosomal maps, however, are available only for 2 species, the green anole A. carolinensis [Alföldi et al, 2011] and the painted turtle Chrysemys picta [Badenhorst et al, 2015], making it difficult to conduct detailed studies on the evolution of genomes and chromosomal rearrangements in reptiles.…”

Sex Reversal in Reptiles: Reproductive Oddity or Powerful Driver of Evolutionary Change?

“…1 ). Recapitulating this point, we observe that the 3 currently identified reptile candidate sex-determining genes are different in squamates ( NR5A1 P. vitticeps; Deakin et al [2016]) and testudines ( WT1 Glyptemys insculpta; Montiel et al [2016] and CIRBP Chelydra serpentina; Schroeder et al [2016] There has been significant concern in the literature about the future of TSD reptiles under climate scenarios with rapid warming events [Cotton and Wedekind, 2009;Sinervo et al, 2010;Boyle et al, 2014]. This is a legitimate concern and indeed the recent discovery of an increasing rate of sex reversal in wild bearded dragon populations suggests that climatic extremes have the potential to perturb even seemingly stable GSD systems [Holleley et al, 2015].…”

ZZ/ZW Sex Chromosomes in the Endemic Puerto Rican Leaf-Toed Gecko (<b><i>Phyllodactylus wirshingi</i></b>)

“…Furthermore, such data do not address which chromosomes in the genome are the sex chromosomes in a comparative framework. However, recent advances in both cytogenetics and DNA sequencing techniques have facilitated the identification of sex chromosomes in many additional species, spawning a renewed interest in ascertaining and classifying the sex chromosome systems of previously intractable taxa [Pokorná et al, 2011;Deakin et al, 2016;Gamble et al, 2017Gamble et al, , 2018Nielsen et al, 2018].…”