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Novel X-linked genes revealed by quantitative polymerase chain reaction in the green anole, Anolis carolinensis.

ABSTRACT: The green anole, Anolis carolinensis (ACA), is the model reptile for a vast array of biological disciplines. It was the first nonavian reptile to have its genome fully sequenced. During the genome project, the XX/XY system of sex chromosomes homologous to chicken chromosome 15 (GGA15) was revealed, and 106 X-linked genes were identified. We selected 38 genes located on eight scaffolds in ACA and having orthologs located on GGA15, then tested their linkage to ACA X chromosome by using comparative quantitative fluorescent real-time polymerase chain reaction applied to male and female genomic DNA. All tested genes appeared to be X-specific and not present on the Y chromosome. Assuming that all genes located on these scaffolds should be localized to the ACA X chromosome, we more than doubled the number of known X-linked genes in ACA, from 106 to 250. While demonstrating that the gene content of chromosome X in ACA and GGA15 is largely conserved, we nevertheless showed that numerous interchromosomal rearrangements had occurred since the splitting of the chicken and anole evolutionary lineages. The presence of many ACA X-specific genes localized to distinct contigs indicates that the ACA Y chromosome should be highly degenerated, having lost a large amount of its original gene content during evolution. The identification of novel genes linked to the X chromosome and absent on the Y chromosome in the model lizard species contributes to ongoing research as to the evolution of sex determination in reptiles and provides important information for future comparative and functional genomics.

SUBMITTER: Rovatsos M

PROVIDER: S-EPMC4232536 | biostudies-literature | 2014 Nov

REPOSITORIES: biostudies-literature

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Novel X-linked genes revealed by quantitative polymerase chain reaction in the green anole, Anolis carolinensis.

Rovatsos Michail M Altmanová Marie M Pokorná Martina Johnson MJ Kratochvíl Lukáš L

G3 (Bethesda, Md.) 20140828 11

The green anole, Anolis carolinensis (ACA), is the model reptile for a vast array of biological disciplines. It was the first nonavian reptile to have its genome fully sequenced. During the genome project, the XX/XY system of sex chromosomes homologous to chicken chromosome 15 (GGA15) was revealed, and 106 X-linked genes were identified. We selected 38 genes located on eight scaffolds in ACA and having orthologs located on GGA15, then tested their linkage to ACA X chromosome by using comparative ...[more]

PMID: 25172916

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Project description:In allopatric species, reproductive isolation evolves through the accumulation of genetic incompatibilities. The degree of divergence required for complete reproductive isolation is highly variable across taxa, which makes the outcome of secondary contact between allopatric species unpredictable. Since before the Pliocene, two species of Anolis lizards, Anolis carolinensis and Anolis porcatus, have been allopatric, yet this period of independent evolution has not led to substantial species-specific morphological differentiation, and therefore, they might not be reproductively isolated. In this study, we determined the genetic consequences of localized, secondary contact between the native green anole, A. carolinensis, and the introduced Cuban green anole, A. porcatus, in South Miami. Using 18 microsatellite markers, we found that the South Miami population formed a genetic cluster distinct from both parental species. Mitochondrial DNA revealed maternal A. porcatus ancestry for 35% of the individuals sampled from this population, indicating a high degree of cytonuclear discordance. Thus, hybridization with A. porcatus, not just population structure within A. carolinensis, may be responsible for the genetic distinctiveness of this population. Using tree-based maximum-likelihood analysis, we found support for a more recent, secondary introduction of A. porcatus to Florida. Evidence that ~33% of the nuclear DNA resulted from a secondary introduction supports the hybrid origin of the green anole population in South Miami. We used multiple lines of evidence and multiple genetic markers to reconstruct otherwise cryptic patterns of species introduction and hybridization. Genetic evidence for a lack of reproductive isolation, as well as morphological similarities between the two species, supports revising the taxonomy of A. carolinensis to include A. porcatus from western Cuba. Future studies should target the current geographic extent of introgression originating from the past injection of genetic material from Cuban green anoles and determine the consequences for the evolutionary trajectory of green anole populations in southern Florida.

Project description:BackgroundTandem amino acid repeats are characterised by the consecutive recurrence of a single amino acid. They exhibit high rates of length mutations in addition to point mutations and have been proposed to be involved in genetic plasticity. Squamate reptiles (lizards and snakes) diversify in both morphology and physiology. The underlying mechanism is yet to be understood. In a previous phylogenomic analysis of reptiles, the density of tandem repeats in an anole lizard diverged heavily from that of the other reptiles. To gain further insight into the tandem amino acid repeats in squamates, we analysed the repeat content in the green anole (Anolis carolinensis) proteome and compared the amino acid repeats in a large orthologous protein data set from six vertebrates (the Western clawed frog, the green anole, the Chinese softshell turtle, the zebra finch, mouse and human).ResultsOur results revealed that the number of amino acid repeats in the green anole exceeded those found in the other five species studied. Species-only repeats were found in high proportion in the green anole but not in the other five species, suggesting that the green anole had gained many amino acid repeats in either the Anolis or the squamate lineage. Since the amino acid repeat containing genes in the green anole were highly enriched in genes related to transcription and development, an important family of developmental genes, i.e., the Hox family, was further studied in a wide collection of squamates. Abundant amino acid repeats were also observed, implying the general high tolerance of amino acid repeats in squamates. A particular enrichment of amino acid repeats was observed in the central class Hox genes that are known to be responsible for defining cervical to lumbar regions.ConclusionsOur study suggests that the abundant amino acid repeats in the green anole, and possibly in other squamates, may play a role in increasing the genetic variability, and contribute to the evolutionary diversity of this clade.

Dataset Information

Novel X-linked genes revealed by quantitative polymerase chain reaction in the green anole, Anolis carolinensis.

Publications

Novel X-linked genes revealed by quantitative polymerase chain reaction in the green anole, Anolis carolinensis.

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