Dataset Information

Exploring the genetic basis of adaptation to high elevations in reptiles: a comparative transcriptome analysis of two toad-headed agamas (genus Phrynocephalus).

ABSTRACT: High elevation adaptation offers an excellent study system to understand the genetic basis of adaptive evolution. We acquired transcriptome sequences of two closely related lizards, Phrynocephalus przewalskii from low elevations and P. vlangalii from high elevations. Within a phylogenetic framework, we compared their genomic data along with green anole, chicken and Chinese softshell turtle, and identified candidate genes and functional categories that are potentially linked to adaptation to high elevation environments. More than 100 million sequence reads were generated for each species via Illumina sequencing. A de novo assembly produced 70,919 and 62,118 transcripts for P. przewalskii and P. vlangalii, respectively. Based on a well-established reptile phylogeny, we detected 143 positively selected genes (PSGs) along the P. vlangalii lineage from the 7,012 putative orthologs using a branch-site model. Furthermore, ten GO categories and one KEGG pathway that are over-represented by PSGs were recognized. In addition, 58 GO categories were revealed to have elevated evolutionary rates along the P. vlangalii lineage relative to P. przewalskii. These functional analyses further filter out PSGs that are most likely involved in the adaptation process to high elevations. Among them, ADAM17, MD, and HSP90B1 likely contributed to response to hypoxia, and POLK likely contributed to DNA repair. Many other candidate genes involved in gene expression and metabolism were also identified. Genome-wide scan for candidate genes may serve as the first step to explore the genetic basis of high elevation adaptation. Detailed comparative study and functional verification are needed to solidify any conclusions. High elevation adaptation requires coordinated changes in multiple genes that involve various physiological and biochemical pathways; we hope that our genetic studies will provide useful directions for future physiological or molecular studies in reptiles as well as other poikilothermic species.

SUBMITTER: Yang W

PROVIDER: S-EPMC4227734 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Exploring the genetic basis of adaptation to high elevations in reptiles: a comparative transcriptome analysis of two toad-headed agamas (genus Phrynocephalus).

Yang Weizhao W Qi Yin Y Fu Jinzhong J

PloS one 20141111 11

High elevation adaptation offers an excellent study system to understand the genetic basis of adaptive evolution. We acquired transcriptome sequences of two closely related lizards, Phrynocephalus przewalskii from low elevations and P. vlangalii from high elevations. Within a phylogenetic framework, we compared their genomic data along with green anole, chicken and Chinese softshell turtle, and identified candidate genes and functional categories that are potentially linked to adaptation to high ...[more]

PMID: 25386640

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Project description:We hypothesize the phylogenetic relationships of the agamid genus Phrynocephalus to assess how past environmental changes shaped the evolutionary and biogeographic history of these lizards and especially the impact of paleogeography and climatic factors. Phrynocephalus is one of the most diverse and taxonomically confusing lizard genera. As a key element of Palearctic deserts, it serves as a promising model for studies of historical biogeography and formation of arid habitats in Eurasia. We used 51 samples representing 33 of 40 recognized species of Phrynocephalus covering all major areas of the genus. Molecular data included four mtDNA (COI, ND2, ND4, Cytb; 2,703 bp) and four nuDNA protein-coding genes (RAG1, BDNF, AKAP9, NKTR; 4,188 bp). AU-tests were implemented to test for significant differences between mtDNA- and nuDNA-based topologies. A time-calibrated phylogeny was estimated using a Bayesian relaxed molecular clock with nine fossil calibrations. We reconstructed the ancestral area of origin, biogeographic scenarios, body size, and the evolution of habitat preference. Phylogenetic analyses of nuDNA genes recovered a well-resolved and supported topology. Analyses detected significant discordance with the less-supported mtDNA genealogy. The position of Phrynocephalus mystaceus conflicted greatly between the two datasets. MtDNA introgression due to ancient hybridization best explained this result. Monophyletic Phrynocephalus contained three main clades: (I) oviparous species from south-western and Middle Asia; (II) viviparous species of Qinghai-Tibetan Plateau (QTP); and (III) oviparous species of the Caspian Basin, Middle and Central Asia. Phrynocephalus originated in late Oligocene (26.9 Ma) and modern species diversified during the middle Miocene (14.8-13.5 Ma). The reconstruction of ancestral areas indicated that Phrynocephalus originated in Middle East-southern Middle Asia. Body size miniaturization likely occurred early in the history of Phrynocephalus. The common ancestor of Phrynocephalus probably preferred sandy substrates with the inclusion of clay or gravel. The time of Agaminae radiation and origin of Phrynocephalus in the late Oligocene significantly precedes the landbridge between Afro-Arabia and Eurasia in the Early Miocene. Diversification of Phrynocephalus coincides well with the mid-Miocene climatic transition when a rapid cooling of climate drove progressing aridification and the Paratethys salinity crisis. These factors likely triggered the spreading of desert habitats in Central Eurasia, which Phrynocephalus occupied. The origin of the viviparous Tibetan clade has been associated traditionally with uplifting of the QTP; however, further studies are needed to confirm this. Progressing late Miocene aridification, the decrease of the Paratethys Basin, orogenesis, and Plio-Pleistocene climate oscillations likely promoted further diversification within Phrynocephalus. We discuss Phrynocephalus taxonomy in scope of the new analyses.

Project description:Intraspecific rearrangements of mitochondrial genomes are rarely reported in reptiles, even in vertebrates. The sunwatcher toad-headed agama, Phryncoephalus helioscopus, can serve as an excellent model for investigating the dynamic mitogenome structure at intraspecific level. To date, seven subspecies of P. helioscopus are well recognized, but little is known about the mitogenomic evolution among different subspecies. In this study, complete mitogenomes of subspecies P. helioscopus varius II and P. helioscopus cameranoi were determined by next-generation sequencing, and another P. helioscopus varius I retrieved from GenBank was compiled for comparative analysis. The nucleotide composition and the codon usage are similar to those previously published from toad-headed agamas. P. helioscopus varius II and P. helioscopus cameranoi have 23 tRNA genes, including standard 22 tRNA genes and one extra tRNA-Phe (tRNA-Phe duplication). Gene order and phylogenetic analyses in the genus Phrynocephalus support prevalent intraspecific gene rearrangement in P. helioscopus and other congener species including P. erythrurus, P. vlangalii, and P. forsythii. Six different mitochondrial gene arrangements are observed in Phrynocephalus. Overall, the occurrence of rearrangements may result from multiple independent structural dynamic events. The split of the two subspecies in P. helioscopus was dated at approximately 2.34 million years ago (Ma). Two types of gene rearrangements are found in the three mitogenomes of P. helioscopus, and this intraspecific rearrangement phenomenon can be explained by the tandem duplication/random loss (TDRL) model. Post duplication, the alternative loss types can occur in 0.23-0.72 Ma, suggesting that the duplication and fixation of these rearrangements can occur quite quickly. These findings highlight the need for more mitogenomes at the population level in order to better understand the potentially rampant intraspecific mitogenomic reorganization in Phrynocephalus.

Dataset Information

Exploring the genetic basis of adaptation to high elevations in reptiles: a comparative transcriptome analysis of two toad-headed agamas (genus Phrynocephalus).

Publications

Exploring the genetic basis of adaptation to high elevations in reptiles: a comparative transcriptome analysis of two toad-headed agamas (genus Phrynocephalus).

Similar Datasets

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