Dataset Information

Divergent and parallel routes of biochemical adaptation in high-altitude passerine birds from the Qinghai-Tibet Plateau.

ABSTRACT: When different species experience similar selection pressures, the probability of evolving similar adaptive solutions may be influenced by legacies of evolutionary history, such as lineage-specific changes in genetic background. Here we test for adaptive convergence in hemoglobin (Hb) function among high-altitude passerine birds that are native to the Qinghai-Tibet Plateau, and we examine whether convergent increases in Hb-O₂ affinity have a similar molecular basis in different species. We documented that high-altitude parid and aegithalid species from the Qinghai-Tibet Plateau have evolved derived increases in Hb-O₂ affinity in comparison with their closest lowland relatives in East Asia. However, convergent increases in Hb-O₂ affinity and convergence in underlying functional mechanisms were seldom attributable to the same amino acid substitutions in different species. Using ancestral protein resurrection and site-directed mutagenesis, we experimentally confirmed two cases in which parallel substitutions contributed to convergent increases in Hb-O₂ affinity in codistributed high-altitude species. In one case involving the ground tit (Parus humilis) and gray-crested tit (Lophophanes dichrous), parallel amino acid replacements with affinity-enhancing effects were attributable to nonsynonymous substitutions at a CpG dinucleotide, suggesting a possible role for mutation bias in promoting recurrent changes at the same site. Overall, most altitude-related changes in Hb function were caused by divergent amino acid substitutions, and a select few were caused by parallel substitutions that produced similar phenotypic effects on the divergent genetic backgrounds of different species.

SUBMITTER: Zhu X

PROVIDER: S-EPMC5828625 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Divergent and parallel routes of biochemical adaptation in high-altitude passerine birds from the Qinghai-Tibet Plateau.

Zhu Xiaojia X Guan Yuyan Y Signore Anthony V AV Natarajan Chandrasekhar C DuBay Shane G SG Cheng Yalin Y Han Naijian N Song Gang G Qu Yanhua Y Moriyama Hideaki H Hoffmann Federico G FG Fago Angela A Lei Fumin F Storz Jay F JF

Proceedings of the National Academy of Sciences of the United States of America 20180205 8

When different species experience similar selection pressures, the probability of evolving similar adaptive solutions may be influenced by legacies of evolutionary history, such as lineage-specific changes in genetic background. Here we test for adaptive convergence in hemoglobin (Hb) function among high-altitude passerine birds that are native to the Qinghai-Tibet Plateau, and we examine whether convergent increases in Hb-O<sub>2</sub> affinity have a similar molecular basis in different specie ...[more]

PMID: 29432191

Similar Datasets

Project description:Background and aimsExploring how species diverge is vital for understanding the drivers of speciation. Factors such as geographical separation and ecological selection, hybridization, polyploidization and shifts in mating system are all major mechanisms of plant speciation, but their contributions to divergence are rarely well understood. Here we test these mechanisms in two plant species, Gentiana lhassica and G. hoae, with the goal of understanding recent allopatric species divergence on the Qinghai-Tibet Plateau (QTP).MethodsWe performed Bayesian clustering, phylogenetic analysis and estimates of hybridization using 561 302 nuclear genomic single nucleotide polymorphisms (SNPs). We performed redundancy analysis, and identified and annotated species-specific SNPs (ssSNPs) to explore the association between climatic preference and genetic divergence. We also estimated genome sizes using flow cytometry to test for overlooked polyploidy.Key resultsGenomic evidence confirms that G. lhassica and G. hoae are closely related but distinct species, while genome size estimates show divergence occurred without polyploidy. Gentiana hoae has significantly higher average FIS values than G. lhassica. Population clustering based on genomic SNPs shows no signature of recent hybridization, but each species is characterized by a distinct history of hybridization with congeners that has shaped genome-wide variation. Gentiana lhassica has captured the chloroplast and experienced introgression with a divergent gentian species, while G. hoae has experienced recurrent hybridization with related taxa. Species distribution modelling suggested range overlap in the Last Interglacial Period, while redundancy analysis showed that precipitation and temperature are the major climatic differences explaining the separation of the species. The species differ by 2993 ssSNPs, with genome annotation showing missense variants in genes involved in stress resistance.ConclusionsThis study suggests that the distinctiveness of these species on the QTP is driven by a combination of hybridization, geographical isolation, mating system differences and evolution of divergent climatic preferences.

Project description:BackgroundOrganisms living at high altitudes must overcome three major environmental challenges: hypoxia, cold, and intense UV radiation. The molecular mechanisms that enable these challenges to be overcome have mainly been studied in endothermic organisms; relatively little attention has been paid to poikilothermic species. Here, we present deep transcriptome sequencing in two closely related lizards, the high altitude-dwelling Phrynocephalus erythrurus and the lowland-dwelling P. putjatia, to identify candidate genes under positive selection and to explore the convergent evolutionary adaptation of poikilothermic animals to high altitude life.ResultsMore than 70 million sequence reads were generated for each species via Illumina sequencing. De novo assembly produced 56,845 and 63,140 transcripts for P. erythrurus and P. putjatia, respectively. P. erythrurus had higher Ka/Ks ratios than P. putjatia, implying an accelerated evolutionary rate in the high altitude lizard lineage. 206 gene ontology (GO) categories with accelerated evolutionary rates and 43 candidate positively selected genes were detected along the P. erythrurus lineage. Some of these GO categories have functions associated with responses to hypoxia, energy metabolism and responses to UV damage. We also found that the high-altitude ranid frog R. kukunoris had higher Ka/Ks ratios than the closely related low-altitude frog R. chensinensis, and that the functional categories with accelerated evolutionary rates in R. kukunoris overlapped extensively with those detected along the P. erythrurus lineage.ConclusionsThe mechanisms of high altitude adaptation in P. erythrurus were tentatively inferred. By comparing two pairs of low- and high-altitude poikilothermic species, we found that similar functional categories had undergone positive selection in high altitude-dwelling Phrynocephalus and Rana lineages, indicating that similar mechanisms of adaptation to high altitude might have evolved in both genera. Our findings provide important guidance for future functional studies on high altitude adaptation in poikilothermic animals.

Project description:BackgroundThe arid region of the Qinghai-Tibet Plateau has a harsh natural environment that spans a vast altitudinal range, where plant growth suffers from various environmental stresses such as low temperature and drought. Shrubs are one of the most important plant functional groups in this region, and different shrub types have developed various nutrient strategies in response to these environmental stresses. However, nutrient characteristics and biogeographical patterns in different shrub types have seldom been investigated. The aboveground concentrations of carbon (C), nitrogen (N), and phosphorus (P) of the three shrub types (leaf-normal, leaf-reduced, and succulent shrubs) and soil physicochemical properties were measured in 138 sampling sites in the arid region of the Qinghai-Tibet Plateau.ResultsMean C, N, and P concentrations in all shrubs were 382.09 mg/g, 24.63 mg/g, and 1.43 mg/g in the arid region of the Qinghai-Tibet Plateau. Mean C, N, and P concentrations were 347.64, 24.30, and 1.25 mg/g in succulent shrubs, which were significantly lower than those of leaf-normal shrubs (C: 418.43 mg/g; N: 24.57 mg/g; P: 1.55 mg/g) and leaf-reduced shrubs (C: 399.71 mg/g; N: 25.96 mg/g; P: 1.65 mg/g). With increasing in longitude, C, N, and P concentrations in leaf-normal and leaf-reduced shrubs increased but these nutrients in succulent shrubs decreased. Increasing altitude only increased N and P concentrations for leaf-normal shrubs. These results demonstrated that the three shrub types had divergent nutrient biogeographical patterns. N and P concentrations of leaf-normal and leaf-reduced shrubs were directly driven by soil total N and total P concentrations and indirectly regulated by mean annual temperature and mean annual precipitation, promoting the formation of longitude or altitude nutrient patterns. Meanwhile, N and P concentrations in succulent shrubs were only regulated by soil pH, total N, and total P concentrations, driving the formation of longitude nutrient patterns. These results indicated divergent driving factors for nutrient biogeographical patterns among the three shrub types.ConclusionsOur study highlights the unique nutrient characteristics of succulent shrubs, reveals driving factors of nutrient biogeographical patterns in the three shrub types, and contributes to the understanding of biogeochemical cycling in arid ecosystems.

Dataset Information

Divergent and parallel routes of biochemical adaptation in high-altitude passerine birds from the Qinghai-Tibet Plateau.

Publications

Divergent and parallel routes of biochemical adaptation in high-altitude passerine birds from the Qinghai-Tibet Plateau.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets