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Evolution of beak morphology in the Ground Tit revealed by comparative transcriptomics.

ABSTRACT: Background:Beak morphology exhibits considerable adaptive plasticity in birds, which results in highly varied or specialized forms in response to variations in ecology and life history. As the only parid species endemic to the Qinghai-Tibet Plateau, the Ground Tit (Parus humilis) has evolved a distinctly long and curved beak from other parids. An integration of morphometrics, phylogenetics, transcriptomics and embryology allows us to address the evolutionary and developmental mechanisms of the adaptive beak structure observed in the Ground Tit. Results:A morphometric approach quantified that the Ground Tit has a comparatively longer and more decurved upper beaks than other parids. We estimated that the ancestor of the Ground Tit likely had a short straight upper beak similar to most current recognized parid species using an ancestral state reconstruction. This morphological specialization is considered an adaptation to its ground-oriented behavior on the high plateau. To identify genetic mechanisms behind this adaptive change, a comparative transcriptomic analysis was applied between the Ground Tit and its closely related species, the Great Tit (Parus major). We detected that 623 genes were significantly differentially expressed in embryonic upper beaks between the two species, 17 of which were functionally annotated to correlate with bone development and morphogenesis, although genes related to bone development were not found to undergo accelerated evolution in the Ground Tit. RT-qPCR validation confirmed differential expression of five out of eight genes that were selected from the 17 genes. Subsequent functional assays in chicken embryos demonstrated that two of these genes, FGF13 and ITGB3, may affect beak morphology by modulating levels of osteoblasts and osteoclasts. Conclusions:Our results provide preliminary evidence that development of the long decurved beak of the Ground Tit is likely regulated by transcriptional activities of multiple genes coordinating osteoblasts and osteoclasts. The integration of multiple approaches employed here sheds light on ecological and genetic mechanisms in the evolution of avian morphology.

SUBMITTER: Cheng Y

PROVIDER: S-EPMC5740785 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Evolution of beak morphology in the Ground Tit revealed by comparative transcriptomics.

Cheng Yalin Y Gao Bin B Wang Haitao H Han Naijian N Shao Shimiao S Wu Shaoyuan S Song Gang G Zhang Yong E YE Zhu Xiaojia X Lu Xin X Qu Yanhua Y Lei Fumin F

Frontiers in zoology 20171221

<h4>Background</h4>Beak morphology exhibits considerable adaptive plasticity in birds, which results in highly varied or specialized forms in response to variations in ecology and life history. As the only parid species endemic to the Qinghai-Tibet Plateau, the Ground Tit (<i>Parus humilis</i>) has evolved a distinctly long and curved beak from other parids. An integration of morphometrics, phylogenetics, transcriptomics and embryology allows us to address the evolutionary and developmental mech ...[more]

PMID: 29299037

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Project description:BackgroundMorphological characters of birds reflect their adaptive evolution and ecological requirements and are also relevant to phylogenetic relationships within a group of related species. The tits (Paridae) are known to be outwardly homogeneous in shape, with one aberrant member, the Ground Tit (Pseudopodoces humilis), which is quite different from its relatives in both body morphology and beak shape. We combined traditional measurements and geometric morphometrics to quantify the variation in body morphology and beak shape of 14 Paridae species distributed in China. Based on these results, we sought to assess the contribution of phylogeny, altitude and species interactions to the evolution of morphological traits.ResultsThe basic features for discriminating among the 14 species studied here were overall body size, the ratio of body and tail length to culmen and tarsus length, and beak shape (long/slender/pointy vs. short/robust/blunt). These dimensions clearly separate Ps. humilis and Melanochlora sultanea from the other species in shape space. Body length and PC3 of beak shape (round outline vs. straight outline) show significant phylogenetic signals. Across 14 species, altitude is related to tarsus, culmen length and PC1 of beak shape. Within Parus major, altitude is related to body weight, body length, culmen length and PC1 of body morphology. Morphological distances and geographic distances among species are positively correlated.ConclusionsThe body morphology of Paridae species shows extensive evolutionary changes, while their beak has mainly evolved along the long/slender/pointy vs. short/robust/blunt dimension. Only body length and beak curvature show a phylogenetic signal. Altitude correlates with multiple traits both across and within species, suggesting that altitude is an important factor in promoting morphological divergence. The deviant appearance of Ps. humilis corresponds to its foraging and feeding adaptations to high-altitude steppe habitats. Our results also show a higher level of morphological divergence with greater difference in distribution ranges among the Paridae species involved in this study.

Dataset Information

Evolution of beak morphology in the Ground Tit revealed by comparative transcriptomics.

Publications

Evolution of beak morphology in the Ground Tit revealed by comparative transcriptomics.

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