Significance: Harsh conditions in high elevations present strong stresses for organisms. Previous studies targeting phylogenetically distinct species revealed cases of diversified adaptations, but it remains largely unknown how common ancestry contributes to evolution of similar adaptations. Our study based on a species complex (snowfinches) living on Qinghai–Tibet Plateau shows that ancestral snowfinches had phenotypically evolved larger body size and genetically an accelerated selection on genes related to development and signaling. From this ancestral state of adaptation three descendants have undergone independent adaptive processes in response to the differences in selective pressures acting on them. A striking example is a DNA repair gene, DTL , in which nonsynonymous substitutions evolving in ancestor and descendants have led to different DNA damage repair kinetics.

Exposure to a hypoxic environment at high altitudes imposes severe pressure on animals living there, which utilize substantial cardiovascular and respiratory responses to meet the physiological challenge of oxygen requirement. These responses may result from phenotypic plasticity through short‐term exposure (i.e., within a generation) to a new environment or shaped by adaptation (i.e., many generations) through long‐term evolution. For example, plasticity triggers a sympathetic‐mediated adrenergic response, resulting in an elevation of heart rate and hypoxia‐induced pulmonary vasoconstriction that eventually contributes to pulmonary hypertension in some animals. Adaptation to high altitudes can drive an increase in muscular capillarization and adaptive cardiac growth, which promote oxygen diffusion and transportation. Exposure to a high‐altitude hypoxic environment stimulates excessive erythropoiesis, which has maladaptive effects and contributes to chronic mountain sickness. Maladaptation caused by plasticity at early stages can be reversed during adaptation. Despite extensive research on high‐altitude adaptation, the phenotypic changes and genetic variations in cardiovascular systems responding to high‐altitude hypoxia remain insufficiently integrated across taxa. While genomic and transcriptomic studies have advanced our understanding, a cross‐taxa comparison of cardiovascular adaptations is still incomplete. We here review recent literature on phenotypic plasticity, adaptations, and genetic and transcriptional basis of cardiovascular systems of mammals and birds living in high altitudes with respect to their duration of exposure at high altitudes. By integrating and comparing data across mammalian and avian species, we aim to provide a framework for understanding the plasticity and adaptation of the cardiovascular system in high‐altitude environments.

Aim Species living in a shared environment face similar selective pressures and often evolve adaptive divergence to avoid competition. Quantifying phenotypic divergence and its genetic parallelism among sympatric species is important for understanding of ecologically moderated biodiversity. Here, we integrate ecologic, phenotypic and genomic datasets to study to what extent three sympatrically snowfinches (Montifringilla adamsi, Pyrgilauda ruficollis and Onychostruthus taczanowskii) differ in their adaptations in order to co-exist in a shared environment. Location Qinghai–Tibetan Plateau. Methods We used principal component analysis to summarize and compare environmental and phenotypic divergence. We compared phenotypes relevant to body and beak sizes (n = 68) because they are indicators of niche and food segregation, thus critical for establishing co-existence of sympatric birds. We used comparative genomics (n = 33) to identify genetic loci that are highly divergent between species as well as loci unique for each of species. Using vector analyses, we integrated correlation and permutation to quantify parallelism between phenotypic and genetic divergences. Results We found that body and beak sizes are significantly different among three snowfinches. The phenotypic differentiations are greater in species that share similar ecological conditions than in those that do not. We showed that genes related to developmental process are over-represented within highly divergent genomic regions and unique genetic loci of each species. We found that the extent of phenotypic divergence between snowfinch pairs is more strongly correlated with the magnitude of divergence in developmental genes than in the whole genome. Main conclusions Adaptive divergence of sympatric snowfinches is highly constrained on developmental genes. As this genetic divergence is strongly correlated with divergence of the traits related to segregation in niche and food resources, this correlation reflects either causal effects or indirect consequences of ecological mediated changes. Our study provides novel insights into the mechanisms underlying evolutionary versatility and ecological success among sympatric species.

Phenotypic plasticity facilitates organismal invasion of novel environments, and the resultant phenotypic change may later be modified by genetic change, so called ‘plasticity first.’ Herein, we quantify gene expression plasticity and regulatory adaptation in a wild bird (Eurasian Tree Sparrow) from its original lowland (ancestral stage), experimentally implemented hypoxia acclimation (plastic stage), and colonized highland (colonized stage). Using a group of co-expressed genes from the cardiac and flight muscles, respectively, we demonstrate that gene expression plasticity to hypoxia tolerance is more often reversed than reinforced at the colonized stage. By correlating gene expression change with muscle phenotypes, we show that colonized tree sparrows reduce maladaptive plasticity that largely associated with decreased hypoxia tolerance. Conversely, adaptive plasticity that is congruent with increased hypoxia tolerance is often reinforced in the colonized tree sparrows. Genes displaying large levels of reinforcement or reversion plasticity (i.e. 200% of original level) show greater genetic divergence between ancestral and colonized populations. Overall, our work demonstrates that gene expression plasticity at the initial stage of high-elevation colonization can be reversed or reinforced through selection-driven adaptive modification.

High elevation imposes unrelenting and unavoidable hypoxia on species inhabiting these environments, providing an excellent natural setting for studying convergent or divergent evolution. By integrating measures of phenotypic variation, gene regulation, and functional performance, our study demonstrates that recent colonizers of high-elevation environments exhibit fundamentally different cardiovascular changes compared to long-term natives of these environments. Through the studying of heart morphological phenotypes, we showed that recent colonizers exhibit signs of cardiac hypertrophy, reflected by increased relative heart mass (heart mass/body mass) and cardiomyocyte size compared to their low-elevation relatives. In contrast, native species show no signs of cardiac hypertrophy and instead have 3-fold higher capillary densities than the colonizers, a change that likely enhances tissue oxygen diffusing capacity in the former. Using phylogenetic principal component analysis to quantify multivariate trait divergence, we show that native species are similar in cardiovascular phenotype and underlying gene expression, but differ appreciably from recent colonizers. We further demonstrate, using a functional assay, that differential expression of two genes (IRS2 and AKT1) in a conserved regulatory pathway mediates cardiomyocyte hypertrophy, which could explain the observed variation in cardiomyocyte size between native species and recent colonizers. This regulatory basis of variation in cardiac phenotype involves the differential expression of genes in a cardiomyocyte hypertrophy pathway that is conserved across birds, humans and other mammals. Collectively, our study highlights that evolutionary history is a critical determinant of cardiovascular variation in high-elevation environments.

The evolution of distinct lung architectures in birds (tubular air capillaries) and mammals (alveoli) represents a classic example of convergent evolution, yet their cellular differences remain poorly characterized. We present the comparative single-cell atlas of avian and mammalian lungs, revealing four key findings. First, we discover a persistent hybrid cell population (AT1/AT2) in neonatal and adult birds that disappears postnatally in mice, uncovering distinct strategies for lung maintenance. Second, cross-species comparisons highlight striking divergence in alveolar cell types, reflecting specialized adaptations to different respiratory demands. Third, avian lungs show unique molecular signatures in proliferation and saccular development pathways, potentially explaining their superior respiratory efficiency. Fourth, our viral receptor analysis uncovered differential ACE2 (SARS-CoV-2 receptor) expression but conserved EGFR (influenza A receptor), suggesting species-specific disease vulnerabilities. This work provides unprecedented insights into the evolutionary and developmental mechanisms shaping lung diversity in endotherms, with implications for respiratory biology, regenerative medicine, and zoonotic disease research.