Genetic mechanism of adaptive evolution: the example of adaptation to high altitudes.

Since Darwin's time, elucidating the mechanism of adaptive evolution has been one of the most important scientific issues in evolutionary biology and ecology. Adaptive evolution usually means that species evolve special phenotypic traits to increase fitness under selective pressures. Phenotypic adaptation can be observed at different hierarchical levels of morphology, physiology, biochemistry, histology, and behavior. With the breakthroughs of molecular biology and next-generation sequencing technologies, mounting evidence has uncovered the genetic architecture driving adaptive complex phenotypes. Studying the molecular genetic mechanisms of evolutionary adaption will enable us to understand the forces shaping biodiversity and set up genotype-phenotype-environment interactions. Genetic bases of adaptive evolution have been explained by multiple hypotheses, including major-effect genes, supergenes, polygenicity, noncoding regions, repeated regions, and introgression. The strong selection pressure exerted by high-altitude extreme environments greatly promotes the occurrence of phenotypic and genetic adaptation in species. Studies on multi-omics data provide new insights into adaptive evolution. In this review, we systematically summarize the genetic mechanism of adaptive evolution, research progress in adaptation to high-altitude environmental conditions, and existing challenges and discuss the future perspectives, thereby providing guidance for researchers in this field.

Potential millennial-scale avian declines by humans in southern China.

Mounting observational records demonstrate human-caused faunal decline in recent decades, while accumulating archaeological evidence suggests an early biodiversity impact of human activities during the Holocene. A fundamental question arises concerning whether modern wildlife population declines began during early human disturbance. Here, we performed a population genomic analysis of six common forest birds in East Asia to address this question. For five of them, demographic history inference based on 25-33 genomes of each species revealed dramatic population declines by 4- to 48-fold over millennia (e.g. 2000-5000 thousand years ago). Nevertheless, summary statistics detected nonsignificant correlations between these population size trajectories and Holocene temperature variations, and ecological niche models explicitly predicted extensive range persistence during the Holocene, implying limited demographic consequence of Holocene climate change. Further analyses suggest high negative correlations between the reconstructed population declines and human disturbance intensities and indicate a potential driver of human activities. These findings provide a deep-time and large-scale insight into the recently recognized avifaunal decline and support an early origin hypothesis of human effects on biodiversity. Overall, our study sheds light on the current biodiversity crisis in the context of long-term human-environment interactions and offers a multi-evidential framework for quantitatively assessing the ecological consequences of human disturbance.

The De Novo Genome Sequencing of Silver Pheasant (Lophura nycthemera).

Silver pheasant (Lophura nycthemera) belongs to Phasianidae, Galliformes, which exhibits high subspecific differentiation. In this study, we assembled a novel genome based on 98.42 Gb of Illumina sequencing data and 30.20 Gb of PacBio sequencing data. The size of the final assembled genome was 1.01 Gb, with a contig N50 of 6.96 Mb. Illumina paired-end reads (94.96%) were remapped to the contigs. The assemble genome shows high completeness, with a complete BUSCO score of 92.35% using the avian data set. A total of 16,747 genes were predicted from the generated assembly, and 16,486 (98.44%) of the genes were annotated. The average length of genes, exons, and introns were 19,827.53, 233.69, and 1841.19 bp, respectively. Noncoding RNAs included 208 miRNAs, 40 rRNAs, and 264 tRNAs, and a total of 189 pseudogenes were identified; 116.31 Mb (11.47%) of the genome consisted of repeat sequences, with the greatest proportion of LINEs. This assembled genome provides a valuable reference genome for further studies on the evolutionary history and conversion genetics of L. nycthemera and the phylogenomics of the Galliformes lineage.

Population genomic, climatic and anthropogenic evidence suggest the role of human forces in endangerment of green peafowl (Pavo muticus).

Both anthropogenic impacts and historical climate change could contribute to population decline and species extinction, but their relative importance is still unclear. Emerging approaches based on genomic, climatic and anthropogenic data provide a promising analytical framework to address this question. This study applied such an integrative approach to examine potential drivers for the endangerment of the green peafowl (Pavo muticus). Several demographic reconstructions based on population genomes congruently retrieved a drastic population declination since the mid-Holocene. Furthermore, a comparison between historical and modern genomes suggested genetic diversity decrease during the last 50 years. However, climate-based ecological niche models predicted stationary general range during these periods and imply the little impact of climate change. Further analyses suggested that human disturbance intensities were negatively correlated with the green peafowl's effective population sizes and significantly associated with its survival status (extirpation or persistence). Archaeological and historical records corroborate the critical role of humans, leaving the footprint of low genomic diversity and high inbreeding in the survival populations. This study sheds light on the potential deep-time effects of human disturbance on species endangerment and offers a multi-evidential approach in examining underlying forces for population declines.

The niches of nuthatches affect their lineage evolution differently across latitude.

Ecological niche evolution can promote or hinder the differentiation of taxa and determine their distribution. Niche-mediated evolution may differ among climatic regimes, and thus, species that occur across a wide latitudinal range offer a chance to test these heterogeneous evolutionary processes. In this study, we examine (a) how many lineages have evolved across the continent-wide range of the Eurasian nuthatch (Sitta europaea), (b) whether the lineages' niches are significantly divergent or conserved and (c) how their niche evolution explains their geographic distribution. Phylogenetic reconstruction and ecological niche models (ENMs) showed that the Eurasian nuthatch contained six parapatric lineages that diverged within 2 Myr and did not share identical climatic niches. However, the niche discrepancy between these distinct lineages was relatively conserved compared with the environmental differences between their ranges and thus was unlikely to drive lineage divergence. The ENMs of southern lineages tended to cross-predict with their neighbouring lineages whereas those of northern lineages generally matched with their abutting ranges. The coalescence-based analyses revealed more stable populations for the southern lineages than the northern ones during the last glaciation cycle. In contrast to the overlapping ENMs, the smaller parapatric distribution suggests that the southern lineages might have experienced competitive exclusion to prevent them from becoming sympatric. On the other hand, the northern lineages have expanded their ranges and their current abutting distribution might have resulted from lineages adapting to different climatic conditions in allopatry. This study suggests that niche evolution may affect lineage distribution in different ways across latitude.

Ice age unfrozen: severe effect of the last interglacial, not glacial, climate change on East Asian avifauna.

BACKGROUND: The glacial-interglacial cycles in the Pleistocene caused repeated range expansion and contraction of species in several regions in the world. However, it remains uncertain whether such climate oscillations had similar impact on East Asian biota, despite its widely recognized importance in global biodiversity. Here we use both molecular and ecological niche profiles on 11 East Asian avian species with various elevational ranges to reveal their response to the late Pleistocene climate changes. RESULTS: The ecological niche models (ENM) consistently showed that these avian species might substantially contract their ranges to the south during the Last Interglacial period (LIG) and expanded their northern range margins through the Last Glacial Maximum (LGM), leading to the LGM ranges observed for all 11 species. Consistently, coalescent simulations based on 25-30 nuclear genes retrieved signatures of significant population growth through the last glacial period across all species studied. Climate statistics suggested that high climatic variability during the LIG and a relatively mild climate at the LGM potentially explained the historical population dynamics of these birds. CONCLUSIONS: This is the first study based on multiple species and both lines of ecological niche profiles and genetic data to characterize the unique response of East Asian biota to late Pleistocene climate. The present study highlights regional differences in the evolutionary consequence of climate change during the last glacial cycle and implies that global warming might pose a great risk to species in this region given potentially higher climatic variation in the future analogous to that during the LIG.

Data on taxonomic status and phylogenetic relationship of tits.

The data in this paper are related to the research article entitled "Taxonomic status and phylogenetic relationship of tits based on mitogenomes and nuclear segments" (X.J. Li et al., 2016) [1]. The mitochondrial genomes and nuclear segments of tits were sequenced to analyze mitochondrial characteristics and phylogeny. In the data, the analyzed results are presented. The data holds the resulting files of mitochondrial characteristics, heterogeneity, best schemes, and trees.

Flying high: limits to flight performance by sparrows on the Qinghai-Tibet Plateau.

Limits to flight performance at high altitude potentially reflect variable constraints deriving from the simultaneous challenges of hypobaric, hypodense and cold air. Differences in flight-related morphology and maximum lifting capacity have been well characterized for different hummingbird species across elevational gradients, but relevant within-species variation has not yet been identified in any bird species. Here we evaluate load-lifting capacity for Eurasian tree sparrow (Passer montanus) populations at three different elevations in China, and correlate maximum lifted loads with relevant anatomical features including wing shape, wing size, and heart and lung masses. Sparrows were heavier and possessed more rounded and longer wings at higher elevations; relative heart and lung masses were also greater with altitude, although relative flight muscle mass remained constant. By contrast, maximum lifting capacity relative to body weight declined over the same elevational range, while the effective wing loading in flight (i.e. the ratio of body weight and maximum lifted weight to total wing area) remained constant, suggesting aerodynamic constraints on performance in parallel with enhanced heart and lung masses to offset hypoxic challenge. Mechanical limits to take-off performance may thus be exacerbated at higher elevations, which may in turn result in behavioral differences in escape responses among populations.

Climate niche differentiation between two passerines despite ongoing gene flow.

Niche evolution underpins the generation and maintenance of biological diversity, but niche conservatism, in which niches remain little changed over time in closely related taxa, and the role of ecology in niche evolution are continually debated. To test whether climate niches are conserved in two closely related passerines in East Asia - the vinous-throated (Paradoxornis webbianus) and ashy-throated (P. alphonsianus) parrotbills - we established their potential allopatric and sympatric regions using ecological niche models and compared differences in their climate niches using niche overlap indices in background tests and multivariate statistical analyses. We also used polymorphism data on 44 nuclear genes to infer their divergence demography. We found that these two parrotbills occupy different climate niches, in both their allopatric and potential sympatric regions. Because the potential sympatric region is the area predicted to be suitable for both parrotbills based on the ecological niche models, it can serve as a natural common garden. Therefore, their observed niche differences in this potential sympatry were not simply rendered by phenotypic plasticity and probably had a genetic basis. Our genetic analyses revealed that the two parrotbills are not evolutionarily independent for the most recent part of their divergence history. The two parrotbills diverged c. 856,000 years ago and have had substantial gene flow since a presumed secondary contact c. 290,000 years ago. This study provides an empirical case demonstrating that climate niches may not be homogenized in nascent species in spite of substantial, ongoing gene flow, which in turn suggests a role for ecology in promoting and maintaining diversification among incipient species.

Testing hypotheses of mitochondrial gene-tree paraphyly: unravelling mitochondrial capture of the Streak-breasted Scimitar Babbler (Pomatorhinus ruficollis) by the Taiwan Scimitar Babbler (Pomatorhinus musicus).

Species-level paraphyly inferred from mitochondrial gene trees is a prevalent phenomenon in taxonomy and systematics, but there are several potential causes that are not easily explained by currently used methods. This study aimed to test the underlying causes behind the observed paraphyly of Streak-breasted Scimitar Babbler (Pomatorhinus ruficollis) via statistical analyses of four mitochondrial (mtDNA) and nine nuclear (nuDNA) genes. Mitochondrial gene trees show paraphyly of P. ruficollis with respect to the Taiwan Scimitar Babbler (Pomatorhinus musicus), but nuclear genealogies support a sister-group relationship. Predictive coalescent simulations imply several hypothetical explanations, the most likely being mitochondrial capture of P. ruficollis by P. musicus for the observed cyto-nuclear incongruence. Further approximate Bayesian computation suggests a unidirectional introgression model with substantial level of gene flow from P. ruficollis to P. musicus during their initial divergence during the Late Pleistocene. This specific observation frames several potential causes for incongruent outcomes of mitochondrial and nuclear introgression in general, and on the whole, our results underscore the strength of multiple independent loci for species delimitation and importance of testing hypotheses that explain disparate causes of mitochondrial gene-tree paraphyly.

Sequencing and phylogenetic analysis of the Pyrgilauda ruficollis (Aves, Passeridae) complete mitochondrial genome.

In this study, both long PCR and conserved primers walking sequencing methods were used to determine the complete sequence of the of Pyrgilauda ruficollis mitochondrial genome (KC836121). The results showed that the complete mitochondrial genome of P. ruficollis is 1 6909 bp in length with 55.0% A+T content, harboring the typical 37 genes. The mitogenome had the same gene order with that of Podoces hendersoni. All protein coding genes started with ATG codon, except ND3 with GTG. For the stop codon usage, most genes terminate with codons TAA or TAG, but ND5 terminated with AGA, while ND1 and COI genes with AGG, and both the genes COⅢ and ND4 have an incomplete termination codon (T). The secondary structures of 22 tRNA genes were also predicted, showing that all tRNAs can form typical clover-leaf secondary structures, except for the tRNA(Ser) (AGN) which loses the DHU arm, while tRNA(Phe) harbor an extra nucleotide inserted in the TψC arm. The predicted secondary structures of 12S rRNA and 16S rRNA exhibit 47 helices in 4 domains and 60 helices in 6 domains respectively. The control region of P. ruficollis with the length of 1 305 bp was located between tRNA(Glu) and tRNA(Phe), and typical domains of which could be found as other bird groups. Using the data from 13 mitochondrial protein-coding genes, results of a final phylogenetic analysis strongly supports the traditional view that P. ruficollis is closely related with Passeridae and Fringillidae.

Molecular systematics and plumage coloration evolution of an enigmatic babbler (Pomatorhinus ruficollis) in East Asia.

The streak-breasted scimitar babbler, Pomatorhinus ruficollis, is a polytypic and taxonomically enigmatic babbler common in southern, eastern, and southeastern Asia. To infer the phylogeny of the P. ruficollis, we examined the sequences of two complete mitochondrial genes (2184 bp in total) from fourteen of the fifteen known subspecies, and an additional five nuclear genes (2657 bp in total) from ten subspecies. The mitochondrial phylogeny indicates four major clades with large geographical identity in P. ruficollis and paraphyly of the P. ruficollis species complex, with the inclusion of the olivaceus group of congeneric P. schisticeps. Together with their interbreeding in northern Indochina, we propose to lump this group into P. ruficollis. Analysis of both multilocus networks and species-tree inference recovered poor phylogenetic structure among mainland/ Hainan subspecies and exclusive groupings of the Taiwanese subspecies, consistent with the recent taxonomic revision of its species status. Our analyses also suggest strong incongruence between the morphological-based classification and molecular systematics, implying the strength of multilocus data for taxonomy.

Inferring the geographic mode of speciation by contrasting autosomal and sex-linked genetic diversity.

When geographic isolation drives speciation, concurrent termination of gene flow among genomic regions will occur immediately after the formation of the barrier between diverging populations. Alternatively, if speciation is driven by ecologically divergent selection, gene flow of selectively neutral genomic regions may go on between diverging populations until the completion of reproductive isolation. It may also lead to an unsynchronized termination of gene flow between genomic regions with different roles in the speciation process. Here, we developed a novel Approximate Bayesian Computation pipeline to infer the geographic mode of speciation by testing for a lack of postdivergence gene flow and a concurrent termination of gene flow in autosomal and sex-linked markers jointly. We applied this approach to infer the geographic mode of speciation for two allopatric highland rosefinches, the vinaceous rosefinch Carpodacus vinaceus and the Taiwan rosefinch C. formosanus from DNA polymorphisms of both autosomal and Z-linked loci. Our results suggest that the two rosefinch species diverged allopatrically approximately 0.5 Ma. Our approach allowed us further to infer that female effective population sizes are about five times larger than those of males, an estimate potentially useful when comparing the intensity of sexual selection across species.

[Sequencing and analysis of the complete mitochondrial genome of Remiz consobrinus].

The complete mitochondrial genome sequence of Remiz consobrinus was determined using long PCR and conserved primers walking approaches. Based on the results of assembling and annotation, the structure, sequence composition and codon usage of the genome protein-coding genes were analyzed, and the prediction of the secondary structure of 22 tRNA and 2 rRNA, the control region structure, and the phylogeny were also conducted, which provided new information for phylogenetic studies of passerine birds. The entire mitochondrial genome of Remiz consobrinus was 16 737 bp in length, the accession number was KC463856 and the content of A, T, C, and G were 27.8%, 21.5%, 35.4%, and 15.3%, respectively. The genome harbored the same gene order with that of other birds, and contained 13 protein coding genes (PCGs), 22 tRNA, 2 rRNA, and a non-coding control region. There were 77 bp intergenic intervals between 18 pair genes and 30 bp overlaps between 7 pair genes. Except for ND3 gene, which used ATT as the initiation codon, all other PCGs started with the typical ATG codon. Except for COIII and ND4, which used incomplete termination codon T, the other 11 PCGs used standard TAA, TAG, AGA or AGG as termination codons. The tRNAs all formed typical cloverleaf secondary structure, except for tRNASer-AGN, which lost the DHU arm in its structure. A total of 27 base mismatches appeared, with 19 common G-U mismatches. The predicted secondary structure of SrRNA and LrRNA contained 3 domains with 47 helices and 6 domains with 60 helices, respectively. Besides F-box, D-box, C-box, and B-box, Bird similarity-box and CSB1-box were also found in the control region of Remiz consobrinus, as found in other bird species. Our results suggest Remizidae as a separate family. The monophyly of Sylviidae and Remizidae was supported.

[Preliminary discussion on the phylogenetic and taxonomic relationship of Pomatorhinus ruficollis].

The phylogenetic relationships among subspecies of Pomatorhinus ruficollis are not clear. In this paper we sequenced two mitochondrial genes (Cyt b and ND2, in total 2 184 bp) and examined twenty individuals representing ten of the eleven subspecies of P. ruficollis in China. Molecular phylogenetic trees were reconstructed using maximum parsimony, maximum likelihood and Bayesian inference methods, with P. ruficollis and P. schisticeps as in-groups, P. montanus, P. ochraceiceps, P. ferruginosus and Xiphirhynchus superciliaris as out-groups. Results indicated that P. ruficollis was paraphyletic, in which P. schisticeps was embedded, and was divided into three phylogeographic groups: southwestern China group, southeastern China group and central China group. Our results also suggested discordances between phylogenetic relationships and morphological characteristics, and clarified some intraspecific taxonomic debates.

[Sequencing and analysis of the complete mitochondrial genome of Podoces hendersoni (Ave, Corvidae)].

The complete mitochondrial genome of a China endemic bird, Podoces hendersoni, was sequenced using La-PCR and conserved primer walking approaches. The mtDNA seqnence is 16 867 bp in length and deposited in GenBank with accession number GU592504. The mitochondrial genomic organization of P. hendersoni is the same with that in chicken, which contains 13 protein coding genes (PCGs), 22 tRNA, 2 rRNA, and a control region. Except for COI gene, which uses GTG as the initiation codon, all other 12 PCGs of the P. hendersoni mtDNA start with the typical ATG codon. Codons TAA, AGG, and AGA were used in 11 PCGs as usual termination codons; however, the COIII and ND4 had incomplete termination codon T. The secondary structures of 20 tRNAs formed typical cloverleaf, except for tRNASer (AGY) that had an absence of the DHU arm and tRNALeu (CUN) in which anticodon-loop consisted of 9 bases, rather than the standard 7 bases. The secondary structures of rRNA were predicted. There are 4 domains, 43 helices structures in 12S rRNA, and 6 domains, 55 helices structures in 16S rRNA. Besides, F-box, D-box, C-box, B-box, Bird similarity-box and CSB1-box, which were found in the control region of other birds, also existed in the P. hendersoni.

[Sequencing and analysis of the complete mitochondrial genome of Pseudopodoces humilis (Aves, Paridae)].

The complete sequence of Pseudopodoces humilis mitochondrial genome was determined by using long PCR and conserved primers walking approaches. The results showed that the entire mitochondrial genome of Pseudopodoces humilis was 16 809 bp in length with 52.9% A+T content, and the 37 genes had the same gene order with that of Gallus gallus. All protein coding genes of the Pseudopodoces humilis mitochondrial genome started with ATG codon, except for COI with GTG. For terminate codon usage, most of genes terminate with codons TAA or TAG, ND1 and ND5 were AGA, COII was AGG, and the COIII and ND4 genes had an incomplete termination codon (T). The secondary structures of 22 tRNA were predicted, all tRNA can form typical secondary structure, except tRNASer ( AGN ) with an absence of DHU arm, and tRNAPhe with an extra nucleotide inserted in the TpsiC arm. The predicted secondary structures of 12S rRNA and 16S rRNA exhibit 47 helics in 3 structural domains and 60 helics in 6 domains, respectively. The control region of Pseudopodoces humilis located between tRNAGlu and tRNAPhe with 1 240 bp in length, and has structure domains found in that of the other birds.

Use of parsimony analysis to identify areas of endemism of chinese birds: implications for conservation and biogeography.

Parsimony analysis of endemicity (PAE) was used to identify areas of endemism (AOEs) for Chinese birds at the subregional level. Four AOEs were identified based on a distribution database of 105 endemic species and using 18 avifaunal subregions as the operating geographical units (OGUs). The four AOEs are the Qinghai-Zangnan Subregion, the Southwest Mountainous Subregion, the Hainan Subregion and the Taiwan Subregion. Cladistic analysis of subregions generally supports the division of China's avifauna into Palaearctic and Oriental realms. Two PAE area trees were produced from two different distribution datasets (year 1976 and 2007). The 1976 topology has four distinct subregional branches; however, the 2007 topology has three distinct branches. Moreover, three Palaearctic subregions in the 1976 tree clustered together with the Oriental subregions in the 2007 tree. Such topological differences may reflect changes in the distribution of bird species through circa three decades.

Phylogeography of ground tit (Pseudopodoces humilis) based on mtDNA: evidence of past fragmentation on the Tibetan Plateau.

Pseudopodoces humilis, a long misclassified terrestrial tit, is the only species of parid whose distribution is limited to treeless terrain and endemic to the Tibetan Plateau. We revealed the phylogeographic structure of the species by using mitochondrial control region, as well as comparing morphological characters. The distinct geographic distributions of two major clades suggest spatial and temporal separations that coincide with important climatic and paleogeographic changes following the uplift of the Tibetan Plateau. Population expansion was inferred for the population at the platform of the Plateau 0.17 million years before present (Ma B.P.), and restricted gene flow with isolation by distance was detected within this region, congruent with expansion occurring after the extensive glacial period. A significant decrease in body size with decreasing altitude was found, possibly indicating selection for larger-sized birds at higher altitude.