Genomic Consequences of and Demographic Response to Pervasive Hybridization Over Time in Climate-Sensitive Pikas.

Rare and geographically restricted species may be vulnerable to genetic effects from inbreeding depression in small populations or from genetic swamping through hybridization with common species, but a third possibility is that selective gene flow can restore fitness (genetic rescue). Climate-sensitive pikas (Ochotona spp.) of the Qinghai-Tibetan Plateau (QHTP) and its vicinity have been reduced to residual populations through the movement of climatic zones during the Pleistocene and recent anthropogenic disturbance, whereas the plateau pika (O. curzoniae) remains common. Population-level whole-genome sequencing (n = 142) of six closely related species in the subgenus Ochotona revealed several phases of ancient introgression, lineage replacement, and bidirectional introgression. The strength of gene flow was the greatest from the dominant O. curzoniae to ecologically distinct species in areas peripheral to the QHTP. Genetic analyses were consistent with environmental reconstructions of past population movements. Recurrent periods of introgression throughout the Pleistocene revealed an increase in genetic variation at first but subsequent loss of genetic variation in later phases. Enhanced dispersion of introgressed genomic regions apparently contributed to demographic recovery in three peripheral species that underwent range shifts following climate oscillations on the QHTP, although it failed to drive recovery of northeastern O. dauurica and geographically isolated O. sikimaria. Our findings highlight differences in timescale and environmental background to determine the consequence of hybridization and the unique role of the QHTP in conserving key evolutionary processes of sky island species.

Phylogenetic conflict between species tree and maternally inherited gene trees in a clade of Emberiza buntings (Aves: Emberizidae).

Different genomic regions may reflect conflicting phylogenetic topologies primarily due to incomplete lineage sorting and/or gene flow. Genomic data are necessary to reconstruct the true species tree and explore potential causes of phylogenetic conflict. Here, we investigate the phylogenetic relationships of four Emberiza species (Aves: Emberizidae) and discuss the potential causes of the observed mitochondrial non-monophyly of Emberiza godlewskii (Godlewski's bunting) using phylogenomic analyses based on whole genome resequencing data from 41 birds. Analyses based on both the whole mitochondrial genome and ~39 kilobases from the non-recombining W chromosome reveal sister relationships between each the northern and southern populations of E. godlewskii with E. cioides and E. cia, respectively. In contrast, the monophyly of E. godlewskii is reflected by the phylogenetic signal of autosomal and Z chromosomal sequence data as well as demographic inference analyses, which - in combination - support the following tree topology: (((E. godlewskii, E. cia), E. cioides), E. jankowskii). Using D-statistics, we detected multiple gene flow events among different lineages, indicating pervasive introgressive hybridization within this clade. Introgression from an unsampled lineage that is sister to E. cioides or introgression from an unsampled mitochondrial + W chromosomal lineage of E. cioides into northern E. godlewskii may explain the phylogenetic conflict between the species tree estimated from genome-wide data versus mtDNA/W tree topologies. These results underscore the importance of using genomic data for phylogenetic reconstruction and species delimitation.

The evolution of ancestral and species-specific adaptations in snowfinches at the Qinghai-Tibet Plateau.

Species in a shared environment tend to evolve similar adaptations under the influence of their phylogenetic context. Using snowfinches, a monophyletic group of passerine birds (Passeridae), we study the relative roles of ancestral and species-specific adaptations to an extreme high-elevation environment, the Qinghai-Tibet Plateau. Our ancestral trait reconstruction shows that the ancestral snowfinch occupied high elevations and had a larger body mass than most nonsnowfinches in Passeridae. Subsequently, this phenotypic adaptation diversified in the descendant species. By comparing high-quality genomes from representatives of the three phylogenetic lineages, we find that about 95% of genes under positive selection in the descendant species are different from those in the ancestor. Consistently, the biological functions enriched for these species differ from those of their ancestor to various degrees (semantic similarity values ranging from 0.27 to 0.5), suggesting that the three descendant species have evolved divergently from the initial adaptation in their common ancestor. Using a functional assay to a highly selective gene, DTL, we demonstrate that the nonsynonymous substitutions in the ancestor and descendant species have improved the repair capacity of ultraviolet-induced DNA damage. The repair kinetics of the DTL gene shows a twofold to fourfold variation across the ancestor and the descendants. Collectively, this study reveals an exceptional case of adaptive evolution to high-elevation environments, an evolutionary process with an initial adaptation in the common ancestor followed by adaptive diversification of the descendant species.

Genomic and phenotypic changes associated with alterations of migratory behaviour in a songbird.

The seasonal migration of birds is a fascinating natural wonder. Avian migratory behaviour changes are common and are probably a polygenic process as avian migration is governed by multiple correlated components with a variable genetic basis. However, the genetic and phenotypic changes involving migration changes are poorly studied. Using one annotated near-chromosomal level de novo genome assembly, 50 resequenced genomes, hundreds of morphometric data and species distribution information, we investigated population structure and genomic and phenotypic differences associated with differences in migratory behaviour in a songbird species, Yellow-throated Bunting Emberiza elegans (Aves: Emberizidae). Population genomic analyses reveal extensive gene flow between the southern resident and the northern migratory populations of this species. The hand-wing index is significantly lower in the resident populations than in the migratory populations, indicating reduced flight efficiency of the resident populations. Here, we discuss the possibility that nonmigratory populations may have originated from migratory populations though migration loss. We further infer that the alterations of genes related to energy metabolism, nervous system and circadian rhythm may have played major roles in regulating migration change. Our study sheds light on phenotypic and polygenic changes involving migration change.

Most Genomic Loci Misrepresent the Phylogeny of an Avian Radiation Because of Ancient Gene Flow.

Phylogenetic trees based on genome-wide sequence data may not always represent the true evolutionary history for a variety of reasons. One process that can lead to incorrect reconstruction of species phylogenies is gene flow, especially if interspecific gene flow has affected large parts of the genome. We investigated phylogenetic relationships within a clade comprising eight species of passerine birds (Phylloscopidae, Phylloscopus, leaf warblers) using one de novo genome assembly and 78 resequenced genomes. On the basis of hypothesis-exclusion trials based on D-statistics, phylogenetic network analysis, and demographic inference analysis, we identified ancient gene flow affecting large parts of the genome between one species and the ancestral lineage of a sister species pair. This ancient gene flow consistently caused erroneous reconstruction of the phylogeny when using large amounts of genome-wide sequence data. In contrast, the true relationships were captured when smaller parts of the genome were analyzed, showing that the "winner-takes-all democratic majority tree" is not necessarily the true species tree. Under this condition, smaller amounts of data may sometimes avoid the effects of gene flow due to stochastic sampling, as hidden reticulation histories are more likely to emerge from the use of larger data sets, especially whole-genome data sets. In addition, we also found that genomic regions affected by ancient gene flow generally exhibited higher genomic differentiation but a lower recombination rate and nucleotide diversity. Our study highlights the importance of considering reticulation in phylogenetic reconstructions in the genomic era.[Bifurcation; introgression; recombination; reticulation; Phylloscopus.].

Genomic signatures of rapid adaptive divergence in a tropical montane species.

Mountain regions contain extraordinary biodiversity. The environmental heterogeneity and glacial cycles often accelerate speciation and adaptation of montane species, but how these processes influence the genomic differentiation of these species is largely unknown. Using a novel chromosome-level genome and population genomic comparisons, we study allopatric divergence and selection in an iconic bird living in a tropical mountain region in New Guinea, Archbold's bowerbird (Amblyornis papuensis). Our results show that the two populations inhabiting the eastern and western Central Range became isolated ca 11 800 years ago, probably because the suitable habitats for this cold-tolerating bird decreased when the climate got warmer. Our genomic scans detect that genes in highly divergent genomic regions are over-represented in developmental processes, which is probably associated with the observed differences in body size between the populations. Overall, our results suggest that environmental differences between the eastern and western Central Range probably drive adaptive divergence between them.

Gene expression plasticity followed by genetic change during colonization in a high-elevation environment.

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.

Rapid phenotypic evolution with shallow genomic differentiation during early stages of high elevation adaptation in Eurasian Tree Sparrows.

Known as the 'third polar region', the Qinghai-Tibet Plateau represents one of the harshest highland environments in the world and yet a number of organisms thrive there. Previous studies of birds, animals and humans have focused on well-differentiated populations in later stages of phenotypic divergence. The adaptive processes during the initial phase of highland adaptation remain poorly understood. We studied a human commensal, the Eurasian Tree Sparrow, which has followed human agriculture to the Qinghai-Tibet Plateau. Despite strong phenotypic differentiation at multiple levels, in particular in muscle-related phenotypes, highland and lowland populations show shallow genomic divergence and the colonization event occurred within the past few thousand years. In a one-month acclimation experiment investigating phenotypic plasticity, we exposed adult lowland tree sparrows to a hypoxic environment and did not observe muscle changes. Through population genetic analyses, we identified a signature of polygenic adaptation, whereby shifts in allele frequencies are spread across multiple loci, many of which are associated with muscle-related processes. Our results reveal a case of positive selection in which polygenic adaptation appears to drive rapid phenotypic evolution, shedding light on early stages of adaptive evolution to a novel environment.

Complete mitochondrial genome of Grey-headed Lapwing Vanellus cinereus (Ciconiiformes: Charadriidae).

The Grey-headed Lapwing (Vanellus cinereus) is a Vanellus bird belonging to the group Ciconiiformes, which breeds in northeast China and Japan. In this study, we sequenced its complete mitochondrial genome by PCR-based method. The mitochondrial DNA is packaged in a compact 17,135 based pair (bp) circular molecule with A + T content of 55.14%. It contains 37 typical mitochondrial genes, including 13 protein-coding genes, 2 rRNAs and 22 tRNAs and a non-coding control region (D-loop). All protein-coding genes are initiated by ATG codon, except for the COI gene and ND5 gene starting with GTG codon, and ND3 uses ATC codon. TAA is the most frequent stop codon. All tRNAs possess the classic cloverleaf secondary structure except for tRNA(Ser(AGY)) and tRNA(Leu(CUN)), which lack the ''DHU'' stem. The D-loop is a 1563 bp long A + T-rich region, which is located between tRNA(Glu) and tRNA(Phe).