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We describe a new species of Polynesian sandpiper from Henderson Island, Prosobonia sauli sp. nov., based on multiple Holocene fossil bones collected during the Sir Peter Scott Commemorative Expedition to the Pitcairn Islands (1991–92). Prosobonia sauli is the only species of Prosobonia to be described from bone accumulations and extends the record of known extinct Polynesian sandpipers to four. It is readily differentiated from the extant Tuamotu Sandpiper P. parvirostris in several features of the legs and bill, implying ecological adaptations to different environments. The geographically nearest Prosobonia populations to Henderson Island were found on Mangareva, where it is now extinct. A previous record of a species of Prosobonia from Tubuai, Austral Islands, is here shown to belong to the Sanderling Calidris alba. Our analyses of newly sequenced genetic data, which include the mitochondrial genomes of P. parvirostris and the extinct Tahiti Sandpiper P. leucoptera, confidently resolve the position of Prosobonia as sister-taxon to turnstones and calidrine sandpipers. We present a hypothesis for the timing of divergence between species of Prosobonia and other scolopacid lineages. Our results further provide a framework to interpret the evolution of sedentary lineages within the normally highly migratory Scolopacidae.

Summary: The evolution of the genera Bos and Bison, and the nature of gene flow between wild and domestic species, is poorly understood, with genomic data of wild species being limited. We generated two genomes from the likely extinct kouprey (Bos sauveli) and analyzed them alongside other Bos and Bison genomes. We found that B. sauveli possessed genomic signatures characteristic of an independent species closely related to Bos javanicus and Bos gaurus. We found evidence for extensive incomplete lineage sorting across the three species, consistent with a polytomic diversification of the major ancestry in the group, potentially followed by secondary gene flow. Finally, we detected significant gene flow from an unsampled Asian Bos-like source into East Asian zebu cattle, demonstrating both that the full genomic diversity and evolutionary history of the Bos complex has yet to be elucidated and that museum specimens and ancient DNA are valuable resources to do so.

Simple Summary It is of great interest to quantify adaptive evolution in human lineage by studying genes under positive selection, since these genes could reveal insights into our own adaptive evolutionary history compared to our closely related species and often these genes are functionally important. We used the great apes as the subjects to detect gene-level adaptive evolution signals in all the great ape lineages and investigated the evolutionary patterns and functional relevance of these adaptive evolution signals. Even the differences in population size among these closely related great apes have resulted in differences in their ability to remove deleterious alleles and to adapt to changing environments, we found that they experienced comparable numbers of positive selection. Notably, we identified several genes that offer insights into great ape and human evolution. For example, SOD1, a gene associated with aging in humans, experienced positive selection in the common ancestor of the great ape and this positive selection may contribute to the aging evolution in great apes. Overall, an updated list of positively selected genes reported by this study not only informs us of adaptive evolution during great ape evolution, but is also helpful to the further study of non-human primate models for disease and other fields. Abstract Alleles that cause advantageous phenotypes with positive selection contribute to adaptive evolution. Investigations of positive selection in protein-coding genes rely on the accuracy of orthology, models, the quality of assemblies, and alignment. Here, based on the latest genome assemblies and gene annotations, we present a comparative analysis on positive selection in four great ape species and identify 211 high-confidence positively selected genes (PSGs). Even the differences in population size among these closely related great apes have resulted in differences in their ability to remove deleterious alleles and to adapt to changing environments, we found that they experienced comparable numbers of positive selection. We also uncovered that more than half of multigene families exhibited signals of positive selection, suggesting that imbalanced positive selection resulted in the functional divergence of duplicates. Moreover, at the expression level, although positive selection led to a more non-uniform pattern across tissues, the correlation between positive selection and expression patterns is diverse. Overall, this updated list of PSGs is of great significance for the further study of the phenotypic evolution in great apes.

Emu and other ratites are more informative than any other birds in reconstructing the evolution of the ancestral avian or vertebrate karyotype because of their much slower rate of genome evolution. Here, we generated a new chromosome-level genome assembly of a female emu, and estimated the tempo of chromosome evolution across major avian phylogenetic branches, by comparing it to chromosome-level genome assemblies of 11 other bird and one turtle species. We found ratites exhibited the lowest numbers of intra- and inter-chromosomal changes among birds since their divergence with turtles. The small-sized and gene-rich emu microchromosomes have frequent inter-chromosomal contacts that are associated with housekeeping genes, which appears to be driven by clustering their centromeres in the nuclear interior, away from the macrochromosomes in the nuclear periphery. Unlike nonratite birds, only less than one-third of the emu W Chromosome regions have lost homologous recombination and diverged between the sexes. The emu W is demarcated into a highly heterochromatic region (WS0) and another recently evolved region (WS1) with only moderate sequence divergence with the Z Chromosome. WS1 has expanded its inactive chromatin compartment, increased chromatin contacts within the region, and decreased contacts with the nearby regions, possibly influenced by the spreading of heterochromatin from WS0. These patterns suggest that alteration of chromatin conformation comprises an important early step of sex chromosome evolution. Overall, our results provide novel insights into the evolution of avian genome structure and sex chromosomes in three-dimensional space.

Background Species domestication is generally characterized by the exploitation of high-impact mutations through processes that involve complex shifting demographics of domesticated species. These include not only inbreeding and artificial selection that may lead to the emergence of evolutionary bottlenecks, but also post-divergence gene flow and introgression. Although domestication potentially affects the occurrence of both desired and undesired mutations, the way wild relatives of domesticated species evolve and how expensive the genetic cost underlying domestication is remain poorly understood. Here, we investigated the demographic history and genetic load of chicken domestication. Results We analyzed a dataset comprising over 800 whole genomes from both indigenous chickens and wild jungle fowls. We show that despite having a higher genetic diversity than their wild counterparts (average π, 0.00326 vs. 0.00316), the red jungle fowls, the present-day domestic chickens experienced a dramatic population size decline during their early domestication. Our analyses suggest that the concomitant bottleneck induced 2.95% more deleterious mutations across chicken genomes compared with red jungle fowls, supporting the “cost of domestication” hypothesis. Particularly, we find that 62.4% of deleterious SNPs in domestic chickens are maintained in heterozygous states and masked as recessive alleles, challenging the power of modern breeding programs to effectively eliminate these genetic loads. Finally, we suggest that positive selection decreases the incidence but increases the frequency of deleterious SNPs in domestic chicken genomes. Conclusion This study reveals a new landscape of demographic history and genomic changes associated with chicken domestication and provides insight into the evolutionary genomic profiles of domesticated animals managed under modern human selection.

Background Ducks have a typical avian karyotype that consists of macro- and microchromosomes, but a pair of much less differentiated ZW sex chromosomes compared to chickens. To elucidate the evolution of chromosome architectures between ducks and chickens, and between birds and mammals, we produced a nearly complete chromosomal assembly of a female Pekin duck by combining long-read sequencing and multiplatform scaffolding techniques. Results A major improvement of genome assembly and annotation quality resulted from the successful resolution of lineage-specific propagated repeats that fragmented the previous Illumina-based assembly. We found that the duck topologically associated domains (TAD) are demarcated by putative binding sites of the insulator protein CTCF, housekeeping genes, or transitions of active/inactive chromatin compartments, indicating conserved mechanisms of spatial chromosome folding with mammals. There are extensive overlaps of TAD boundaries between duck and chicken, and also between the TAD boundaries and chromosome inversion breakpoints. This suggests strong natural selection pressure on maintaining regulatory domain integrity, or vulnerability of TAD boundaries to DNA double-strand breaks. The duck W chromosome retains 2.5-fold more genes relative to chicken. Similar to the independently evolved human Y chromosome, the duck W evolved massive dispersed palindromic structures, and a pattern of sequence divergence with the Z chromosome that reflects stepwise suppression of homologous recombination. Conclusions Our results provide novel insights into the conserved and convergently evolved chromosome features of birds and mammals, and also importantly add to the genomic resources for poultry studies.

Many paleognaths (ratites and tinamous) have a pair of homomorphic ZW sex chromosomes in contrast to the highly differentiated sex chromosomes of most other birds. To understand the evolutionary causes for the different tempos of sex chromosome evolution, we produced female genomes of 12 paleognathous species and reconstructed the phylogeny and the evolutionary history of paleognathous sex chromosomes. We uncovered that Palaeognathae sex chromosomes had undergone stepwise recombination suppression and formed a pattern of "evolutionary strata". Nine of the 15 studied species' sex chromosomes have maintained homologous recombination in their long pseudoautosomal regions extending more than half of the entire chromosome length. We found that in the older strata, the W chromosome suffered more serious functional gene loss. Their homologous Z-linked regions, compared with other genomic regions, have produced an excess of species-specific autosomal duplicated genes that evolved female-specific expression, in contrast to their broadly expressed progenitors. We speculate such "defeminization" of Z chromosome with underrepresentation of female-biased genes and slow divergence of sex chromosomes of paleognaths might be related to their distinctive mode of sexual selection targeting females rather than males, which evolved in their common ancestors.

Whole-genome sequencing projects are increasingly populating the tree of life and characterizing biodiversity1–4. Sparse taxon sampling has previously been proposed to confound phylogenetic inference5, and captures only a fraction of the genomic diversity. Here we report a substantial step towards the dense representation of avian phylogenetic and molecular diversity, by analysing 363 genomes from 92.4% of bird families—including 267 newly sequenced genomes produced for phase II of the Bird 10,000 Genomes (B10K) Project. We use this comparative genome dataset in combination with a pipeline that leverages a reference-free whole-genome alignment to identify orthologous regions in greater numbers than has previously been possible and to recognize genomic novelties in particular bird lineages. The densely sampled alignment provides a single-base-pair map of selection, has more than doubled the fraction of bases that are confidently predicted to be under conservation and reveals extensive patterns of weak selection in predominantly non-coding DNA. Our results demonstrate that increasing the diversity of genomes used in comparative studies can reveal more shared and lineage-specific variation, and improve the investigation of genomic characteristics. We anticipate that this genomic resource will offer new perspectives on evolutionary processes in cross-species comparative analyses and assist in efforts to conserve species., A dataset of the genomes of 363 species from the Bird 10,000 Genomes Project shows increased power to detect shared and lineage-specific variation, demonstrating the importance of phylogenetically diverse taxon sampling in whole-genome sequencing.

BackgroundDucks have a typical avian karyotype that consists of macro- and microchromosomes, but a pair of much less differentiated ZW sex chromosomes compared to chicken. To elucidate the evolution of chromosome architectures between duck and chicken, and between birds and mammals, we produced a nearly complete chromosomal assembly of a female Pekin duck by combining long-read sequencing and multiplatform scaffolding techniques.ResultsThe major improvement of genome assembly and annotation quality resulted from successful resolution of lineage-specific propagated repeats that fragmented the previous Illumina-based assembly. We found that the duck topologically associated domains (TAD) are demarcated by putative binding sites of the insulator protein CTCF, housekeeping genes, or transitions of active/inactive chromatin compartments, indicating the conserved mechanisms of spatial chromosome folding with mammals. There are extensive overlaps of TAD boundaries between duck and chicken, and also between the TAD boundaries and chromosome inversion breakpoints. This suggests strong natural selection on maintaining regulatory domain integrity, or vulnerability of TAD boundaries to DNA double-strand breaks. The duck W chromosome retains 2.5-fold more genes relative to chicken. Similar to the independently evolved human Y chromosome, the duck W evolved massive dispersed palindromic structures, and a pattern of sequence divergence with the Z chromosome that reflects stepwise suppression of homologous recombination.ConclusionsOur results provide novel insights into the conserved and convergently evolved chromosome features of birds and mammals, and also importantly add to the genomic resources for poultry studies.

New genome assemblies have been arriving at a rapidly increasing pace, thanks to decreases in sequencing costs and improvements in third-generation sequencing technologies1–3. For example, the number of vertebrate genome assemblies currently in the NCBI (National Center for Biotechnology Information) database4 increased by more than 50% to 1,485 assemblies in the year from July 2018 to July 2019. In addition to this influx of assemblies from different species, new human de novo assemblies5 are being produced, which enable the analysis of not only small polymorphisms, but also complex, large-scale structural differences between human individuals and haplotypes. This coming era and its unprecedented amount of data offer the opportunity to uncover many insights into genome evolution but also present challenges in how to adapt current analysis methods to meet the increased scale. Cactus6, a reference-free multiple genome alignment program, has been shown to be highly accurate, but the existing implementation scales poorly with increasing numbers of genomes, and struggles in regions of highly duplicated sequences. Here we describe progressive extensions to Cactus to create Progressive Cactus, which enables the reference-free alignment of tens to thousands of large vertebrate genomes while maintaining high alignment quality. We describe results from an alignment of more than 600 amniote genomes, which is to our knowledge the largest multiple vertebrate genome alignment created so far., The Progressive Cactus program can create reference-free alignments of hundreds of large vertebrate genomes efficiently, and is used for the alignment of more than 600 amniote genomes.

Despite the substantial role that chickens have played in human societies across the world, both the geographic and temporal origins of their domestication remain controversial. To address this issue, we analyzed 863 genomes from a worldwide sampling of chickens and representatives of all four species of wild jungle fowl and each of the five subspecies of red jungle fowl (RJF). Our study suggests that domestic chickens were initially derived from the RJF subspecies Gallus gallus spadiceus whose present-day distribution is predominantly in southwestern China, northern Thailand and Myanmar. Following their domestication, chickens were translocated across Southeast and South Asia where they interbred locally with both RJF subspecies and other jungle fowl species. In addition, our results show that the White Leghorn chicken breed possesses a mosaic of divergent ancestries inherited from other subspecies of RJF. Despite the strong episodic gene flow from geographically divergent lineages of jungle fowls, our analyses show that domestic chickens undergo genetic adaptations that underlie their unique behavioral, morphological and reproductive traits. Our study provides novel insights into the evolutionary history of domestic chickens and a valuable resource to facilitate ongoing genetic and functional investigations of the world’s most numerous domestic animal.

Strains of red fox (Vulpes vulpes) with markedly different behavioural phenotypes have been developed in the famous long-term selective breeding programme known as the Russian farm-fox experiment. Here we sequenced and assembled the red fox genome and re-sequenced a subset of foxes from the tame, aggressive and conventional farm-bred populations to identify genomic regions associated with the response to selection for behaviour. Analysis of the re-sequenced genomes identified 103 regions with either significantly decreased heterozygosity in one of the three populations or increased divergence between the populations. A strong positional candidate gene for tame behaviour was highlighted: SorCS1, which encodes the main trafficking protein for AMPA glutamate receptors and neurexins and suggests a role for synaptic plasticity in fox domestication. Other regions identified as likely to have been under selection in foxes include genes implicated in human neurological disorders, mouse behaviour and dog domestication. The fox represents a powerful model for the genetic analysis of affiliative and aggressive behaviours that can benefit genetic studies of behaviour in dogs and other mammals, including humans.

Sex chromosomes of mammals and most birds are heteromorphic, while those of many paleognaths (ratites and tinamous) are inexplicably homomorphic. To dissect the mechanisms underlying the different tempo of sex chromosome evolution, we produced high-quality genomes of 12 paleognathous species, and reconstructed their phylogeny based on alignments of the non-coding sequences extending to nearly 40% of the genome. Our phylogenomic tree grouped the South American rheas and tinamous together, and supported the independent evolution of gigantism and loss of flight among ratites. The small-bodied tinamous have much higher rates of genome-wide substitutions and transposon turnovers. Yet majorities of both have retained exceptionally long recombining regions occupying over half of the entire sex chromosome, with the rest sex-linked regions diverging from each other at a much lower rate relative to neognathous birds. Each species exhibits a punctuated sequence divergence pattern between sex chromosomes termed ‘evolutionary strata’, because of stepwise suppression of recombination. We concluded that all paleognaths share one evolutionary stratum with all other birds, and convergently formed between one to three strata after their rapid speciation. Contrary to the classic notion, we provided clear evidence that the youngest stratum of some tinamous formed without chromosomal inversion. Intriguingly, some of the encompassing W-linked genes have upregulated their expression levels in ovary, probably due to the female-specific selection. We proposed here that the unique male-only parental care system of paleognaths has reduced the intensity of sexual selection, and contributed to these species’ low rates of sex chromosome evolution. We also provided novel insights into the evolution of W-linked genes at their early stages.

Summary Human-induced environmental change and habitat fragmentation pose major threats to biodiversity and require active conservation efforts to mitigate their consequences. Genetic rescue through translocation and the introduction of variation into imperiled populations has been argued as a powerful means to preserve, or even increase, the genetic diversity and evolutionary potential of endangered species [1, 2, 3, 4]. However, factors such as outbreeding depression [5, 6] and a reduction in available genetic diversity render the success of such approaches uncertain. An improved evaluation of the consequence of genetic restoration requires knowledge of temporal changes to genetic diversity before and after the advent of management programs. To provide such information, a growing number of studies have included small numbers of genomic loci extracted from historic and even ancient specimens [7, 8]. We extend this approach to its natural conclusion, by characterizing the complete genomic sequences of modern and historic population samples of the crested ibis (Nipponia nippon), an endangered bird that is perhaps the most successful example of how conservation effort has brought a species back from the brink of extinction. Though its once tiny population has today recovered to >2,000 individuals [9], this process was accompanied by almost half of ancestral loss of genetic variation and high deleterious mutation load. We furthermore show how genetic drift coupled to inbreeding following the population bottleneck has largely purged the ancient polymorphisms from the current population. In conclusion, we demonstrate the unique promise of exploiting genomic information held within museum samples for conservation and ecological research., Highlights • Recent population decline of crested ibis in 10 kya was likely shaped by human activity • Modern group has lost almost half of genetic variations in pre-bottleneck ancestors • Modern group suffers from a high inbreeding coefficient and deleterious mutation load • Ancestral balancing selection is outweighed by genetic drift in the modern group, Feng et al. use whole-genome sequencing of contemporary and historic crested ibis, an iconic endangered bird species, to explore how their genetic diversity has changed through time. Their analyses reveal the roles of genetic drift and intensive inbreeding on the loss of genetic diversity in today’s population.

As the only endemic neotropical parrot to have recently lived in the northern hemisphere, the Carolina parakeet (Conuropsis carolinensis) was an iconic North American bird. The last surviving specimen died in the Cincinnati Zoo in 1918 [1]. The cause of its extinction remains contentious: besides excessive mortality associated to habitat destruction and active hunting, their survival could have been negatively affected by its range having become increasingly patchy [2] or by the exposure to poultry pathogens [3, 4]. In addition, the Carolina parakeet showed a predilection for cockleburs, an herbaceous plant that contains a powerful toxin, carboxyatractyloside, or CAT [5], which did not seem to affect them but made the birds notoriously toxic to most predators [3]. To explore the demographic history of this bird, we generated the complete genomic sequence of a preserved specimen held in a private collection in Espinelves (Girona, Spain), as well as of a close extant relative, Aratinga solstitialis. We identified two non-synonymous genetic changes in two highly conserved proteins known to interact with CAT that could underlie a specific dietary adaptation to this toxin. Our genomic analyses did not reveal evidence of a dramatic past demographic decline in the Carolina parakeet; also, its genome did not exhibit the long runs of homozygosity that are signals of recent inbreeding and are typically found in endangered species. As such, our results suggest its extinction was an abrupt process and thus likely solely attributable to human causes. Gelabert et al. report the whole genome of the extinct Carolina parakeet and provide evidence of its phylogeny, adaptation to a toxic cocklebur diet, and demographic history. The lack of signs of recent inbreeding typically found in endangered species suggests its abrupt extinction was human mediated., This work was supported by ERC Consolidator Grant 681396 “Extinction Genomics” to M.T.P.G. and M.S.-V., Obra Social ‘‘La Caixa’’ and Secretaria d’Universitats i Recerca ( GRC2017-SGR880 ) to T.M.-B. and C.L.-F., BFU2017-86471-P and PGC2018-101927-B-I00 from MINECO/FEDER, UE to T.M.-B, and PGC2018-095931-B-100 from MINECO/FEDER, UE to C.L.-F. T.M.-B. is also supported by a U01 MH106874 grant and Howard Hughes International Early Career and CERCA Programme (Generalitat de Catalunya). A.A. is partially supported by the Strategic Funding UID/Multi/04423/2019 through national funds provided by the Portuguese Foundation for Science and Technology (FCT) and the European Regional Development Fund —program PT2020 , by the European Structural and Investment Funds —Competitiveness and Internationalization Operational Program-COMPETE 2020, and by National Funds through the FCT under the project PTDC/CTA-AMB/31774/2017(POCI-01-0145-FEDER/031774/2017 ).

Songbirds have a species number close to that of mammals and are classic models for studying speciation and sexual selection. Sex chromosomes are hotspots of both processes, yet their evolutionary history in songbirds remains unclear. We characterized genomes of 11 songbird species, with 5 genomes of bird-of-paradise species. We conclude that songbird sex chromosomes have undergone four periods of recombination suppression before species radiation, producing a gradient of pairwise sequence divergence termed ‘evolutionary strata’. The latest stratum was probably due to a songbird-specific burst of retrotransposon CR1–E1 elements at its boundary, instead of the chromosome inversion generally assumed for suppressing sex-linked recombination. The formation of evolutionary strata has reshaped the genomic architecture of both sex chromosomes. We find stepwise variations of Z-linked inversions, repeat and guanine–cytosine (GC) contents, as well as W-linked gene loss rate associated with the age of strata. A few W-linked genes have been preserved for their essential functions, indicated by higher and broader expression of lizard orthologues compared with those of other sex-linked genes. We also find a different degree of accelerated evolution of Z-linked genes versus autosomal genes among species, potentially reflecting diversified intensity of sexual selection. Our results uncover the dynamic evolutionary history of songbird sex chromosomes and provide insights into the mechanisms of recombination suppression. Songbirds are a species-rich group known for their diversified sexual traits. Genomic analysis of 11 songbird species reveals evolutionary strata and shows their role in reshaping the genomic architecture of songbird sex chromosomes.

The genome of a red fox (Vulpes vulpes) was recently sequenced and assembled using next-generation sequencing (NGS). The assembly is of high quality, with 94X coverage and a scaffold N50 of 11.8 Mbp, but is split into 676,878 scaffolds, some of which are likely to contain assembly errors. Fragmentation and misassembly hinder accurate gene prediction and downstream analysis such as the identification of loci under selection. Therefore, assembly of the genome into chromosome-scale fragments was an important step towards developing this genomic model. Scaffolds from the assembly were aligned to the dog reference genome and compared to the alignment of an outgroup genome (cat) against the dog to identify syntenic sequences among species. The program Reference-Assisted Chromosome Assembly (RACA) then integrated the comparative alignment with the mapping of the raw sequencing reads generated during assembly against the fox scaffolds. The 128 sequence fragments RACA assembled were compared to the fox meiotic linkage map to guide the construction of 40 chromosomal fragments. This computational approach to assembly was facilitated by prior research in comparative mammalian genomics, and the continued improvement of the red fox genome can in turn offer insight into canid and carnivore chromosome evolution. This assembly is also necessary for advancing genetic research in foxes and other canids.

The development of efficient sequencing techniques has resulted in large numbers of genomes being available for evolutionary studies. However, only one genome is available for all amphibians, that of Xenopus tropicalis, which is distantly related from the majority of frogs. More than 96% of frogs belong to the Neobatrachia, and no genome exists for this group. This dearth of amphibian genomes greatly restricts genomic studies of amphibians and, more generally, our understanding of tetrapod genome evolution. To fill this gap, we provide the de novo genome of a Tibetan Plateau frog, Nanorana parkeri, and compare it to that of X. tropicalis and other vertebrates. This genome encodes more than 20,000 protein-coding genes, a number similar to that of Xenopus. Although the genome size of Nanorana is considerably larger than that of Xenopus (2.3 vs. 1.5 Gb), most of the difference is due to the respective number of transposable elements in the two genomes. The two frogs exhibit considerable conserved whole-genome synteny despite having diverged approximately 266 Ma, indicating a slow rate of DNA structural evolution in anurans. Multigenome synteny blocks further show that amphibians have fewer interchromosomal rearrangements than mammals but have a comparable rate of intrachromosomal rearrangements. Our analysis also identifies 11 Mb of anuran-specific highly conserved elements that will be useful for comparative genomic analyses of frogs. The Nanorana genome offers an improved understanding of evolution of tetrapod genomes and also provides a genomic reference for other evolutionary studies.