Publications

2022
Opazo JC, Hoffman FG, Zavala K, Edwards SV. Evolution of the DAN gene family in vertebrates. Developmental Biology. 2022;482 :34-43. Publisher's VersionAbstract
The DAN gene family (DAN, Differential screening-selected gene Aberrant in Neuroblastoma) is a group of genes that is expressed during development and plays fundamental roles in limb bud formation and digitation, kidney formation and morphogenesis and left-right axis specification. During adulthood the expression of these genes are associated with diseases, including cancer. Although most of the attention to this group of genes has been dedicated to understanding its role in physiology and development, its evolutionary history remains poorly understood. Thus, the goal of this study is to investigate the evolutionary history of the DAN gene family in vertebrates, with the objective of complementing the already abundant physiological information with an evolutionary context. Our results recovered the monophyly of all DAN gene family members and divide them into five main groups. In addition to the well-known DAN genes, our phylogenetic results revealed the presence of two new DAN gene lineages; one is only retained in cephalochordates, whereas the other one (GREM3) was only identified in cartilaginous fish, holostean fish, and coelacanth. According to the phyletic distribution of the genes, the ancestor of gnathostomes possessed a repertoire of eight DAN genes, and during the radiation of the group GREM1, GREM2, SOST, SOSTDC1, and NBL1 were retained in all major groups, whereas, GREM3, CER1, and DAND5 were differentially lost.
Yung Wa Sin S, Cloutier A, Nevitt G, Edwards SV. Olfactory receptor subgenome and expression in a highly olfactory procellariiform seabird. Genetics. 2022;220 (2) :iyab210. Publisher's VersionAbstract

Procellariiform seabirds rely on their sense of smell for foraging and homing. Both genomes and transcriptomes yield important clues about how olfactory receptor (OR) subgenomes are shaped by natural and sexual selection, yet no transcriptomes have been made of any olfactory epithelium of any bird species thus far. Here, we assembled a high-quality genome and nasal epithelium transcriptome of the Leach’s storm-petrel (Oceanodroma leucorhoa) to extensively characterize their OR repertoire. Using a depth-of-coverage-assisted counting method, we estimated over 160 intact OR genes (∼500 including OR fragments). This method reveals the highest number of intact OR genes and the lowest proportion of pseudogenes compared to other waterbirds studied, and suggests that rates of OR gene duplication vary between major clades of birds, with particularly high rates in passerines. OR expression patterns reveal two OR genes (OR6-6 and OR5-11) highly expressed in adults, and four OR genes (OR14-14, OR14-12, OR10-2, and OR14-9) differentially expressed between age classes of storm-petrels. All four genes differentially expressed between age classes were more highly expressed in chicks compared to adults, suggesting that OR genes may exhibit ontogenetic specializations. Three highly differentially expressed OR genes also had high copy number ratios, suggesting that expression variation may be linked to copy number in the genome. We provide better estimates of OR gene number by using a copy number-assisted counting method, and document ontogenetic changes in OR gene expression that may be linked to olfactory specialization. These results provide valuable insight into the expression, development, and macroevolution of olfaction in seabirds.

multigene family evolutionolfactionolfactory receptor genesOR gene duplicationprocellariiform seabirdstorm-petrel

Lewin HA, Richards S, Aiden EL, Allende ML, Archibaldg JM, Bálint M, Barker KB, Baumgartner B, Belov K, Bertorelle G, et al. The Earth BioGenome Project 2020: Starting the clock. Proceedings of the National Academy of Sciences. 2022;119 (4). Publisher's VersionAbstract
November 2020 marked 2 y since the launch of the Earth BioGenome Project (EBP), which aims to sequence all known eukaryotic species in a 10-y timeframe. Since then, significant progress has been made across all aspects of the EBP roadmap, as outlined in the 2018 article describing the project’s goals, strategies, and challenges (1). The launch phase has ended and the clock has started on reaching the EBP’s major milestones. This Special Feature explores the many facets of the EBP, including a review of progress, a description of major scientific goals, exemplar projects, ethical legal and social issues, and applications of biodiversity genomics. In this Introduction, we summarize the current status of the EBP, held virtually October 5 to 9, 2020, including recent updates through February 2021. References to the nine Perspective articles included in this Special Feature are cited to guide the reader toward deeper understanding of the goals and challenges facing the EBP.
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Blaxter M, Archibald JM, Childers AK, Coddington JA, Crandall KA, Di Palma F, Durbin R, Edwards SV, Graves JAM, Hackett KJ, et al. Why sequence all eukaryotes?. Proceedings of the National Academy of Sciences. 2022;119 (4). Publisher's VersionAbstract
Life on Earth has evolved from initial simplicity to the astounding complexity we experience today. Bacteria and archaea have largely excelled in metabolic diversification, but eukaryotes additionally display abundant morphological innovation. How have these innovations come about and what constraints are there on the origins of novelty and the continuing maintenance of biodiversity on Earth? The history of life and the code for the working parts of cells and systems are written in the genome. The Earth BioGenome Project has proposed that the genomes of all extant, named eukaryotes—about 2 million species—should be sequenced to high quality to produce a digital library of life on Earth, beginning with strategic phylogenetic, ecological, and high-impact priorities. Here we discuss why we should sequence all eukaryotic species, not just a representative few scattered across the many branches of the tree of life. We suggest that many questions of evolutionary and ecological significance will only be addressable when whole-genome data representing divergences at all of the branchings in the tree of life or all species in natural ecosystems are available. We envisage that a genomic tree of life will foster understanding of the ongoing processes of speciation, adaptation, and organismal dependencies within entire ecosystems. These explorations will resolve long-standing problems in phylogenetics, evolution, ecology, conservation, agriculture, bioindustry, and medicine. genome j diversity j ecology j evolution j conservation
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Whittington CM, Van Dyke JU, Liang SQT, Edwards SV, Shine R, Grueber CE. Understanding the evolution of viviparity using intraspecific variation in reproductive mode and transitional forms of pregnancyBiological Reviews . Biological Reviews. 2022. Publisher's VersionAbstract
How innovations such as vision, flight and pregnancy evolve is a central question in evolutionary biology. Examination of transitional (intermediate) forms of these traits can help address this question, but these intermediate phenotypes are very rare in extant species. Here we explore the biology and evolution of transitional forms of pregnancy that are midway between the ancestral state of oviparity (egg-laying) and the derived state, viviparity (live birth). Transitional forms of pregnancy occur in only three vertebrates, all of which are lizard species that also display intraspecific variation in reproductive phenotype. In these lizards (Lerista bougainvilliiSaiphos equalis, and Zootoca vivipara), geographic variation of three reproductive forms occurs within a single species: oviparity, viviparity, and a transitional form of pregnancy. This phenomenon offers the valuable prospect of watching ‘evolution in action’. In these species, it is possible to conduct comparative research using different reproductive forms that are not confounded by speciation, and are of relatively recent origin. We identify major proximate and ultimate questions that can be addressed in these species, and the genetic and genomic tools that can help us understand how transitional forms of pregnancy are produced, despite predicted fitness costs. We argue that these taxa represent an excellent prospect for understanding the major evolutionary shift between egg-laying and live birth, which is a fundamental innovation in the history of animals.
Termignoni-Garcia F, Kirchman JJ, Kirchman J, Clark J, Edwards SV. Comparative Population Genomics of Cryptic Speciation and Adaptive Divergence in Bicknell’s and Gray-Cheeked Thrushes (Aves: Catharus bicknelli and Catharus minimus). Genome Biology and Evolution. 2022;14 (1) :evab255. Publisher's VersionAbstract
Cryptic speciation may occur when reproductive isolation is recent or the accumulation of morphological differences between sister lineages is slowed by stabilizing selection preventing phenotypic differentiation. In North America, Bicknell’s Thrush (Catharus bicknelli) and its sister species, the Gray-cheeked Thrush (Catharus minimus), are parapatrically breeding migratory songbirds, distinguishable in nature only by subtle differences in song and coloration, and were recognized as distinct species only in the 1990s. Previous molecular studies have estimated that the species diverged approximately 120,000–420,000 YBP and found very low levels of introgression despite their similarity and sympatry in the spring (prebreeding) migration. To further clarify the history, genetic divergence, genomic structure, and adaptive processes in C. bicknelli and C. minimus, we sequenced and assembled highcoverage reference genomes of both species and resequenced genomes from population samples of C. bicknelli, C. minimus, and two individuals of the Swainson’s Thrush (Catharus ustulatus). The genome of C. bicknelli exhibits markedly higher abundances of transposable elements compared with other Catharus and chicken. Demographic and admixture analyses confirm moderate genome-wide differentiation (Fst 0.10) and limited gene flow between C. bicknelli and C. minimus, but suggest a more recent divergence than estimates based on mtDNA. We find evidence of rapid evolution of the Z-chromosome and elevated divergence consistent with natural selection on genomic regions near genes involved with neuronal processes in C. bicknelli. These genomes are a useful resource for future investigations of speciation, migration, and adaptation in Catharus thrushes. Key words: transposable element, speciation, selective sweeps, divergence time, effective population size.
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Edwards SV, Robin VV, Ferrand N, Moritz C. The evolution of comparative phylogeography: putting the geography (and more) into comparative population genomics. Genome Biology and Evolution. 2022;14 (1) :evab176. Publisher's VersionAbstract

Comparative population genomics is an ascendant field using genomic comparisons between species to draw inferences about forces regulating genetic variation. Comparative phylogeography, by contrast, focuses on the shared lineage histories of species codistributed geographically and is decidedly organismal in perspective. Comparative phylogeography is approximately 35 years old, and, by some metrics, is showing signs of reduced growth. Here, we contrast the goals and methods of comparative population genomics and comparative phylogeography and argue that comparative phylogeography offers an important perspective on evolutionary history that succeeds in integrating genomics with landscape evolution in ways that complement the suprageographic perspective of comparative population genomics. Focusing primarily on terrestrial vertebrates, we review the history of comparative phylogeography, its milestones and ongoing conceptual innovations, its increasingly global focus, and its status as a bridge between landscape genomics and the process of speciation. We also argue that, as a science with a strong “sense of place,” comparative phylogeography offers abundant “place-based” educational opportunities with its focus on geography and natural history, as well as opportunities for collaboration with local communities and indigenous peoples. Although comparative phylogeography does not yet require whole-genome sequencing for many of its goals, we conclude that it nonetheless plays an important role in grounding our interpretation of genetic variation in the fundamentals of geography and Earth history.

Gott Earth projectionwhole-genome sequencinglandscape genomicsplace-based educationindigenous knowledge

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2021
Card DC, Shapiro B, Girabet G, Moritz C, Edwards SV. Museum genomics. Annual Review of Genetics. 2021;55 :633-59. Publisher's VersionAbstract
Anthropocene, ancient DNA, cryogenic collections, museomics, museum curation, natural history collections Abstract Natural history collections are invaluable repositories of biological information that provide an unrivaled record of Earth’s biodiversity. Museum genomics—genomics research using traditional museum and cryogenic collections and the infrastructure supporting these investigations—has particularly enhanced research in ecology and evolutionary biology, the study of extinct organisms, and the impact of anthropogenic activity on biodiversity. However, leveraging genomics in biological collections has exposed challenges, such as digitizing, integrating, and sharing collections data; updating practices to ensure broadly optimal data extraction from existing and new collections; and modernizing collections practices, infrastructure, and policies to ensure fair, sustainable, and genomically manifold uses of museum collections by increasingly diverse stakeholders. Museum genomics collections are poised to address these challenges and, with increasingly sensitive genomics approaches, will catalyze a future era of reproducibility, innovation, and insight made possible through integrating museum and genome sciences.
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Bravo GA, Schmitt CJ, Edwards SV. What have we learned from the first 500 avian genomes?. Annual Review of Ecology, Evolution, and Systematics. 2021;52 :611-639. Publisher's VersionAbstract

The increased capacity of DNA sequencing has significantly advanced our understanding of the phylogeny of birds and the proximate and ultimate mechanisms molding their genomic diversity. In less than a decade, the number of available avian reference genomes has increased to over 500—approximately 5% of bird diversity—placing birds in a privileged position to advance the fields of phylogenomics and comparative, functional, and population genomics. Whole-genome sequence data, as well as indels and rare genomic changes, are further resolving the avian tree of life. The accumulation of bird genomes, increasingly with long-read sequence data, greatly improves the resolution of genomic features such as germline-restricted chromosomes and the W chromosome, and is facilitating the comparative integration of genotypes and phenotypes. Community-based initiatives such as the Bird 10,000 Genomes Project and Vertebrate Genome Project are playing a fundamental role in amplifying and coalescing a vibrant international program in avian comparative genomics.

Keywords

comparative genomicsphylogenomicsgenome evolutionAvesa posteriori marker selectionchromosomes

Toda Y, Ko M-C, Miller ET, Rico-Guevara A, Nakagita T, Sakakibara A, Uemura K, Sackton T, Hayakawa T, Sin SYW, et al. Early origin of sweet perception in the songbird radiation. Science. 2021;373 (6551) :226-231. Publisher's VersionAbstract
Seeing a bird eat nectar from a flower is a common sight in our world. The ability to detect sugars, however, is not ancestral in the bird lineage, where most species were carnivorous. Toda et al. looked at receptors within the largest group of birds, the passerines or songbirds, and found that the emergence of sweet detection involved a single shift in a receptor for umami (see the Perspective by Barker). This ancient change facilitated sugar detection not just in nectar feeding birds, but also across the songbird group, and in a way that was different from, though convergent with, that in hummingbirds.
Sarre SD, Duncan RP, Dickman CD, Edwards SV, Greeville A, Wardle G, Gruber B. slimr: An R package for integrating data and tailor-made population genomic simulations over space and time. bioRxiv. 2021. Publisher's VersionAbstract
Software for realistically simulating complex population genomic processes is revolutionizing our understanding of evolutionary processes, and providing novel opportunities for integrating empirical data with simulations. However, the integration between simulation software and software designed for working with empirical data is currently not well developed. In particular, SLiM 3.0, which is one of the most powerful population genomic simulation frameworks for linking evolutionary dynamics with ecological patterns and processes is a standalone scripting language with limited data manipulation abilities. Here we present slimr, an R package designed to create a available under aCC-BY-NC-ND 4.0 International license. (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made bioRxiv preprint doi: https://doi.org/10.1101/2021.08.05.455258; this version posted August 6, 2021. The copyright holder for this preprint seamless link between SLiM 3.0 and the R development environment, with its powerful data manipulation and analysis tools. ● We show how slimr, in combination with SliM, facilitates smooth integration between genetic data, ecological data and simulation in a single environment. The package enables pipelines that begin with data reading, cleaning, and manipulation, proceed to constructing empirically-based parameters and initial conditions for simulations, then to running numerical simulations, and finally to retrieving simulation results in a format suitable for comparisons with empirical data – aided by advanced analysis and visualization tools provided by R (such as ABC and deep learning). ● We demonstrate the use of slimr with an example from our own work on the landscape population genomics of desert mammals, highlighting the advantage of having a single integrated tool for both data analysis and simulation. ● slimr makes the powerful simulation ability of SliM 3.0 directly accessible to R users, allowing integrated simulation projects that incorporate empirical data without the need to switch between software environments. This should provide more opportunities for evolutionary biologists and ecologists to use realistic simulations to better understand the interplay between ecological and evolutionary processes. slimr is available at https://rdinnager.github.io/slimr/. Keywords: population genomics; simulation; landscape genomics; evolution; ecology; evolutionary ecology; application; software
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Feng S, Stiller J, Deng Y, Armstrong J, Fang Q, Reeve AH, Xie D, Chen G, Guo C, Faircloth BC, et al. Author Correction: Dense sampling of bird diversity increases power of comparative genomics. Nature. 2021;592 (7856) :E24-E24. Publisher's VersionAbstract
In Supplementary Table 1 of this Article, 23 samples (B10K-DU-029-32, B10K-DU-029-33, B10K-DU-029-36 to B10K-DU-029-44, B10K-DU-029-46, B10K-DU-029-47, B10K-DU-029-49 to B10K-DU-029-53, B10K-DU-029-75 to B10K-DU-029-77, B10K-DU-029-80, and B10K-DU-030-03; styled in boldface in the revised table) were assigned to the incorrect institution. Supplementary Table 1 has been amended to reflect the correct source institution for these samples, and associated data (tissue, museum ID/source specimen ID, site, state/province, latitude, longitude, date collected and sex) have been updated accordingly. The original table is provided as Supplementary Information to this Amendment, and the original Article has been corrected online.
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Sin SYW, Hoover BA, Nevitt GA, Edwards SV. Demographic history, not mating system, explains signatures of inbreeding and inbreeding depression in a large outbred population. The American Naturalist. 2021;197 (6) :658-676. Publisher's VersionAbstract
Inbreeding depression is often found in small, inbred populations, but whether it can be detected in and have evolutionary consequences for large, wide-ranging populations is poorly known. Here, we investigate the possibility of inbreeding in a large population to determine whether mild levels of inbreeding can still have genetic and phenotypic consequences and how genomically widespread these effects can be. We apply genome-wide methods to investigate whether individual and parental heterozygosity is related to morphological, growth, or life-history traits in a pelagic seabird, Leach’s storm-petrel (Oceanodroma leucorhoa). Examining 560 individuals as part of a multiyear study, we found a substantial effect of maternal heterozygosity on chick traits: chicks from less heterozygous (relatively inbred) mothers were significantly smaller than chicks from more heterozygous (noninbred) mothers. We show that these heterozygosity-fitness correlations were due to general genome-wide effects and demonstrate a correlation between heterozygosity and inbreeding, suggesting inbreeding depression. We used population genetic models to further show that the variance in inbreeding was probably due to past demographic events rather than the current mating system and ongoing mate choice. Our findings demonstrate that inbreeding depression can be observed in large populations and illustrate how the integration of genomic techniques and fieldwork can elucidate its underlying causes.
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Wang P, Burley JT, Liu Y, Chang J, Chen D, Lu Q, Li S-H, Zhou X, Edwards SV, Zhang Z. Genomic Consequences of Long-Term Population Decline in Brown Eared Pheasant. Molecular Biology and Evolution. 2021;38 (1) :263-273. Publisher's VersionAbstract
Population genetic theory and empirical evidence indicate that deleterious alleles can be purged in small populations. However, this viewpoint remains controversial. It is unclear whether natural selection is powerful enough to purge deleterious mutations when wild populations continue to decline. Pheasants are terrestrial birds facing a long-term risk of extinction as a result of anthropogenic perturbations and exploitation. Nevertheless, there are scant genomics resources available for conservation management and planning. Here, we analyzed comparative population genomic data for the three extant isolated populations of Brown eared pheasant (Crossoptilon mantchuricum) in China. We showed that C. mantchuricum has low genome-wide diversity and a contracting effective population size because of persistent declines over the past 100,000 years. We compared genome-wide variation in C. mantchuricum with that of its closely related sister species, the Blue eared pheasant (C. auritum) for which the conservation concern is low. There were detrimental genetic consequences across all C. mantchuricum genomes including extended runs of homozygous sequences, slow rates of linkage disequilibrium decay, excessive loss-of-function mutations, and loss of adaptive genetic diversity at the major histocompatibility complex region. To the best of our knowledge, this study is the first to perform a comprehensive conservation genomic analysis on this threatened pheasant species. Moreover, we demonstrated that natural selection may not suffice to purge deleterious mutations in wild populations undergoing long-term decline. The findings of this study could facilitate conservation planning for threatened species and help recover their population size.
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Toda Y, Ko M-C, Liang Q, Miller ET, Rico-Guevara A, Nakagita T, Sakakibara A, Uemura K, Sackton T, Hayakawa T, et al. Early origin of sweet perception in the songbird radiation. Science. 2021;373 (6551) :226-231. Publisher's VersionAbstract
Early events in the evolutionary history of a clade can shape the sensory systems of descendant lineages. Although the avian ancestor may not have had a sweet receptor, the widespread incidence of nectar-feeding birds suggests multiple acquisitions of sugar detection. In this study, we identify a single early sensory shift of the umami receptor (the T1R1-T1R3 heterodimer) that conferred sweet-sensing abilities in songbirds, a large evolutionary radiation containing nearly half of all living birds. We demonstrate sugar responses across species with diverse diets, uncover critical sites underlying carbohydrate detection, and identify the molecular basis of sensory convergence between songbirds and nectar-specialist hummingbirds. This early shift shaped the sensory biology of an entire radiation, emphasizing the role of contingency and providing an example of the genetic basis of convergence in avian evolution.
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Lamichhaney S, Catullo R, Keogh K, Clulow S, Edwards SV. A bird-like genome from a frog: Mechanisms of genome size reduction in the ornate burrowing frog, Platyplectrum ornatum. Proceedings of the National Academy of Sciences. 2021;118 (11). Publisher's VersionAbstract
The diversity of genome sizes across the tree of life is of key interest in evolutionary biology. Various correlates of variation in genome size, such as accumulation of transposable elements (TEs) or rate of DNA gain and loss, are well known, but the underlying molecular mechanisms driving or constraining genome size are poorly understood. Here, we study one of the smallest genomes among frogs characterized thus far, that of the ornate burrowing frog (Platyplectrum ornatum) from Australia, and compare it to other published frog and vertebrate genomes to examine the forces driving reduction in genome size. At ∼1.06 gigabases (Gb), the P. ornatum genome is like that of birds, revealing four major mechanisms underlying TE dynamics: reduced abundance of all major classes of TEs; increased net deletion bias in TEs; drastic reduction in intron lengths; and expansion via gene duplication of the repertoire of TE-suppressing Piwi genes, accompanied by increased expression of Piwi-interacting RNA (piRNA)-based TE-silencing pathway genes in germline cells. Transcriptomes from multiple tissues in both sexes corroborate these results and provide insight into sex-differentiation pathways in Platyplectrum. Genome skimming of two closely related frog species (Lechriodus fletcheri and Limnodynastes fletcheri) confirms a reduction in TEs as a major driver of genome reduction in Platyplectrum and supports a macroevolutionary scenario of small genome size in frogs driven by convergence in life history, especially rapid tadpole development and tadpole diet. The P. ornatum genome offers a model for future comparative studies on mechanisms of genome size reduction in amphibians and vertebrates generally.
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2020
Edwards SV. Bicycling, Birding and #BLM across America in a Summer of Chaos. Biodiversity Information Science and Standards. 2020;4 (e59303). Publisher's VersionAbstract
From 6 June to 20 August, 2020, I undertook a 76-day, ~3800 mile bicycle trip across the United States from the Atlantic to the Pacific oceans. In this talk I will share with you some of the amazing people, landscapes and birds I encountered, mostly in rural towns and along blue highways. The gradually changing birdscape, both in sight and sound, underscored the sensitive ecological gradients to which birds respond, as well as the ability of some species to thrive in agricultural monocultures. Rivers large and small regularly benchmarked my progress, as well as the western journey of Lewis & Clark over 200 years ago. The recent incidents in the US involving African Americans as targets of white violence inexorably caused me to festoon my bicycle with #BlackLivesMatter (#BLM) signs and share my experiences on social media. I encountered a variety of reactions, often positive and occasionally sharply negative, in a sea of generosity and extraordinary kindness as I wheeled my way through towns on the brink of collapse, vast private ranches and the occasional city. Rural America exhibits an abundance of loyalty and empathy for local communities, yet it is sometimes hard for Americans – myself included – to empathize with people they have never met in person. Two imperatives I took away, with ramifications for both biodiversity and political stability, were the need to somehow bring divergent communities together and to encourage empathy at the national level, among communities that otherwise experience each other only on TV.
Sin SYW, Lu L, Edwards SV. De Novo Assembly of the Northern Cardinal (Cardinalis cardinalis) Genome Reveals Candidate Regulatory Regions for Sexually Dichromatic Red Plumage Coloration. G3: Genes, Genomes, Genetics. 2020;10 (10) :3541–3548.
Feng S, Stiller J, Deng Y, Armstrong J, Fang Q, Reeve AH, Xie D, Chen G, Guo C, Faircloth BC, et al. Dense sampling of bird diversity increases power of comparative genomics. Nature. 2020;587 (7833) :252–257.
Hedrick BP, Heberling MJ, Meineke EK, Turner KG, Grassa CJ, Park DS, Kennedy J, Clarke JA, Cook JA, Blackburn DC, et al. Digitization and the future of natural history collections. BioScience. 2020;70 (3) :243–251.

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