What Have We Learned from the First 500 Avian Genomes?

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. Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 52 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Taxonomic sampling and rare genomic changes overcome long-branch attraction in the phylogenetic placement of pseudoscorpions

Long-branch attraction is a systematic artifact that results in erroneous groupings of fast-evolving taxa. The combination of short, deep internodes in tandem with LBA artifacts has produced empirically intractable parts of the Tree of Life. One such group is the arthropod subphylum Chelicerata, whose backbone phylogeny has remained unstable despite improvements in phylogenetic methods and genome-scale datasets. Pseudoscorpion placement is particularly variable across datasets and analytical frameworks, with this group either clustering with other long-branch orders or with Arachnopulmonata (scorpions and tetrapulmonates). To surmount LBA, we investigated the effect of taxonomic sampling via sequential deletion of basally branching pseudoscorpion superfamilies, as well as varying gene occupancy thresholds in supermatrices. We show that concatenated supermatrices and coalescent-based summary species tree approaches support a sister group relationship of pseudoscorpions and scorpions, when more of the basally branching taxa are sampled. Matrix completeness had demonstrably less influence on tree topology. As an external arbiter of phylogenetic placement, we leveraged the recent discovery of an ancient genome duplication in the common ancestor of Arachnopulmonata as a litmus test for competing hypotheses of pseudoscorpion relationships. We generated a high-quality developmental transcriptome and the first genome for pseudoscorpions to assess the incidence of arachnopulmonate-specific duplications (e.g., homeobox genes and miRNAs). Our results support the inclusion of pseudoscorpions in Arachnopulmonata (new definition), as the sister group of scorpions. Panscorpiones (new name) is proposed for the clade uniting Scorpiones and Pseudoscorpiones.

Taxonomic sampling and rare genomic changes overcome long-branch attraction in the phylogenetic placement of pseudoscorpions

Long-branch attraction is a systematic artifact that results in erroneous groupings of fast-evolving taxa. The combination of short, deep internodes in tandem with LBA artifacts has produced empirically intractable parts of the Tree of Life. One such group is the arthropod subphylum Chelicerata, whose backbone phylogeny has remained unstable despite improvements in phylogenetic methods and genome-scale datasets. Pseudoscorpion placement is particularly variable across datasets and analytical frameworks, with this group either clustering with other long-branch orders or with Arachnopulmonata (scorpions and tetrapulmonates). To surmount LBA, we investigated the effect of taxonomic sampling via sequential deletion of basally branching pseudoscorpion superfamilies, as well as varying gene occupancy thresholds in supermatrices. We show that concatenated supermatrices and coalescent-based summary species tree approaches support a sister group relationship of pseudoscorpions and scorpions, when more of the basally branching taxa are sampled. Matrix completeness had demonstrably less influence on tree topology. As an external arbiter of phylogenetic placement, we leveraged the recent discovery of an ancient genome duplication in the common ancestor of Arachnopulmonata as a litmus test for competing hypotheses of pseudoscorpion relationships. We generated a high-quality developmental transcriptome and the first genome for pseudoscorpions to assess the incidence of arachnopulmonate-specific duplications (e.g., homeobox genes and miRNAs). Our results support the inclusion of pseudoscorpions in Arachnopulmonata, as the sister group of scorpions. Panscorpiones (new name) is proposed for the clade uniting Scorpiones and Pseudoscorpiones.

Plastome phylogenomics and characterization of rare genomic changes as taxonomic markers in plastome groups 1 and 2 Poeae (Pooideae; Poaceae)

A phylogenomic analysis of 42 complete plastid genomes (plastomes), including 16 that were newly sequenced, was conducted. Plastomes were sampled from 19 subtribes of Pooideae, to investigate relationships within and between Chloroplast Group 1 (Aveneae) and Group 2 (Poeae) species. Two data partitions: complete plastomes, and a combined plastome and rare genomic change (RGC) data matrix, were analyzed. Overall, 156 non-ambiguous RGC were identified, of which homology was inferred for 38 RGC. Among the 38 RGC identified, six were synapomorphic among the Group 1 subtribes: Aveninae, Agrostidinae, and Anthoxanthinae, (Phalaridinae + Torreyochloinae), and 27 were synapomorphic among the Group 2 subtribes: Loliinae, (Ammochloinae + Parapholiinae + Dactylidinae), Parapholiinae, Dactylidinae, Poinae, and Coleanthinae. Four RGC were determined to be homoplasious in Groups 1 and 2. Two other RGC originated through intrastrand deletion events. The remaining RGC events likely originated through recombination given their size and lack of sequence evidence for other types of mutations. This study also determined that relationships between taxa, even those only weakly supported in previous studies, could be inferred with strong support when utilizing complete plastomes.

Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus

ABSTRACTTardigrada, a phylum of meiofaunal organisms, have been at the center of discussions of the evolution of Metazoa, the biology of survival in extreme environments, and the role of horizontal gene transfer in animal evolution. Tardigrada are placed as sisters to Arthropoda and Onychophora (velvet worms) in the superphylum Ecdysozoa by morphological analyses, but many molecular phylogenies fail to recover this relationship. This tension between molecular and morphological understanding may be very revealing of the mode and patterns of evolution of major groups. Similar to bdelloid rotifers, nematodes and other animals of the water film, limno-terrestrial tardigrades display extreme cryptobiotic abilities, including anhydrobiosis and cryobiosis. These extremophile behaviors challenge understanding of normal, aqueous physiology: how does a multicellular organism avoid lethal cellular collapse in the absence of liquid water? Meiofaunal species have been reported to have elevated levels of HGT events, but how important this is in evolution, and in particular in the evolution of extremophile physiology, is unclear. To address these questions, we resequenced and reassembled the genome of Hypsibius dujardini, a limno-terrestrial tardigrade that can undergo anhydrobiosis only after extensive pre-exposure to drying conditions, and compared it to the genome of Ramazzottius varieornatus, a related species with tolerance to rapid desiccation. The two species had contrasting gene expression responses to anhydrobiosis, with major transcriptional change in H. dujardini but limited regulation in R. varieornatus. We identified few horizontally transferred genes, but some of these were shown to be involved in entry into anhydrobiosis. Whole-genome molecular phylogenies supported a Tardigrada+Nematoda relationship over Tardigrada+Arthropoda, but rare genomic changes tended to support Tardigrada+Arthropoda.

Genomic analysis reveals hidden biodiversity within colugos, the sister group to primates

Colugos are among the most poorly studied mammals despite their centrality to resolving supraordinal primate relationships. Two described species of these gliding mammals are the sole living members of the order Dermoptera, distributed throughout Southeast Asia. We generated a draft genome sequence for a Sunda colugo and a Philippine colugo reference alignment, and used these to identify colugo-specific genetic changes that were enriched in sensory and musculoskeletal-related genes that likely underlie their nocturnal and gliding adaptations. Phylogenomic analysis and catalogs of rare genomic changes overwhelmingly support the contested hypothesis that colugos are the sister group to primates (Primatomorpha), to the exclusion of treeshrews. We captured ~140 kb of orthologous sequence data from colugo museum specimens sampled across their range and identified large genetic differences between many geographically isolated populations that may result in a >300% increase in the number of recognized colugo species. Our results identify conservation units to mitigate future losses of this enigmatic mammalian order.