Whole-genome Analyses Reveal Past Population Fluctuations and Low Genetic Diversities of the North Pacific Albatrosses.

Throughout the Plio-Pleistocene, climate change has impacted tropical marine ecosystems substantially, with even more severe impacts predicted in the Anthropocene. Although many studies have clarified demographic histories of seabirds in polar regions, the history of keystone seabirds of the tropics is unclear, despite the prominence of albatrosses (Diomedeidae, Procellariiformes) as the largest and most threatened group of oceanic seabirds. To understand the impact of climate change on tropical albatrosses, we investigated the evolutionary and demographic histories of all four North Pacific albatrosses and their prey using whole-genome analyses. We report a striking concordance in demographic histories among the four species, with a notable dip in effective population size at the beginning of the Pleistocene and a population expansion in the Last Glacial Period when sea levels were low, which resulted in increased potential coastal breeding sites. Abundance of the black-footed albatross dropped again during the Last Glacial Maximum, potentially linked to climate-driven loss of breeding sites and concordant genome-derived decreases in its major prey. We find very low genome-wide (π < 0.001) and adaptative genetic diversities across the albatrosses, with genes of the major histocompatibility complex close to monomorphic. We also identify recent selective sweeps at genes associated with hyperosmotic adaptation, longevity, and cognition and memory. Our study has shed light on the evolutionary and demographic histories of the largest tropical oceanic seabirds and provides evidence for their large population fluctuations and alarmingly low genetic diversities.

Museomics and phylogenomics of lovebirds (Psittaciformes, Psittaculidae, Agapornis) using low-coverage whole-genome sequencing.

Natural history collections contain specimens that provide important insights into studies of ecology and evolution. With the advancement of high-throughput sequencing, historical DNA (hDNA) from museum specimens has become a valuable source of genomic data to study the evolutionary history of organisms. Low-coverage whole genome sequencing (WGS) has been increasingly applied to museum specimens for analyzing organelle genomes, but is still uncommon for genotyping the nuclear DNA fraction. In this study, we applied low-coverage WGS to phylogenomic analyses of parrots in the genus Agapornis by including both modern samples and historical specimens of âˆ¼100-year-old. Agapornis are small-sized African and Malagasy parrots with diverse characters. Earlier phylogenetic studies failed to resolve the positions of some key lineages, prohibiting a robust interpretation of the biogeography and evolution of these African parrots. Here, we demonstrated the use of low-coverage WGS for generating both mitochondrial and nuclear genomic data, and evaluated data quality differences between modern and historical samples. Our resolved Agapornis phylogeny indicates the ancestor of Agapornis likely colonized Madagascar from Australasia by trans-oceanic dispersal events before dispersing to the African continent. Genome-wide SNPs also allowed us to identify the parental origins of hybrid Agapornis individuals. This study demonstrates the potential of applying low-coverage WGS to phylogenomics and population genomics analyses and illustrates how including historical museum specimens can address outstanding questions regarding the evolutionary history of contemporary lineages.

Eco-genetic additivity of diploids in allopolyploid wild wheats.

Underpinnings of the distribution of allopolyploid species (hybrids with duplicated genome) along spatial and ecological gradients are elusive. As allopolyploid speciation combines the range of genetic and ecological characteristics of divergent diploids, allopolyploids initially show their additivity and are predicted to evolve differentiated ecological niches to establish in face of their competition. Here, we use four diploid wild wheats that differentially combined into four independent allopolyploid species to test for such additivity and assess the impact of ecological constraints on species ranges. Divergent genetic variation from diploids being fixed in heterozygote allopolyploids supports their genetic additivity. Spatial integration of comparative phylogeography and modelling of climatic niches supports ecological additivity of locally adapted diploid progenitors into allopolyploid species which subsequently colonised wide ranges. Allopolyploids fill suitable range to a larger extent than diploids and conservative evolution following the combination of divergent species appears to support their expansion under environmental changes.

Hybridization preceded radiation in diploid wheats.

Evolutionary relationships among the Aegilops-Triticum relatives of cultivated wheats have been difficult to resolve owing to incomplete lineage sorting and reticulate evolution. Recent studies have suggested that the wheat D-genome lineage (progenitor of Ae. tauschii) originated through homoploid hybridization between the A-genome lineage (progenitor of Triticum s.str.) and the B-genome lineage (progenitor of Ae. speltoides). This scenario of reticulation has been debated, calling for adequate phylogenetic analyses based on comprehensive sampling. To reconstruct the evolution of Aegilops-Triticum diploids, we here combined high-throughput sequencing of 38 nuclear low-copy loci of multiple accessions of all 13 species with inferences of the species phylogeny using the full-parameterized MCMC_SEQ method. Phylogenies recovered a monophyletic Aegilops-Triticum lineage that began diversifying ~6.6 Ma ago and gave rise to four sublineages, i.e. the A- (2 species), B- (1 species), D- (9 species) and T- (Ae. mutica) genome lineage. Full-parameterized phylogenies as well as patterns of tree dilation and tree compression supported a hybrid origin of the D-genome lineage from A and B ~3.0-4.0 Ma ago, and did not indicate additional hybridization events. Conflicting ABBA-BABA tests suggestive of further reticulation were shown here to result from ancestral population structure rather than hybridization. This comprehensive and dated phylogeny of wheat relatives indicates that the origin of the hybrid D-genome was followed by intense diversification into the majority of extant diploid as well as allopolyploid wild wheats.

Embracing heterogeneity: coalescing the Tree of Life and the future of phylogenomics.

Building the Tree of Life (ToL) is a major challenge of modern biology, requiring advances in cyberinfrastructure, data collection, theory, and more. Here, we argue that phylogenomics stands to benefit by embracing the many heterogeneous genomic signals emerging from the first decade of large-scale phylogenetic analysis spawned by high-throughput sequencing (HTS). Such signals include those most commonly encountered in phylogenomic datasets, such as incomplete lineage sorting, but also those reticulate processes emerging with greater frequency, such as recombination and introgression. Here we focus specifically on how phylogenetic methods can accommodate the heterogeneity incurred by such population genetic processes; we do not discuss phylogenetic methods that ignore such processes, such as concatenation or supermatrix approaches or supertrees. We suggest that methods of data acquisition and the types of markers used in phylogenomics will remain restricted until a posteriori methods of marker choice are made possible with routine whole-genome sequencing of taxa of interest. We discuss limitations and potential extensions of a model supporting innovation in phylogenomics today, the multispecies coalescent model (MSC). Macroevolutionary models that use phylogenies, such as character mapping, often ignore the heterogeneity on which building phylogenies increasingly rely and suggest that assimilating such heterogeneity is an important goal moving forward. Finally, we argue that an integrative cyberinfrastructure linking all steps of the process of building the ToL, from specimen acquisition in the field to publication and tracking of phylogenomic data, as well as a culture that values contributors at each step, are essential for progress.