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.

Both selection and drift drive the spatial pattern of adaptive genetic variation in a wild mammal.

The major histocompatibility complex (MHC) has been intensively studied for the relative effects of different evolutionary forces in recent decades. Pathogen-mediated balancing selection is generally thought to explain the high polymorphism observed in MHC genes, but it is still unclear to what extent MHC diversity is shaped by selection relative to neutral drift. In this study, we genotyped MHC class II DRB genes and 15 neutral microsatellite loci across 26 geographic populations of European badgers (Meles meles) covering most of their geographic range. By comparing variation of microsatellite and diversity of MHC at different levels, we demonstrate that both balancing selection and drift have shaped the evolution of MHC genes. When only MHC allelic identity was investigated, the spatial pattern of MHC variation was similar to that of microsatellites. By contrast, when functional aspects of the MHC diversity (e.g., immunological supertypes) were considered, balancing selection appears to decrease genetic structuring across populations. Our comprehensive sampling and analytical approach enable us to conclude that the likely mechanisms of selection are heterozygote advantage and/or rare-allele advantage. This study is a clear demonstration of how both balancing selection and genetic drift simultaneously affect the evolution of MHC genes in a widely distributed wild mammal.

Intra-specific copy number variation of MHC class II genes in the Siamese fighting fish.

Duplicates of genes for major histocompatibility complex (MHC) molecules can be subjected to selection independently and vary markedly in their evolutionary rates, sequence polymorphism, and functional roles. Therefore, without a thorough understanding of their copy number variation (CNV) in the genome, the MHC-dependent fitness consequences within a species could be misinterpreted. Studying the intra-specific CNV of this highly polymorphic gene, however, has long been hindered by the difficulties in assigning alleles to loci and the lack of high-quality genomic data. Here, using the high-quality genome of the Siamese fighting fish (Betta splendens), a model for mate choice studies, and the whole-genome sequencing (WGS) data of 17 Betta species, we achieved locus-specific amplification of their three classical MHC class II genes - DAB1, DAB2, and DAB3. By performing quantitative PCR and depth-of-coverage analysis using the WGS data, we revealed intra-specific CNV at the DAB3 locus. We identified individuals that had two allelic copies (i.e., heterozygous or homozygous) or one allele (i.e., hemizygous) and individuals without this gene. The CNV was due to the deletion of a 20-kb-long genomic region harboring both the DAA3 and DAB3 genes. We further showed that the three DAB genes were under different modes of selection, which also applies to their corresponding DAA genes that share similar pattern of polymorphism. Our study demonstrates a combined approach to study CNV within a species, which is crucial for the understanding of multigene family evolution and the fitness consequences of CNV.

Development and characterization of microsatellite markers in Rosy-faced and other lovebirds (Agapornis spp.) using next-generation sequencing.

Agapornis are a group of small African parrots that are heavily traded around the world. They are invasive species in many places, but some of them are listed as Vulnerable or Near Threatened. However, the genetic tools for assessing inter-individual relationships, population structure, and genetic diversity of these birds are very limited. Therefore, we developed polymorphic microsatellite markers in A. roseicollis and tested the transferability on 5 lovebird species including A. personatus, A. nigrigenis, A. fischeri, A. pullarius, and A. canus, and two closely related outgroups (i.e. Bolbopsittacus lunulatus and Loriculus galgulus). We first performed whole-genome re-sequencing on five individuals of A. roseicollis to identify potential polymorphic loci. Out of 37 loci tested in 11 A. roseicollis, 27 loci were demonstrated to be polymorphic, with the number of the alleles ranging from 2 to 7 (mean = 3.963). The observed heterozygosity ranged from 0 to 0.875 (mean = 0.481) and expected heterozygosity ranged from 0.233 to 0.842 (mean = 0.642). Five loci (Agro-A13, p < 0.01; Agro-A15, p < 0.05; Agro-A43, p < 0.05, Agro-A65, p < 0.05; Agro-A67, p < 0.05) were detected to deviate from Hardy-Weinberg equilibrium, with the presence of null alleles suggested in locus Agro-A13 and Agro-A77. The exclusion powers for PE1 and PE2 are 0.997 and 0.999, respectively. The 27 novel polymorphic markers developed here will be useful for parentage and kinship assignment and population genetics study in Agapornis, and provide a tool for scientific research, captive breeding industry, and invasion and conservation management of these species.