Population Genomics Reveal Recent Speciation and Rapid Evolutionary Adaptation in Polar Bears
Shiping LiuEline D. LorenzenMatteo FumagalliBo LiKelley HarrisZijun XiongLong ZhouThorfinn Sand KorneliussenMehmet SomelCourtney C. BabbittGreg WrayJianwen LiWeiming HeZhuo WangWenjing FuXueyan XiangClaire C. MorganAoife DohertyMary J. O’ConnellJames O. McInerneyErik W. BornLove DalénRuné DietzLudovic OrlandoChristian SonneGuojie ZhangRasmus NielsenEske WillerslevJun Wang
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Lineage (genetic)
Contact zones provide an excellent arena in which to address questions about how genomic divergence evolves during lineage divergence. They allow us to both infer patterns of genomic divergence in allopatric populations isolated from introgression and to characterize patterns of introgression after lineages meet. Thusly motivated, we analyze genome-wide introgression data from four contact zones in three genera of lizards endemic to the Australian Wet Tropics. These contact zones all formed between morphologically cryptic lineage-pairs within morphologically defined species, and the lineage-pairs meeting in the contact zones diverged anywhere from 3.1 to 5.8 million years ago. By characterizing patterns of molecular divergence across an average of 11K genes and fitting geographic clines to an average of 7.5K variants, we characterize how patterns of genomic differentiation and introgression change through time. Across this range of divergences, we find that genome-wide differentiation increases but becomes no less heterogeneous. In contrast, we find that introgression heterogeneity decreases dramatically, suggesting that time helps isolated genomes "congeal." Thus, this work emphasizes the pivotal role that history plays in driving lineage divergence.
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Divergence (linguistics)
Coalescent theory
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Abstract Adaptations are features of organisms that have evolved to perform fitness‐enhancing functions. Some conceivable adaptations or combinations of adaptations do not evolve because constraints (which may vary from lineage to lineage) limit the potential of adaptive evolution.
Lineage (genetic)
Fitness landscape
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Abstract Adaptations are features of organisms that have evolved to perform fitness‐enhancing functions. Some conceivable adaptations or combinations of adaptations do not evolve because constraints (which may vary from lineage to lineage) limit the potential of adaptive evolution.
Lineage (genetic)
Fitness landscape
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Significance Determining the order and orientation of conserved chromosome segments in the genomes of extant mammals is important for understanding speciation events, and the lineage-specific adaptations that have occurred during ∼200 My of mammalian evolution. In this paper, we describe the computational reconstruction of chromosome organization for seven ancestral genomes leading to human, including the ancestor of all placental mammals. The evolutionary history of chromosome rearrangements that occurred from the time of the eutherian ancestor until the human lineage is revealed in detail. Our results provide an evolutionary basis for comparison of genome organization of all eutherians, and for revealing the genomic origins of lineage-specific adaptations.
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Ancestor
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Abstract Extinct lineages can leave legacies in the genomes of extant lineages through ancient introgressive hybridization. The patterns of genomic survival of these extinct lineages provide insight into the role of extinct lineages in current biodiversity. However, our understanding on the genomic landscape of introgression from extinct lineages remains limited due to challenges associated with locating the traces of unsampled ‘ghost’ extinct lineages without ancient genomes. Herein, we conducted population genomic analyses on the East China Sea (ECS) lineage of Chaenogobius annularis , which was suspected to have originated from ghost introgression, with the aim of elucidating its genomic origins and characterizing its landscape of introgression. By combining phylogeographic analysis and demographic modelling, we demonstrated that the ECS lineage originated from ancient hybridization with an extinct ghost lineage. Forward simulations based on the estimated demography indicated that the statistic γ of the HyDe analysis can be used to distinguish the differences in local introgression rates in our data. Consistent with introgression between extant organisms, we found reduced introgression from extinct lineage in regions with low recombination rates and with functional importance, thereby suggesting a role of linked selection that has eliminated the extinct lineage in shaping the hybrid genome. Moreover, we identified enrichment of repetitive elements in regions associated with ghost introgression, which was hitherto little known but was also observed in the re‐analysis of published data on introgression between extant organisms. Overall, our findings underscore the unexpected similarities in the characteristics of introgression landscapes across different taxa, even in cases of ghost introgression.
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Homology
R gene
Conserved sequence
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Understanding the mechanisms underlying phenotypic innovation is a key goal of comparative genomic studies. Here, we investigated the evolutionary landscape of lineage-specific accelerated regions (LinARs) across 49 primate species. Genomic comparison with dense taxa sampling of primate species significantly improved LinAR detection accuracy and revealed many novel human LinARs associated with brain development or disease. Our study also yielded detailed maps of LinARs in other primate lineages that may have influenced lineage-specific phenotypic innovation and adaptation. Functional experimentation identified gibbon LinARs, which could have participated in the developmental regulation of their unique limb structures, whereas some LinARs in the Colobinae were associated with metabolite detoxification which may have been adaptive in relation to their leaf-eating diet. Overall, our study broadens knowledge of the functional roles of LinARs in primate evolution.
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Patterns of diversification in species-rich clades provide insight into the processes that generate biological diversity. We tested different models of lineage and phenotypic diversification in an exceptional continental radiation, the ovenbird family Furnariidae, using the most complete species-level phylogenetic hypothesis produced to date for a major avian clade (97% of 293 species). We found that the Furnariidae exhibit nearly constant rates of lineage accumulation but show evidence of constrained morphological evolution. This pattern of sustained high rates of speciation despite limitations on phenotypic evolution contrasts with the results of most previous studies of evolutionary radiations, which have found a pattern of decelerating diversity-dependent lineage accumulation coupled with decelerating or constrained phenotypic evolution. Our results suggest that lineage accumulation in tropical continental radiations may not be as limited by ecological opportunities as in temperate or island radiations. More studies examining patterns of both lineage and phenotypic diversification are needed to understand the often complex tempo and mode of evolutionary radiations on continents.
Lineage (genetic)
Rate of evolution
Genetic algorithm
Adaptive Radiation
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The functional divergence of duplicate genes (ohnologues) retained from whole genome duplication (WGD) is thought to promote evolutionary diversification. However, species radiation and phenotypic diversification are often temporally separated from WGD. Salmonid fish, whose ancestor underwent WGD by autotetraploidization ~95 million years ago, fit such a ‘time-lag’ model of post-WGD radiation, which occurred alongside a major delay in the rediploidization process. Here we propose a model, ‘lineage-specific ohnologue resolution’ (LORe), to address the consequences of delayed rediploidization. Under LORe, speciation precedes rediploidization, allowing independent ohnologue divergence in sister lineages sharing an ancestral WGD event. Using cross-species sequence capture, phylogenomics and genome-wide analyses of ohnologue expression divergence, we demonstrate the major impact of LORe on salmonid evolution. One-quarter of each salmonid genome, harbouring at least 4550 ohnologues, has evolved under LORe, with rediploidization and functional divergence occurring on multiple independent occasions >50 million years post-WGD. We demonstrate the existence and regulatory divergence of many LORe ohnologues with functions in lineage-specific physiological adaptations that potentially facilitated salmonid species radiation. We show that LORe ohnologues are enriched for different functions than ‘older’ ohnologues that began diverging in the salmonid ancestor. LORe has unappreciated significance as a nested component of post-WGD divergence that impacts the functional properties of genes, whilst providing ohnologues available solely for lineage-specific adaptation. Under LORe, which is predicted following many WGD events, the functional outcomes of WGD need not appear ‘explosively’, but can arise gradually over tens of millions of years, promoting lineage-specific diversification regimes under prevailing ecological pressures.
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Adaptive Radiation
Phylogenomics
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Evolutionary dynamics in large asexual populations is strongly influenced by multiple competing beneficial lineages, most of which segregate at very low frequencies. However, technical barriers to tracking a large number of these rare lineages have so far prevented a detailed elucidation of evolutionary dynamics in large bacterial populations. Here, we overcome this hurdle by developing a chromosomal barcoding technique that allows simultaneous tracking of ∼450,000 distinct lineages in E. coli. We used this technique to gather insights into the evolutionary dynamics of large (>10 7 cells) E. coli populations propagated for ∼420 generations in the presence of sub-inhibitory concentrations of common antibiotics. By deep sequencing the barcodes, we reconstructed trajectories of individual lineages at high frequency resolution (< 10 −5 ). Using quantitative tools from ecology, we found that populations lost lineage diversity at distinct rates corresponding to their antibiotic regimen. Additionally, by quantifying the reproducibility of these dynamics across replicate populations, we found that some lineages had similar fates over independent experiments. Combined with an analysis of individual lineage trajectories, these results suggest how standing genetic variation and new mutations may contribute to adaptation to sub-inhibitory antibiotic levels. Altogether, our results demonstrate the power of high-resolution barcoding in studying the dynamics of bacterial evolution.
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Evolutionary Dynamics
Experimental Evolution
Dynamics
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