Population genomics reveal recent speciation and rapid evolutionary adaptation in polar bears.

Polar bears are uniquely adapted to life in the High Arctic and have undergone drastic physiological changes in response to Arctic climates and a hyper-lipid diet of primarily marine mammal prey. We analyzed 89 complete genomes of polar bear and brown bear using population genomic modeling and show that the species diverged only 479-343 thousand years BP. We find that genes on the polar bear lineage have been under stronger positive selection than in brown bears; nine of the top 16 genes under strong positive selection are associated with cardiomyopathy and vascular disease, implying important reorganization of the cardiovascular system. One of the genes showing the strongest evidence of selection, APOB, encodes the primary lipoprotein component of low-density lipoprotein (LDL); functional mutations in APOB may explain how polar bears are able to cope with life-long elevated LDL levels that are associated with high risk of heart disease in humans.

Contingency, repeatability, and predictability in the evolution of a prokaryotic pangenome.

Pangenomes exhibit remarkable variability in many prokaryotic species, much of which is maintained through the processes of horizontal gene transfer and gene loss. Repeated acquisitions of near-identical homologs can easily be observed across pangenomes, leading to the question of whether these parallel events potentiate similar evolutionary trajectories, or whether the remarkably different genetic backgrounds of the recipients mean that postacquisition evolutionary trajectories end up being quite different. In this study, we present a machine learning method that predicts the presence or absence of genes in the Escherichia coli pangenome based on complex patterns of the presence or absence of other accessory genes within a genome. Our analysis leverages the repeated transfer of genes through the E. coli pangenome to observe patterns of repeated evolution following similar events. We find that the presence or absence of a substantial set of genes is highly predictable from other genes alone, indicating that selection potentiates and maintains gene-gene co-occurrence and avoidance relationships deterministically over long-term bacterial evolution and is robust to differences in host evolutionary history. We propose that at least part of the pangenome can be understood as a set of genes with relationships that govern their likely cohabitants, analogous to an ecosystem's set of interacting organisms. Our findings indicate that intragenomic gene fitness effects may be key drivers of prokaryotic evolution, influencing the repeated emergence of complex gene-gene relationships across the pangenome.

Prokaryotic Pangenomes Act as Evolving Ecosystems.

Understanding adaptation to the local environment is a central tenet and a major focus of evolutionary biology. But this is only part of the adaptionist story. In addition to the external environment, one of the main drivers of genome composition is genetic background. In this perspective, I argue that there is a growing body of evidence that intra-genomic selective pressures play a significant part in the composition of prokaryotic genomes and play a significant role in the origin, maintenance and structuring of prokaryotic pangenomes.

Evidence for Selection in the Abundant Accessory Gene Content of a Prokaryote Pangenome.

A pangenome is the complete set of genes (core and accessory) present in a phylogenetic clade. We hypothesize that a pangenome's accessory gene content is structured and maintained by selection. To test this hypothesis, we interrogated the genomes of 40 Pseudomonas species for statistically significant coincident (i.e., co-occurring/avoiding) gene patterns. We found that 86.7% of common accessory genes are involved in ≥1 coincident relationship. Further, genes that co-occur and/or avoid each other-but are not vertically inherited-are more likely to share functional categories, are more likely to be simultaneously transcribed, and are more likely to produce interacting proteins, than would be expected by chance. These results are not due to coincident genes being adjacent to one another on the chromosome. Together, these findings suggest that the accessory genome is structured into sets of genes that function together within a given strain. Given the similarity of the Pseudomonas pangenome with open pangenomes of other prokaryotic species, we speculate that these results are generalizable.

Endosymbiotic origin and differential loss of eukaryotic genes.

Chloroplasts arose from cyanobacteria, mitochondria arose from proteobacteria. Both organelles have conserved their prokaryotic biochemistry, but their genomes are reduced, and most organelle proteins are encoded in the nucleus. Endosymbiotic theory posits that bacterial genes in eukaryotic genomes entered the eukaryotic lineage via organelle ancestors. It predicts episodic influx of prokaryotic genes into the eukaryotic lineage, with acquisition corresponding to endosymbiotic events. Eukaryotic genome sequences, however, increasingly implicate lateral gene transfer, both from prokaryotes to eukaryotes and among eukaryotes, as a source of gene content variation in eukaryotic genomes, which predicts continuous, lineage-specific acquisition of prokaryotic genes in divergent eukaryotic groups. Here we discriminate between these two alternatives by clustering and phylogenetic analysis of eukaryotic gene families having prokaryotic homologues. Our results indicate (1) that gene transfer from bacteria to eukaryotes is episodic, as revealed by gene distributions, and coincides with major evolutionary transitions at the origin of chloroplasts and mitochondria; (2) that gene inheritance in eukaryotes is vertical, as revealed by extensive topological comparison, sparse gene distributions stemming from differential loss; and (3) that continuous, lineage-specific lateral gene transfer, although it sometimes occurs, does not contribute to long-term gene content evolution in eukaryotic genomes.

Origins of major archaeal clades correspond to gene acquisitions from bacteria.

The mechanisms that underlie the origin of major prokaryotic groups are poorly understood. In principle, the origin of both species and higher taxa among prokaryotes should entail similar mechanisms--ecological interactions with the environment paired with natural genetic variation involving lineage-specific gene innovations and lineage-specific gene acquisitions. To investigate the origin of higher taxa in archaea, we have determined gene distributions and gene phylogenies for the 267,568 protein-coding genes of 134 sequenced archaeal genomes in the context of their homologues from 1,847 reference bacterial genomes. Archaeal-specific gene families define 13 traditionally recognized archaeal higher taxa in our sample. Here we report that the origins of these 13 groups unexpectedly correspond to 2,264 group-specific gene acquisitions from bacteria. Interdomain gene transfer is highly asymmetric, transfers from bacteria to archaea are more than fivefold more frequent than vice versa. Gene transfers identified at major evolutionary transitions among prokaryotes specifically implicate gene acquisitions for metabolic functions from bacteria as key innovations in the origin of higher archaeal taxa.

Bipartite Network Analysis of Gene Sharings in the Microbial World.

Extensive microbial gene flows affect how we understand virology, microbiology, medical sciences, genetic modification, and evolutionary biology. Phylogenies only provide a narrow view of these gene flows: plasmids and viruses, lacking core genes, cannot be attached to cellular life on phylogenetic trees. Yet viruses and plasmids have a major impact on cellular evolution, affecting both the gene content and the dynamics of microbial communities. Using bipartite graphs that connect up to 149,000 clusters of homologous genes with 8,217 related and unrelated genomes, we can in particular show patterns of gene sharing that do not map neatly with the organismal phylogeny. Homologous genes are recycled by lateral gene transfer, and multiple copies of homologous genes are carried by otherwise completely unrelated (and possibly nested) genomes, that is, viruses, plasmids and prokaryotes. When a homologous gene is present on at least one plasmid or virus and at least one chromosome, a process of "gene externalization," affected by a postprocessed selected functional bias, takes place, especially in Bacteria. Bipartite graphs give us a view of vertical and horizontal gene flow beyond classic taxonomy on a single very large, analytically tractable, graph that goes beyond the cellular Web of Life.

Combined Analysis of Variation in Core, Accessory and Regulatory Genome Regions Provides a Super-Resolution View into the Evolution of Bacterial Populations.

The use of whole-genome phylogenetic analysis has revolutionized our understanding of the evolution and spread of many important bacterial pathogens due to the high resolution view it provides. However, the majority of such analyses do not consider the potential role of accessory genes when inferring evolutionary trajectories. Moreover, the recently discovered importance of the switching of gene regulatory elements suggests that an exhaustive analysis, combining information from core and accessory genes with regulatory elements could provide unparalleled detail of the evolution of a bacterial population. Here we demonstrate this principle by applying it to a worldwide multi-host sample of the important pathogenic E. coli lineage ST131. Our approach reveals the existence of multiple circulating subtypes of the major drug-resistant clade of ST131 and provides the first ever population level evidence of core genome substitutions in gene regulatory regions associated with the acquisition and maintenance of different accessory genome elements.

Formation of chimeric genes with essential functions at the origin of eukaryotes.

BACKGROUND: Eukaryotes evolved from the symbiotic association of at least two prokaryotic partners, and a good deal is known about the timings, mechanisms, and dynamics of these evolutionary steps. Recently, it was shown that a new class of nuclear genes, symbiogenetic genes (S-genes), was formed concomitant with endosymbiosis and the subsequent evolution of eukaryotic photosynthetic lineages. Understanding their origins and contributions to eukaryogenesis would provide insights into the ways in which cellular complexity has evolved. RESULTS: Here, we show that chimeric nuclear genes (S-genes), built from prokaryotic domains, are critical for explaining the leap forward in cellular complexity achieved during eukaryogenesis. A total of 282 S-gene families contributed solutions to many of the challenges faced by early eukaryotes, including enhancing the informational machinery, processing spliceosomal introns, tackling genotoxicity within the cell, and ensuring functional protein interactions in a larger, more compartmentalized cell. For hundreds of S-genes, we confirmed the origins of their components (bacterial, archaeal, or generally prokaryotic) by maximum likelihood phylogenies. Remarkably, Bacteria contributed nine-fold more S-genes than Archaea, including a two-fold greater contribution to informational functions. Therefore, there is an additional, large bacterial contribution to the evolution of eukaryotes, implying that fundamental eukaryotic properties do not strictly follow the traditional informational/operational divide for archaeal/bacterial contributions to eukaryogenesis. CONCLUSION: This study demonstrates the extent and process through which prokaryotic fragments from bacterial and archaeal genes inherited during eukaryogenesis underly the creation of novel chimeric genes with important functions.

The role of public goods in planetary evolution.

Biological public goods are broadly shared within an ecosystem and readily available. They appear to be widespread and may have played important roles in the history of life on Earth. Of particular importance to events in the early history of life are the roles of public goods in the merging of genomes, protein domains and even cells. We suggest that public goods facilitated the origin of the eukaryotic cell, a classic major evolutionary transition. The recognition of genomic public goods challenges advocates of a direct graph view of phylogeny, and those who deny that any useful phylogenetic signal persists in modern genomes. Ecological spillovers generate public goods that provide new ecological opportunities.This article is part of the themed issue 'Reconceptualizing the origins of life'.

Networks: expanding evolutionary thinking.

Networks allow the investigation of evolutionary relationships that do not fit a tree model. They are becoming a leading tool for describing the evolutionary relationships between organisms, given the comparative complexities among genomes.

Gene similarity networks provide tools for understanding eukaryote origins and evolution.

The complexity and depth of the relationships between the three domains of life challenge the reliability of phylogenetic methods, encouraging the use of alternative analytical tools. We reconstructed a gene similarity network comprising the proteomes of 14 eukaryotes, 104 prokaryotes, 2,389 viruses and 1,044 plasmids. This network contains multiple signatures of the chimerical origin of Eukaryotes as a fusion of an archaebacterium and a eubacterium that could not have been observed using phylogenetic trees. A number of connected components (gene sets with stronger similarities than expected by chance) contain pairs of eukaryotic sequences exhibiting no direct detectable similarity. Instead, many eukaryotic sequences were indirectly connected through a "eukaryote-archaebacterium-eubacterium-eukaryote" similarity path. Furthermore, eukaryotic genes highly connected to prokaryotic genes from one domain tend not to be connected to genes from the other prokaryotic domain. Genes of archaebacterial and eubacterial ancestry tend to perform different functions and to act at different subcellular compartments, but in such an intertwined way that suggests an early rather than late integration of both gene repertoires. The archaebacterial repertoire has a similar size in all eukaryotic genomes whereas the number of eubacterium-derived genes is much more variable, suggesting a higher plasticity of this gene repertoire. Consequently, highly reduced eukaryotic genomes contain more genes of archaebacterial than eubacterial affinity. Connected components with prokaryotic and eukaryotic genes tend to include viral and plasmid genes, compatible with a role of gene mobility in the origin of Eukaryotes. Our analyses highlight the power of network approaches to study deep evolutionary events.

Integration of two ancestral chaperone systems into one: the evolution of eukaryotic molecular chaperones in light of eukaryogenesis.

Eukaryotic genomes are mosaics of genes acquired from their prokaryotic ancestors, the eubacterial endosymbiont that gave rise to the mitochondrion and its archaebacterial host. Genomic footprints of the prokaryotic merger at the origin of eukaryotes are still discernable in eukaryotic genomes, where gene expression and function correlate with their prokaryotic ancestry. Molecular chaperones are essential in all domains of life as they assist the functional folding of their substrate proteins and protect the cell against the cytotoxic effects of protein misfolding. Eubacteria and archaebacteria code for slightly different chaperones, comprising distinct protein folding pathways. Here we study the evolution of the eukaryotic protein folding pathways following the endosymbiosis event. A phylogenetic analysis of all 64 chaperones encoded in the Saccharomyces cerevisiae genome revealed 25 chaperones of eubacterial ancestry, 11 of archaebacterial ancestry, 10 of ambiguous prokaryotic ancestry, and 18 that may represent eukaryotic innovations. Several chaperone families (e.g., Hsp90 and Prefoldin) trace their ancestry to only one prokaryote group, while others, such as Hsp40 and Hsp70, are of mixed ancestry, with members contributed from both prokaryotic ancestors. Analysis of the yeast chaperone-substrate interaction network revealed no preference for interaction between chaperones and substrates of the same origin. Our results suggest that the archaebacterial and eubacterial protein folding pathways have been reorganized and integrated into the present eukaryotic pathway. The highly integrated chaperone system of yeast is a manifestation of the central role of chaperone-mediated folding in maintaining cellular fitness. Most likely, both archaebacterial and eubacterial chaperone systems were essential at the very early stages of eukaryogenesis, and the retention of both may have offered new opportunities for expanding the scope of chaperone-mediated folding.

A pluralistic account of homology: adapting the models to the data.

Defining homologous genes is important in many evolutionary studies but raises obvious issues. Some of these issues are conceptual and stem from our assumptions of how a gene evolves, others are practical, and depend on the algorithmic decisions implemented in existing software. Therefore, to make progress in the study of homology, both ontological and epistemological questions must be considered. In particular, defining homologous genes cannot be solely addressed under the classic assumptions of strong tree thinking, according to which genes evolve in a strictly tree-like fashion of vertical descent and divergence and the problems of homology detection are primarily methodological. Gene homology could also be considered under a different perspective where genes evolve as "public goods," subjected to various introgressive processes. In this latter case, defining homologous genes becomes a matter of designing models suited to the actual complexity of the data and how such complexity arises, rather than trying to fit genetic data to some a priori tree-like evolutionary model, a practice that inevitably results in the loss of much information. Here we show how important aspects of the problems raised by homology detection methods can be overcome when even more fundamental roots of these problems are addressed by analyzing public goods thinking evolutionary processes through which genes have frequently originated. This kind of thinking acknowledges distinct types of homologs, characterized by distinct patterns, in phylogenetic and nonphylogenetic unrooted or multirooted networks. In addition, we define "family resemblances" to include genes that are related through intermediate relatives, thereby placing notions of homology in the broader context of evolutionary relationships. We conclude by presenting some payoffs of adopting such a pluralistic account of homology and family relationship, which expands the scope of evolutionary analyses beyond the traditional, yet relatively narrow focus allowed by a strong tree-thinking view on gene evolution.

Metazoan opsin evolution reveals a simple route to animal vision.

All known visual pigments in Neuralia (Cnidaria, Ctenophora, and Bilateria) are composed of an opsin (a seven-transmembrane G protein-coupled receptor), and a light-sensitive chromophore, generally retinal. Accordingly, opsins play a key role in vision. There is no agreement on the relationships of the neuralian opsin subfamilies, and clarifying their phylogeny is key to elucidating the origin of this protein family and of vision. We used improved methods and data to resolve the opsin phylogeny and explain the evolution of animal vision. We found that the Placozoa have opsins, and that the opsins share a common ancestor with the melatonin receptors. Further to this, we found that all known neuralian opsins can be classified into the same three subfamilies into which the bilaterian opsins are classified: the ciliary (C), rhabdomeric (R), and go-coupled plus retinochrome, retinal G protein-coupled receptor (Go/RGR) opsins. Our results entail a simple scenario of opsin evolution. The first opsin originated from the duplication of the common ancestor of the melatonin and opsin genes in a eumetazoan (Placozoa plus Neuralia) ancestor, and an inference of its amino acid sequence suggests that this protein might not have been light-sensitive. Two more gene duplications in the ancestral neuralian lineage resulted in the origin of the R, C, and Go/RGR opsins. Accordingly, the first animal with at least a C, an R, and a Go/RGR opsin was a neuralian progenitor.

Evolutionary analyses of non-genealogical bonds produced by introgressive descent.

All evolutionary biologists are familiar with evolutionary units that evolve by vertical descent in a tree-like fashion in single lineages. However, many other kinds of processes contribute to evolutionary diversity. In vertical descent, the genetic material of a particular evolutionary unit is propagated by replication inside its own lineage. In what we call introgressive descent, the genetic material of a particular evolutionary unit propagates into different host structures and is replicated within these host structures. Thus, introgressive descent generates a variety of evolutionary units and leaves recognizable patterns in resemblance networks. We characterize six kinds of evolutionary units, of which five involve mosaic lineages generated by introgressive descent. To facilitate detection of these units in resemblance networks, we introduce terminology based on two notions, P3s (subgraphs of three nodes: A, B, and C) and mosaic P3s, and suggest an apparatus for systematic detection of introgressive descent. Mosaic P3s correspond to a distinct type of evolutionary bond that is orthogonal to the bonds of kinship and genealogy usually examined by evolutionary biologists. We argue that recognition of these evolutionary bonds stimulates radical rethinking of key questions in evolutionary biology (e.g., the relations among evolutionary players in very early phases of evolutionary history, the origin and emergence of novelties, and the production of new lineages). This line of research will expand the study of biological complexity beyond the usual genealogical bonds, revealing additional sources of biodiversity. It provides an important step to a more realistic pluralist treatment of evolutionary complexity.

Acquisition of 1,000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea.

Archaebacterial halophiles (Haloarchaea) are oxygen-respiring heterotrophs that derive from methanogens--strictly anaerobic, hydrogen-dependent autotrophs. Haloarchaeal genomes are known to have acquired, via lateral gene transfer (LGT), several genes from eubacteria, but it is yet unknown how many genes the Haloarchaea acquired in total and, more importantly, whether independent haloarchaeal lineages acquired their genes in parallel, or as a single acquisition at the origin of the group. Here we have studied 10 haloarchaeal and 1,143 reference genomes and have identified 1,089 haloarchaeal gene families that were acquired by a methanogenic recipient from eubacteria. The data suggest that these genes were acquired in the haloarchaeal common ancestor, not in parallel in independent haloarchaeal lineages, nor in the common ancestor of haloarchaeans and methanosarcinales. The 1,089 acquisitions include genes for catabolic carbon metabolism, membrane transporters, menaquinone biosynthesis, and complexes I-IV of the eubacterial respiratory chain that functions in the haloarchaeal membrane consisting of diphytanyl isoprene ether lipids. LGT on a massive scale transformed a strictly anaerobic, chemolithoautotrophic methanogen into the heterotrophic, oxygen-respiring, and bacteriorhodopsin-photosynthetic haloarchaeal common ancestor.

Translational selection frequently overcomes genetic drift in shaping synonymous codon usage patterns in vertebrates.

Synonymous codon usage patterns are shaped by a balance between mutation, drift, and natural selection. To date, detection of translational selection in vertebrates has proven to be a challenging task, obscured by small long-term effective population sizes in larger animals and the existence of isochores in some species. The consensus is that, in such species, natural selection is either completely ineffective at overcoming mutational pressures and genetic drift or perhaps is effective but so weak that it is not detectable. The aim of this research is to understand the interplay between mutation, selection, and genetic drift in vertebrates. We observe that although variation in mutational bias is undoubtedly the dominant force influencing codon usage, translational selection acts as a weak additional factor influencing synonymous codon usage. These observations indicate that translational selection is a widespread phenomenon in vertebrates and is not limited to a few species.