BMC Evolutionary Biology - Latest articles

Signatures of selection in natural populations adapted to chronic pollution

Larissa M Williams and Marjorie F Oleksiak — 2008-10-10

Background: Populations of the teleost fish Fundulus heteroclitus appear to flourish in heavily polluted and geographically separated Superfund sites. Populations from three Superfund sites (New Bedford Harbor, MA, Newark Bay, NJ, and Elizabeth River, VA) have independently evolved adaptive resistance to chemical pollutants. In these polluted populations, natural selection likely has altered allele frequencies of loci that affect fitness or that are linked to these loci. The aim of this study was to identify loci that exhibit non-neutral behavior in the F. heteroclitus genome in polluted populations versus clean reference populations. Results: To detect signatures of natural selection and thus identify genetic bases for adaptation to anthropogenic stressors, we examined allele frequencies for many hundreds of amplified fragment length polymorphism markers among populations of F. heteroclitus. Specifically, we contrasted populations from three Superfund sites (New Bedford Harbor, MA, Newark Bay, NJ, and Elizabeth River, VA) to clean reference populations flanking the polluted sites. When empirical FST values were compared to a simulated distribution of FST values, 24 distinct outlier loci were identified among pairwise comparisons of pollutant impacted F. heteroclitus populations and both surrounding reference populations. Upon removal of all outlier loci, there was a strong correlation (R2 = 0.79, p < 0.0001) between genetic and geographical distance. This apparently neutral evolutionary pattern was not evident when outlier loci were included (R2 = 0.092, p = 0.0721). Two outlier loci were shared between New Bedford Harbor and Elizabeth River populations, and two different loci were shared between Newark Bay and Elizabeth River populations. Conclusion: In total, 1% to 6% of loci are implicated as being under selection or linked to areas of the genome under selection in three F. heteroclitus populations that reside in polluted estuaries. Shared loci among polluted sites indicate that selection may be acting on multiple loci involved in adaptation, and loci shared between polluted sites potentially are involved in a generalized adaptive response.

Genetic hitchhiking can promote the initial spread of strong altruism

Mauro Santos and Eors Szathmary — 2008-10-10

Background: The evolutionary origin of strong altruism (where the altruist pays an absolute cost in terms of fitness) towards non-kin has never been satisfactorily explained since no mechanism (except genetic drift) seems to be able to overcome the fitness disadvantage of the individual who practiced altruism in the first place. Results: Here we consider a multilocus, single-generation random group model and demonstrate that with low, but realistic levels of recombination and social heterosis (selecting for allelic diversity within groups) altruism can evolve without invoking kin selection, because sampling effects in the formation of temporary groups and selection for complementary haplotypes generate nonrandom associations between alleles at polymorphic loci. Conclusion: By letting altruism get off the ground, selection on other genes favourably interferes with the eventual fate of the altruistic trait due to genetic hitchhiking.

Unique genes in plants: specificities and conserved features throughout evolution

David Armisen, Alain Lecharny and Sebastien Aubourg — 2008-10-10

Background: Plant genomes contain a high proportion of duplicated genes as a result of numerous whole, segmental and local duplications. These duplications lead up to the formation of gene families, which are the usual material for many evolutionary studies. However, all characterized genomes include single-copy (unique) genes that have not received much attention. Unlike gene duplication, gene loss is not an unspecific mechanism but is rather influenced by a functional selection. In this context, we have established and used stringent criteria in order to identify suitable sets of unique genes present in plant proteomes. Comparisons of unique genes in the green phylum were used to characterize the gene and protein features exhibited by both conserved and species-specific unique genes. Results: We identified the unique genes within both A. thaliana and O. sativa genomes and classified them according to the number of homologs in the alternative species: none (U{1:0}), one (U{1:1}) or several (U{1:m}). Regardless of the species, all the genes in these groups present some conserved characteristics, such as small average protein size and abnormal intron number. In order to understand the origin and function of unique genes, we further characterized the U{1:1} gene pairs. The possible involvement of sequence convergence in the creation of U{1:1} pairs was discarded due to the frequent conservation of intron positions. Furthermore, an orthology relationship between the two members of each U{1:1} pair was strongly supported by a high conservation in the protein sizes and transcription levels. Within the promoter of the unique conserved genes, we found a number of TATA and TELO boxes that specifically differed from their mean number in the whole genome. Many unique genes have been conserved as unique through evolution from the green alga Ostreococcus lucimarinus to higher plants. Plant unique genes may also have homologs in bacteria and we showed a link between the targeting towards plastids of proteins encoded by plant nuclear unique genes and their homology with a bacterial protein. Conclusions: Many of the A. thaliana and O. sativa unique genes are conserved in plants for which the ancestor diverged at least 725 million years ago (MYA). Half of these genes are also present in other eukaryotic and/or prokaryotic species. Thus, our results indicate that (i) a strong negative selection pressure has conserved a number of genes as unique in genomes throughout evolution, (ii) most unique genes are subjected to a low divergence rate, (iii) they have some features observed in housekeeping genes but for most of them there is no functional annotation and (iv) they may have an ancient origin involving a possible gene transfer from ancestral chloroplasts or bacteria to the plant nucleus.

The Caenorhabditis globin gene family reveals extensive nematode-specific radiation and diversification

2008-10-09

Background: Globin isoforms with variant properties and functions have been found in the pseudocoel, body wall and cuticle of various nematode species and even in the eyespots of the insect-parasite Mermis nigrescens. In fact, much higher levels of complexity exist, as shown by recent whole genome analysis studies. In silico analysis of the genome of Caenorhabditis elegans revealed an unexpectedly high number of globin genes featuring a remarkable diversity in gene structure, amino acid sequence and expression profiles. Results: In the present study we have analyzed whole genomic data from C. briggsae, C. remanei, Pristionchus pacificus and Brugia malayi and EST data from several other nematode species to study the evolutionary history of the nematode globin gene family. We find a high level of conservation of the C. elegans globin complement, with even distantly related nematodes harboring orthologs to many Caenorhabditis globins. Bayesian phylogenetic analysis resolves all nematode globins into two distinct globin classes. Analysis of the globin intron-exon structures suggests extensive loss of ancestral introns and gain of new positions in deep nematode ancestors, and mainly loss in the Caenorhabditis lineage. We also show that the Caenorhabditis globin genes are expressed in distinct, mostly non-overlapping, sets of cells and that they are all under strong purifying selection. Conclusion: Our results enable reconstruction of the evolutionary history of the globin gene family in the nematode phylum. A duplication of an ancestral globin gene occurred before the divergence of the Platyhelminthes and the Nematoda and one of the duplicated genes radiated further in the nematode phylum before the split of the Spirurina and Rhabditina and was followed by further radiation in the lineage leading to Caenorhabditis. The resulting globin genes were subject to processes of subfunctionalization and diversification leading to cell-specific expression patterns. Strong purifying selection subsequently dampened further evolution and facilitated fixation of the duplicated genes in the genome.

The IGS-ETS in Bacillus (Insecta Phasmida): molecular characterization and the relevance of sex in ribosomal DNA evolution.

Andrea Ricci, Valerio Scali and Marco Passamonti — 2008-10-09

Background: DNA encoding for ribosomal RNA (rDNA) is arranged in tandemly-repeated subunits, each containing ribosomal genes and non-coding spacers. Because tandemly-repeated, rDNA evolves under a balanced influence of selection and "concerted evolution", which homogenizes rDNA variants over the genome (through genomic turnover mechanisms) and the population (through sexuality). Results: In this paper we analyzed the IGS-ETS of the automictic parthenogen Bacillus atticus and the bisexual B. grandii, two closely related stick-insect species. Both species share the same IGS-ETS structure and sequence, including a peculiar head-to-tail array of putative transcription enhancers, here named Bag530. Sequence variability of both IGS-ETS and Bag530 evidenced a neat geographic and subspecific clustering in B. grandii, while B. atticus shows a little but evident geographic structure. This was an unexpected result, since the parthenogen B. atticus should lack sequence fixation through sexuality. In B. atticus a new variant might spread in a given geographic area through colonization by an all-female clone, but we cannot discard the hypothesis that B. atticus was actually a bisexual taxon in that area at the time the new variant appeared. Moreover, a gene conversion event between two Bag530 variants of B. grandii benazzii and B. grandii maretimi suggested that rRNA might evolve according to the so-called "library hypothesis" model, through differential amplification of rDNA variants in different taxa. Conclusions: On the whole, Bacillus rDNA evolution appears to be under a complex array of interacting mechanisms: homogenization may be achieved through genomic turnover that stabilizes DNA-binding protein interactions but, simultaneously, new sequence variants can be adopted, either by direct appearance of newly mutated repeats, or by competition among repeats, so that both DNA-binding proteins and repeat variants drive each other's evolution. All this, coupled with chromosome reshuffling due to sexuality (when present), might drive a quick fixation of new rDNA variants in the populations.

Lineage specific recombination rates and microevolution in Listeria monocytogenes

2008-10-08

Background: The bacterium Listeria monocytogenes is a saprotroph as well as an opportunistic human foodborne pathogen, which has previously been shown to consist of at least two widespread lineages (termed lineages I and II) and a uncommon lineage (lineage III). While some L. monocytogenes strains show evidence for considerable diversification by homologous recombination, our understanding of the contribution of recombination to L. monocytogenes evolution is still limited. We therefore used STRUCTURE and ClonalFrame, two programs that model the effect of recombination, to make inferences about the population structure and different aspects of the recombination process in L. monocytogenes. Analyses were performed using sequences for seven loci (including the house-keeping genes gap, prs, purM and ribC, the stress response gene sigB, and the virulence genes actA and inlA) for 195 L. monocytogenes isolates. Results: Sequence analyses with ClonalFrame and the Sawyer's test showed that recombination is more prevalent in lineage II than lineage I and is most frequent in two house-keeping genes (ribC and purM) and the two virulence genes (actA and inlA). The relative occurrence of recombination versus point mutation is about six times higher in lineage II than in lineage I, which causes a higher genetic variability in lineage II. Unlike lineage I, lineage II represents a genetically heterogeneous population with a relatively high proportion (30% average) of genetic material imported from external sources. Phylograms, constructed with correcting for recombination, as well as Tajima's D data suggest that both lineages I and II have suffered a population bottleneck. Conclusions: Our study shows that evolutionary lineages within a single bacterial species can differ considerably in the relative contributions of recombination to genetic diversification. Accounting for recombination in phylogenetic studies is critical, and new evolutionary models that account for the possibility of changes in the rate of recombination would be required. While previous studies suggested that only L. monocytogenes lineage I has experienced a recent bottleneck, our analyses clearly show that lineage II experienced a bottleneck at about the same time, which was subsequently obscured by abundant homologous recombination after the lineage II bottleneck. While lineage I and lineage II should be considered separate species from an evolutionary viewpoint, maintaining single species name may be warranted since both lineages cause the same type of human disease.

Relationships of Gag-pol Diversity between Ty3/Gypsy and Retroviridae LTR retroelements and the three kings hypothesis

Carlos Llorens, Mario A Fares and Andres Moya — 2008-10-08

Background: The origin of vertebrate retroviruses (Retroviridae) is yet to be thoroughly investigated, but due to their similarity and identical gag-pol (and env) genome structure, it is accepted that they evolve from Ty3/Gypsy LTR retroelements the retrotransposons and retroviruses of plants, fungi and animals. These 2 groups of LTR retroelements code for 3 proteins rarely studied due to the high variability - gag polyprotein, protease and GPY/F module. In relation to 3 previously proposed Retroviridae classes I, II and II, investigation of the above proteins conclusively uncovers important insights regarding the ancient history of Ty3/Gypsy and Retroviridae LTR retroelements. Results: We performed a comprehensive study of 120 non-redundant Ty3/Gypsy and Retroviridae LTR retroelements. Phylogenetic reconstruction inferred based on the concatenated analysis of the gag and pol polyproteins shows a robust phylogenetic signal regarding the clustering of OTUs. Evaluation of gag and pol polyproteins separately yields discordant information. While pol signal supports the traditional perspective (2 monophyletic groups), gag polyprotein describes an alternative scenario where each Retroviridae class can be distantly related with one or more Ty3/Gypsy lineages. We investigated more in depth this evidence through comparative analyses performed based on the gag polyprotein, the protease and the GPY/F module. Our results indicate that contrary to the traditional monophyletic view of the origin of vertebrate retroviruses, the Retroviridae class I is a molecular fossil, preserving features that were probably predominant among Ty3/Gypsy ancestors predating the split of plants, fungi and animals. In contrast, classes II and III maintain other phenotypes that emerged more recently during Ty3/Gypsy evolution. Conclusions: The 3 Retroviridae classes I, II and III exhibit phenotypic differences that delineate a network never before reported between Ty3/Gypsy and Retroviridae LTR retroelements. This new scenario reveals how the diversity of vertebrate retroviruses is polyphyletically recurrent into the Ty3/Gypsy evolution, i.e. older than previously thought. The simplest hypothesis to explain this finding is that classes I, II and III trace back to at least 3 Ty3/Gypsy ancestors that emerged at different evolutionary times prior to protostomes-deuterostomes divergence. We have called this "the three kings hypothesis" concerning the origin of vertebrate retroviruses.

Patterns of evolutionary constraints on genes in humans

Subhajyoti De, Nuria Lopez-Bigas and Sarah A Teichmann — 2008-10-07

Background: Different regions in a genome evolve at different rates depending on structural and functional constraints. Some genomic regions are highly conserved during metazoan evolution, while other regions may evolve rapidly, either in all species or in a lineage-specific manner. A strong or even moderate change in constraints in functional regions, for example in coding regions, can have significant evolutionary consequences. Results: Here we discuss a novel framework, `BaseDiver', to classify groups of genes in humans based on the patterns of evolutionary constraints on polymorphic positions in their coding regions. Comparing the nucleotide-level divergence among mammals with the extent of deviation from the ancestral base in the human lineage, we identify patterns of evolutionary pressure on nonsynonymous base-positions in groups of genes belonging to the same functional category. Focusing on groups of genes in functional categories, we find that transcription factors contain a significant excess of nonsynonymous base-positions that are conserved in other mammals but changed in human, while immunity related genes harbour mutations at base-positions that evolve rapidly in all mammals including humans due to strong preference for advantageous alleles. Genes involved in olfaction also evolve rapidly in all mammals, and in humans this appears to be due to weak negative selection. Conclusion: While recent studies have identified genes under positive selection in humans, our approach identifies evolutionary constraints on Gene Ontology groups identifying changes in humans relative to some of the other mammals.

The evolution of TEP1, an exceptionally polymorphic immunity gene in Anopheles gambiae

2008-10-07

Background: Host-parasite coevolution can result in balancing selection, which maintains genetic variation in the susceptibility of hosts to parasites. It has been suggested that variation in a thioester-containing protein called TEP1 (AGAP010815) may alter the ability of Anopheles mosquitoes to transmit Plasmodium parasites, and high divergence between alleles of this gene suggests the possible action of long-term balancing selection. We studied whether TEP1 is a case of an ancient balanced polymorphism in an animal immune system. Results: We found evidence that the high divergence between TEP1 alleles is the product of genetic exchange between TEP1 and other TEP loci, i.e. gene conversion. Additionally, some TEP1 alleles showed unexpectedly low variability. Conclusion: The TEP1 gene appears to be a chimera produced from at least two other TEP loci, and the divergence between TEP1 alleles is probably not caused by long-term balancing selection, but is instead due to two independent gene conversion events from one of these other genes. Nevertheless, TEP1 still shows evidence of natural selection, in particular there appears to have been recent changes in the frequency of alleles that has diminished polymorphism within each allelic class. Although the selective force driving this dynamic was not identified, given that susceptibility to Plasmodium parasites is known to be associated with allelic variation in TEP1, these changes in allele frequencies could alter the vectoring capacity of populations.

The Role of Positive Selection in Determining the Molecular Cause of Species Differences in Disease

2008-10-06

Background: Related species, such as humans and chimpanzees, often experience the same disease with varying degrees of pathology, as seen in the cases of Alzheimer's disease, or differing symptomatology as in AIDS. Furthermore, certain diseases such as schizophrenia, epithelial cancers and autoimmune disorders are far more frequent in humans than in other species for reasons not associated with lifestyle. Genes that have undergone positive selection during species evolution are indicative of functional adaptations that drive species differences. Thus we investigate whether biomedical disease differences between species can be attributed to positively selected genes. Results: We identified genes that putatively underwent positive selection during the evolution of humans and four mammals which are often used to model human diseases (mouse, rat, chimpanzee and dog). We show that genes predicted to have been subject to positive selection pressure during human evolution are implicated in diseases such as epithelial cancers, schizophrenia, autoimmune diseases and Alzheimer's disease, all of which differ in prevalence and symptomatology between humans and their mammalian relatives. In agreement with previous studies, the chimpanzee lineage was found to have more genes under positive selection than any of the other lineages. In addition, we found new evidence to support the hypothesis that genes that have undergone positive selection tend to interact with each other. This is the first such evidence to be detected widely among mammalian genes and may be important in identifying molecular pathways causative of species differences. Conclusions: Our dataset of genes predicted to have been subject to positive selection in five species serves as an informative resource that can be consulted prior to selecting appropriate animal models during drug target validation. We conclude that studying the evolution of functional and biomedical disease differences between species is an important way to gain insight into their molecular causes and may provide a method to predict when animal models do not mirror human biology.