Familial versus mass selection in small populations

We used diffusion approximations and a Markov-chain approach to investigate the consequences of familial selection on the viability of small populations both in the short and in the long term. The outcome of familial selection was compared to the case of a random mating population under mass selection. In small populations, the higher effective size, associated with familial selection, resulted in higher fitness for slightly deleterious and/or highly recessive alleles. Conversely, because familial selection leads to a lower rate of directional selection, a lower fitness was observed for more detrimental genes that are not highly recessive, and with high population sizes. However, in the long term, genetic load was almost identical for both mass and familial selection for populations of up to 200 individuals. In terms of mean time to extinction, familial selection did not have any negative effect at least for small populations (N ≤ 50). Overall, familial selection could be proposed for use in management programs of small populations since it increases genetic variability and short-term viability without impairing the overall persistence times.     

Molecular evolution of a family of resistance gene analogs of nucleotide-binding site sequences in <Emphasis Type="Italic">Solanum lycopersicum</Emphasis>

Nucleotide-binding site-leucine-rich repeats (NBS-LRR) gene families are one of the major plant resistance genes. Genomic NBS evolution was studied in many plant species for diverse arrays of NBS gene families. In this study, we focused on one family of NBS sequences in an attempt to understand how closely related NBS sequences evolved in the light of selection in domesticated plant species. A phylogenetic analysis revealed five major clades (A–E) and five subclades (A1–A5) within clade A of cloned NBS sequences. Positive selection was only detected in newly evolved NBS lineages in subclades of clade A. Positively selected codon sites were found among NBS sequences of clade A. A sliding-window analysis revealed that regions with Ka/Ks ratios of >1 were in the inter-motifs when paired clades were compared, but regions with Ka/Ks ratios of >1 were found across NBS sequences when subclades of clade A were compared. Our results based on a family of closely related NBS sequences showed that positive selection was first exerted on specific lineages across all NBS sequences after selective constraints. Subsequently, sequences with mutations in commonly conserved motifs were scrutinized by purifying selection. In the long term, conserved high frequency alleles in commonly conserved motifs and changes in inter-motifs were maintained in the investigated family of NBS sequences. Moreover, codons identified to be under positive selection in the inter-motifs were mainly located in regions involved in functions of ATP binding or hydrolysis.     

Selection Response in Finite Populations

Formulae were derived to predict genetic response under various selection schemes assuming an infinitesimal model. Account was taken of genetic drift, gametic (linkage) disequilibrium (Bulmer effect), inbreeding depression, common environmental variance, and both initial segregating variance within families (σ(AW0)(2)) and mutational (σ(M)(2)) variance. The cumulative response to selection until generation t(CR(t)) can be approximated as & where N(e) is the effective population size, σ(AW &)(2) = N(e)σ(M)(2) is the genetic variance within families at the steady state (or one-half the genic variance, which is unaffected by selection), and D is the inbreeding depression per unit of inbreeding. R(0) is the selection response at generation 0 assuming preselection so that the linkage disequilibrium effect has stabilized. β is the derivative of the logarithm of the asymptotic response with respect to the logarithm of the within-family genetic variance, i.e., their relative rate of change. R(0) is the major determinant of the short term selection response, but σ(M)(2), N(e) and β are also important for the long term. A selection method of high accuracy using family information gives a small N(e) and will lead to a larger response in the short term and a smaller response in the long term, utilizing mutation less efficiently.     

Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages

The nonsynonymous (amino acid-altering) to synonymous (silent) substitution rate ratio (omega = d(N)/d(S)) provides a measure of natural selection at the protein level, with omega = 1, >1, and <1, indicating neutral evolution, purifying selection, and positive selection, respectively. Previous studies that used this measure to detect positive selection have often taken an approach of pairwise comparison, estimating substitution rates by averaging over all sites in the protein. As most amino acids in a functional protein are under structural and functional constraints and adaptive evolution probably affects only a few sites at a few time points, this approach of averaging rates over sites and over time has little power. Previously, we developed codon-based substitution models that allow the omega ratio to vary either among lineages or among sites. In this paper we extend previous models to allow the omega ratio to vary both among sites and among lineages and implement the new models in the likelihood framework. These models may be useful for identifying positive selection along prespecified lineages that affects only a few sites in the protein. We apply those branch-site models as well as previous branch- and site-specific models to three data sets: the lysozyme genes from primates, the tumor suppressor BRCA1 genes from primates, and the phytochrome (PHY) gene family in angiosperms. Positive selection is detected in the lysozyme and BRCA genes by both the new and the old models. However, only the new models detected positive selection acting on lineages after gene duplication in the PHY gene family. Additional tests on several data sets suggest that the new models may be useful in detecting positive selection after gene duplication in gene family evolution.     

High altitude adaptation in Daghestani populations from the Caucasus

We have surveyed 15 high-altitude adaptation candidate genes for signals of positive selection in North Caucasian highlanders using targeted re-sequencing. A total of 49 unrelated Daghestani from three ethnic groups (Avars, Kubachians, and Laks) living in ancient villages located at around 2,000 m above sea level were chosen as the study population. Caucasian (Adygei living at sea level, N = 20) and CEU (CEPH Utah residents with ancestry from northern and western Europe; N = 20) were used as controls. Candidate genes were compared with 20 putatively neutral control regions resequenced in the same individuals. The regions of interest were amplified by long-PCR, pooled according to individual, indexed by adding an eight-nucleotide tag, and sequenced using the Illumina GAII platform. 1,066 SNPs were called using false discovery and false negative thresholds of ~6%. The neutral regions provided an empirical null distribution to compare with the candidate genes for signals of selection. Two genes stood out. In Laks, a non-synonymous variant within HIF1A already known to be associated with improvement in oxygen metabolism was rediscovered, and in Kubachians a cluster of 13 SNPs located in a conserved intronic region within EGLN1 showing high population differentiation was found. These variants illustrate both the common pathways of adaptation to high altitude in different populations and features specific to the Daghestani populations, showing how even a mildly hypoxic environment can lead to genetic adaptation.     

The genome of the Xingu scale-backed antbird (Willisornis vidua nigrigula) reveals lineage-specific adaptations

Antbirds (Thamnophilidae) are a large neotropical family of passerine bird renowned for the ant-following foraging strategies of several members of this clade. The high diversity of antbirds provides ample opportunity for speciation studies, however these studies can be hindered by the lack of an annotated antbird reference genome. In this study, we produced a high-quality annotated reference genome for the Xingu Scale-backed Antbird (Willisornis vidua nigrigula) using 10X Genomics Chromium linked-reads technology. The assembly is 1.09 Gb, with a scaffold N50 of 12.1 Mb and 17,475 annotated protein coding genes. We compare the proteome of W. v. nigrigula to several other passerines, and produce annotations for two additional antbird genomes in order to identify genes under lineage-specific positive selection and gene families with evidence for significant expansions in antbirds. Several of these genes have functions potentially related to the lineage-specific traits of antbirds, including adaptations for thermoregulation in a humid tropical environment.     

A Chromosome-level Genome Assembly of Wild Castor Provides New Insights into its Adaptive Evolution in Tropical Desert

Wild castor grows in the high-altitude tropical desert of the African Plateau,a region known for high ultraviolet radiation,strong light,and extremely dry condition.To investigate the potential genetic basis of adaptation to both highland and tropical deserts,we generated a chromosome-level genome sequence assembly of the wild castor accession WT05,with a genome size of 316 Mb,a scaffold N50 of 31.93 Mb,and a contig N50 of 8.96 Mb,respectively.Compared with cultivated castor and other Euphorbiac...     

Codon-substitution models to detect adaptive evolution that account for heterogeneous selective pressures among site classes.

The nonsynonymous to synonymous substitution rate ratio (omega = d(N)/d(S)) provides a sensitive measure of selective pressure at the protein level, with omega values <1, =1, and >1 indicating purifying selection, neutral evolution, and diversifying selection, respectively. Maximum likelihood models of codon substitution developed recently account for variable selective pressures among amino acid sites by employing a statistical distribution for the omega ratio among sites. Those models, called random-sites models, are suitable when we do not know a priori which sites are under what kind of selective pressure. Sometimes prior information (such as the tertiary structure of the protein) might be available to partition sites in the protein into different classes, which are expected to be under different selective pressures. It is then sensible to use such information in the model. In this paper, we implement maximum likelihood models for prepartitioned data sets, which account for the heterogeneity among site partitions by using different omega parameters for the partitions. The models, referred to as fixed-sites models, are also useful for combined analysis of multiple genes from the same set of species. We apply the models to data sets of the major histocompatibility complex (MHC) class I alleles from human populations and of the abalone sperm lysin genes. Structural information is used to partition sites in MHC into two classes: those in the antigen recognition site (ARS) and those outside. Positive selection is detected in the ARS by the fixed-sites models. Similarly, sites in lysin are classified into the buried and solvent-exposed classes according to the tertiary structure, and positive selection was detected at the solvent-exposed sites. The random-sites models identified a number of sites under positive selection in each data set, confirming and elaborating the results of the fixed-sites models. The analysis demonstrates the utility of the fixed-sites models, as well as the power of previous random-sites models, which do not use the prior information to partition sites.     

Spatial pattern of MHC class II variation in the great snipe (Gallinago media)

The genes of the major histocompatibility complex (MHC) code for proteins involved in antigen recognition and triggering of the adaptive immune response, and are therefore likely to be under selection from parasites. These selection regimes may vary in space and time. Here we report a strong geographical structure in MHC class II B genes of a migrating bird, the great snipe (Gallinago media). Genetic differentiation in the MHC between two ecologically distinct distributional regions (Scandinavian mountain populations vs. East European lowland populations) was still present after statistically controlling for the effect of selectively neutral variation (microsatellites) using partial Mantel tests. This suggests a role for selection in generating this spatial structure and that it represents local adaptation to different environments. Differentiation between populations within the two regions was negligible. Overall, we found a high number of MHC alleles (50, from 175 individuals). This, together with a tendency for a higher rate of nonsynonymous than synonymous substitutions in the peptide binding sites, and high Tajima's D in certain regions of the gene, suggests a history of balancing selection. MHC variation is often thought to be maintained by some form of balancing selection, but the nature of this selection remains unclear. Our results support the hypothesis that spatial variation in selection regimes contributes to the high polymorphism.     

Effects of Partial Inbreeding on Fixation Rates and Variation of Mutant Genes

Diffusion methods were used to investigate the fixation probability, average time until fixation and extinction, and cumulative heterozygosity and genetic variance for single mutant genes in finite populations with partial inbreeding. The critical parameters in the approximation are the coefficient of inbreeding due to nonrandom mating (F) and the effective population size (Ne), which also depends on F and the variance of family size. For large Ns, the fixation probability (u) is u = 2(Ne/N)s (F + h - Fh), where N is the population census, s is the coefficient of selection of the mutant homozygote and h is the coefficient of dominance. For Poisson family size (independent Poisson distributions of selfed and nonselfed offspring with partial selfing, and independent Poisson distributions of male and female numbers with partial sib mating), Ne = N/(1 + F), and the time until fixation is approximately equal to Ne/N times the time to fixation with random mating, but this relation does not hold, however, for other distributions of family size. The cumulative nonadditive variance until fixation or loss for dominant genes is reduced with increasing F while for recessive genes it is increased with intermediate values of F. The average time until extinction of deleterious mutations is reduced by increasing F. This reduction, when expressed as a proportion, is approximately independent of the initial gene frequency as well as the selective disadvantage if this is large.     

Positive selection within sperm-egg adhesion domains of fertilin: an ADAM gene with a potential role in fertilization

Genes with a role in fertilization show a common pattern of rapid evolution. The role played by positive selection versus lack of selective constraints has been more difficult to establish. One problem arises from attempts to detect selection in an overall gene sequence analysis. I have analyzed the pattern of molecular evolution of fertilin, a gene coding for a heterodimeric sperm protein belonging to the ADAM (A disintegrin and A metalloprotease) gene family. A nonsynonymous to synonymous rate ratio (d(N)/d(S)) analysis for different protein domains of fertilin alpha and fertilin beta showed d(N)/d(S) < 1, suggesting that purifying selection has shaped fertilin's evolution. However, an analysis of the distribution of single positively selected codon sites using phylogentic analysis by maximum likelihood (PAML) showed sites within adhesion domains (disintegrin and cysteine-rich) of fertilin beta evolving under positive selection. The region 3' to the EGF-like domain of fertilin alpha, where the transmembrane and cytoplasmic tail regions are supposed to be localized, showed higher d(N) and d(S) than any other fertilin alpha region. However, it was not possible to identify positively selected codon sites due to ambiguous alignments of the carboxy-end region (ClustalX vs. DiAlign2). When this region was excluded from the PAML analysis, most single positively selected codon sites were concentrated within adhesion domains (cysteine-rich and EGF-like). The use of an ancestral sequence prior to a recent duplication event of fertilin alpha among non-Hominidae primates (Macaca, Papio, and Saguinus) revealed that the duplication is partially responsible for masking the detection of positively selected sites within the disintegrin domain. Finally, most ADAM genes with a potential role in sperm maturation and/or fertilization showed significantly higher d(N) estimates than other ADAM genes.     

Selection bias in quantitative trait loci mapping

A simulation study was performed to see whether selection affected quantitative trait loci (QTL) mapping. Populations under random selection, under selection among full-sib families, and under selection within a full-sib family were simulated each with heritability of 0.3, 0.5, and 0.7. They were analyzed with the marker spacing of 10 cM and 20 cM. The accuracy for QTL detection decreased for the populations under selection within full-sib family. Estimates of QTL effects and positions differed (P < .05) from their input values. The problems could be ignored when mapping a QTL for the populations under selection among full-sib families. A large heritability helped reduction of such problems. When the animals were selected within a full-sib family, the QTL was detected for the populations with heritability of 0.5 or larger using the marker spacing of 10 cM, and with heritability of 0.7 using the marker spacing of 20 cM. This study implied that when selection was introduced, the accuracy for QTL detection decreased and the estimates of QTL effects were biased. A caution was warranted on the decision of data (including selected animals to be genotyped) for QTL mapping.     

Differential modes of MHC class IIB gene evolution in cichlid fishes

Cichlid fishes are emblematic models for the study of adaptive radiation, driven by natural and sexual selection. Parasite mediated selection is an important component in these processes, and the evolution of their immune system therefore merits special attention. In this study, light is shed on the phylogeny of the b family of cichlid major histocompatibility complex (MHC) class IIB genes. Full-length coding sequences were used to reconstruct phylogenies using criteria of maximum parsimony, maximum likelihood and Bayesian inference. All analyses suggest monophyly of the b family of cichlid MHC class IIB genes, although sequences of the cichlid sister taxa are currently not available. Two evolutionary lineages of these genes, respectively encompassing the recently defined genomic regions DBB-DEB-DFB and DCB-DDB, show highly contrasting levels of differentiation. To explore putative causes for these differences, exon 2 sequences were screened for variation in recombination rate and strength of selection. The more diversified lineage of cichlid MHC class IIB b genes was found to have higher levels of both recombination and selection. This is consistent with the observation in other taxa that recombination facilitates the horizontal spread of positively selected sites across MHC loci and hence contributes to fast sequence evolution. In contrast, the lineage that showed low diversification might either be under stabilizing selection or is evolutionary constrained by its low recombination rate. We speculate whether this lineage might include MHC genes with non-classical functions.     

Leaf litter variation influences invasion dynamics in the invasive wetland grass Phalaris arundinacea

High litter mass is hypothesized to produce an invader-directed invasion by changing ecosystem properties such as nutrient cycling rates and light availability. An invasive plant species that stimulates litter accumulation may induce a positive feedback when it benefits from high litter conditions. Phalaris arundinacea is an invasive wetland grass that may induce positive litter feedback, as it produces abundant litter that varies in quality due to a wide range of foliar C:N content. In this study we investigated the range of growth responses within native and invasive genotypes of Phalaris that varied in initial foliar C:N levels (high C:N content was present in the invasive genotypes) when grown under varying litter mass. Overwintering with high litter reduced establishing tiller survivorship and the presence of litter delayed tiller emergence by 2 weeks. Overall, genotypes exhibited high trait plasticity in response to litter. Our results indicate that high litter mass can stimulate Phalaris growth, specifically for the genotypes with high initial C:N foliar tissue. Additionally, genotypes with initially high C:N ratios exhibited plastic responses consistent with a Master-of-some strategy indicating that their performance under high litter may depend upon the nutrient conditions under which they are grown. This study provides evidence for conditions that may lead to a positive feedback in Phalaris’ introduced range. Future studies should investigate how changing litter quantity alters nutrient cycling and competitor growth.     

Purifying selection and birth-and-death evolution in the histone H4 gene family

Histones are small basic proteins encoded by a multigene family and are responsible for the nucleosomal organization of chromatin in eukaryotes. Because of the high degree of protein sequence conservation, it is generally believed that histone genes are subject to concerted evolution. However, purifying selection can also generate a high degree of sequence homogeneity. In this study, we examined the long-term evolution of histone H4 genes to determine whether concerted evolution or purifying selection was the major factor for maintaining sequence homogeneity. We analyzed the proportion (p(S)) of synonymous nucleotide differences between the H4 genes from 59 species of fungi, plants, animals, and protists and found that p(S) is generally very high and often close to the saturation level (p(S) ranging from 0.3 to 0.6) even though protein sequences are virtually identical for all H4 genes. A small proportion of genes showed a low level of p(S) values, but this appeared to be caused by recent gene duplication. Our findings suggest that the members of this gene family evolve according to the birth-and-death model of evolution under strong purifying selection. Using histone-like genes in archaebacteria as outgroups, we also showed that H1, H2A, H2B, H3, and H4 histone genes in eukaryotes form separate clusters and that these classes of genes diverged nearly at the same time, before the eukaryotic kingdoms diverged.     

Accuracy and power of bayes prediction of amino acid sites under positive selection

Bayes prediction quantifies uncertainty by assigning posterior probabilities. It was used to identify amino acids in a protein under recurrent diversifying selection indicated by higher nonsynonymous (d(N)) than synonymous (d(S)) substitution rates or by omega = d(N)/d(S) > 1. Parameters were estimated by maximum likelihood under a codon substitution model that assumed several classes of sites with different omega ratios. The Bayes theorem was used to calculate the posterior probabilities of each site falling into these site classes. Here, we evaluate the performance of Bayes prediction of amino acids under positive selection by computer simulation. We measured the accuracy by the proportion of predicted sites that were truly under selection and the power by the proportion of true positively selected sites that were predicted by the method. The accuracy was slightly better for longer sequences, whereas the power was largely unaffected by the increase in sequence length. Both accuracy and power were higher for medium or highly diverged sequences than for similar sequences. We found that accuracy and power were unacceptably low when data contained only a few highly similar sequences. However, sampling a large number of lineages improved the performance substantially. Even for very similar sequences, accuracy and power can be high if over 100 taxa are used in the analysis. We make the following recommendations: (1) prediction of positive selection sites is not feasible for a few closely related sequences; (2) using a large number of lineages is the best way to improve the accuracy and power of the prediction; and (3) multiple models of heterogeneous selective pressures among sites should be applied in real data analysis.     

Parallel selection on gene copy number variations through evolution of three-spined stickleback genomes

Background

Understanding the genetic basis of adaptive evolution is one of the major goals in evolutionary biology. Recently, it has been revealed that gene copy number variations (GCNVs) constitute significant proportions of genomic diversities within natural populations. However, it has been unclear whether GCNVs are under positive selection and contribute to adaptive evolution. Parallel evolution refers to adaptive evolution of the same trait in related but independent lineages, and three-spined stickleback (Gasterosteus aculeatus) is a well-known model organism. Through identification of genetic variations under parallel selection, i.e., variations shared among related but independent lineages, evidence of positive selection is obtained. In this study, we investigated whole-genome resequencing data from the marine and freshwater groups of three-spined sticklebacks from diverse areas along the Pacific and Atlantic Ocean coastlines, and searched for GCNVs under parallel selection.

Results

We identified 24 GCNVs that showed significant differences in the numbers of mapped reads between the two groups, and this number was significantly larger than that expected by chance. The derived group, i.e., freshwater group, was typically characterized by larger gene-copy numbers, which implied that gene duplications or multiplications helped with adaptation to the freshwater environment. Some of the identified GCNVs were those of multigenic family genes, which is consistent with the theory that fatal effects due to copy-number changes of multigenic family genes tend to be less than those of single-copy genes.

Conclusion

The identification of GCNVs that were likely under parallel selection suggests that contribution of GCNVs should be considered in studies on adaptive evolution.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-735) contains supplementary material, which is available to authorized users.     

Genomic regions involved in response to grain yield selection at high and low nitrogen fertilization in maize

In order to validate the role of genomic regions involved in nitrogen use efficiency and detected in a population of recombinant inbred lines (RIL), we have applied from the same population a recurrent selection for adaptation to low N-input (N0) and to high N-input (N1). Variation of allele frequency at neutral marker during the two cycles of recurrent selection may provide information about markers linked to QTLs. Significant temporal variation of allele frequency was investigated using the test of Waples, which tests the hypothesis of genetic drift versus selection. Most genomic regions (12/19) responding to selection were detected for selection at high N-input and only two were common to selection at high and low N-inputs. This was consistent with the greater grain yield response to selection observed for the population selected under high N-input compared with the population selected under low N-input, when they were evaluated at high N-fertilization. In contrast, when they were evaluated at low N-input both types of selection gave similar yield. As was expected, in the first cycle we observed selection of markers linked to grain yield QTLs. In the course of the second cycle three situations were observed: the confirmation of most regions already selected in C1 including all C1 regions overlapping with grain yield QTLs; the non-confirmation of some C1 regions (2/9); and the identification of new genomic zones (10/17). The detected marker–QTL associations revealed the consistency of the involvement of some traits, such as root architecture and glutamine synthetase activity, which would be of major importance for grain yield setting whatever the nitrogen fertilization.