Connecting genomic patterns of local adaptation and niche suitability in teosintes.

The central abundance hypothesis predicts that local adaptation is a function of the distance to the centre of a species' geographic range. To test this hypothesis, we gathered genomic diversity data from 49 populations, 646 individuals and 33,464 SNPs of two wild relatives of maize, the teosintes Zea mays ssp. parviglumis and Zea. mays. ssp. mexicana. We examined the association between the distance to their climatic and geographic centroids and the enrichment of SNPs bearing signals of adaptation. We identified candidate adaptive SNPs in each population by combining neutrality tests and cline analyses. By applying linear regression models, we found that the number of candidate SNPs is positively associated with niche suitability, while genetic diversity is reduced at the limits of the geographic distribution. Our results suggest that overall, populations located at the limit of the species' niches are adapting locally. We argue that local adaptation to this limit could initiate ecological speciation processes and facilitate adaptation to global change.

Statistical detection of chromosomal homology using shared-gene density alone.

MOTIVATION: Over evolutionary time, various processes including point mutations and insertions, deletions and inversions of variable sized segments progressively degrade the homology of duplicated chromosomal regions making identification of the homologous regions correspondingly difficult. Existing algorithms that attempt to detect homology are based on shared-gene density and colinearity and possibly also strand information. RESULTS: Here, we develop a new algorithm for the statistical detection of chromosomal homology, CloseUp, which uses shared-gene density alone to fully exploit the observation that relaxing colinearity requirements in general is beneficial for homology detection and at the same time optimizes computation time. CloseUp has two components: the identification of candidate homologous regions followed by their statistical evaluation using Monte Carlo methods and data randomization. Using both artificial and real data, we compared CloseUp with two existing programs (ADHoRe and LineUp) for chromosomal homology detection and found that in general CloseUp compares favorably. AVAILABILITY: CloseUp and supplementary information are available at http://www.igb.uci.edu/servers/cgss.html CONTACT: pfbaldi@ics.uci.edu.

Molecular evolution of the wound-induced serine protease inhibitor wip1 in Zea and related genera.

Plant defense mechanisms have been the subject of intensive investigation. However, little is known about their long-term evolutionary dynamics. We investigated the molecular diversity of a wound-induced serine protease inhibitor, wip1, in the genus Zea, as well as the divergence of wip1 among four genera, Zea, Tripsacum, Sorghum, and Oryza, in order to gain insight into the long-term evolution of plant defense. The specific objectives of this study were to determine (1) whether wip1 has a history of positive or balancing selection, as has been shown for genes involved in plant defense against pathogens, and (2) if the evolutionary histories of wip1 inhibitory loops, which come into closest contact with proteases, differ from the evolutionary history of other parts of this gene. The Zea polymorphism data are consistent with a neutral evolutionary history. In contrast, relative-rate tests suggest a nonneutral evolutionary history. This inconsistency may indicate that selection acting on wip1 is episodic or that wip1 evolves in response to selection favoring novel alleles. We also detected significant heterogeneity in the evolutionary rates of the two inhibitory loops of wip1-one inhibitory loop is highly conserved, whereas the second has diverged rapidly. Because these two inhibitory loops are predicted to have very similar biochemical functions, the significantly different evolutionary histories suggest that these loops have different ecological functions.

Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.).

We measured sequence diversity in 21 loci distributed along chromosome 1 of maize (Zea mays ssp. mays L.). For each locus, we sequenced a common sample of 25 individuals representing 16 exotic landraces and nine U.S. inbred lines. The data indicated that maize has an average of one single nucleotide polymorphism (SNP) every 104 bp between two randomly sampled sequences, a level of diversity higher than that of either humans or Drosophila melanogaster. A comparison of genetic diversity between the landrace and inbred samples showed that inbreds retained 77% of the level of diversity of landraces, on average. In addition, Tajima's D values suggest that the frequency distribution of polymorphisms in inbreds was skewed toward fewer rare variants. Tests for selection were applied to all loci, and deviations from neutrality were detected in three loci. Sequence diversity was heterogeneous among loci, but there was no pattern of diversity along the genetic map of chromosome 1. Nonetheless, diversity was correlated (r = 0.65) with sequence-based estimates of the recombination rate. Recombination in our sample was sufficient to break down linkage disequilibrium among SNPs. Intragenic linkage disequilibrium declines within 100-200 bp on average, suggesting that genome-wide surveys for association analyses require SNPs every 100-200 bp.

Sequence diversity in the tetraploid Zea perennis and the closely related diploid Z. diploperennis: insights from four nuclear loci.

Polyploidy has been an extremely common phenomenon in the evolutionary history of angiosperms. Despite this there are few data available to evaluate the effects of polyploidy on genetic diversity and to compare the relative effects of drift and selection in polyploids and related diploids. We investigated DNA sequence diversity at four nuclear loci (adh1, glb1, c1, and waxy) from the tetraploid Zea perennis and the closely related diploid Z. diploperennis. Contrary to expectations, we detected no strong evidence for greater genetic diversity in the tetraploid, or for consistent differences in the effects of either drift or selection between the tetraploid and the diploid. Our failure to find greater genetic diversity in Z. perennis may result from its relatively recent origin or demographic factors associated with its origin. In addition to comparing genetic diversity in the two species, we constructed genealogies to infer the evolutionary origin of Z. perennis. Although these genealogies are equivocal regarding the mode of origin, several aspects of these genealogies support an autotetraploid origin. Consistent with previous molecular data the genealogies do not, however, support the division of Zea into two sections, the section Zea and the section Luxuriantes.

A survey of the molecular evolutionary dynamics of twenty-five multigene families from four grass taxa.

We surveyed the molecular evolutionary characteristics of 25 plant gene families, with the goal of better understanding general processes in plant gene family evolution. The survey was based on 247 GenBank sequences representing four grass species (maize, rice, wheat, and barley). For each gene family, orthology and paralogy relationships were uncertain. Recognizing this uncertainty, we characterized the molecular evolution of each gene family in four ways. First, we calculated the ratio of nonsynonymous to synonymous substitutions (d(N)/d(S)) both on branches of gene phylogenies and across codons. Our results indicated that the d(N)/d(S) ratio was statistically heterogeneous across branches in 17 of 25 (68%) gene families. The vast majority of d(N)/d(S) estimates were <<1.0, suggestive of selective constraint on amino acid replacements, and no estimates were >1.0, either across phylogenetic lineages or across codons. Second, we tested separately for nonsynonymous and synonymous molecular clocks. Sixty-eight percent of gene families rejected a nonsynonymous molecular clock, and 52% of gene families rejected a synonymous molecular clock. Thus, most gene families in this study deviated from clock-like evolution at either synonymous or nonsynonymous sites. Third, we calculated the effective number of codons and the proportion of G+C synonymous sites for each sequence in each gene family. One or both quantities vary significantly within 18 of 25 gene families. Finally, we tested for gene conversion, and only six gene families provided evidence of gene conversion events. Altogether, evolution for these 25 gene families is marked by selective constraint that varies among gene family members, a lack of molecular clock at both synonymous and nonsynonymous sites, and substantial variation in codon usage.

The interaction of protein structure, selection, and recombination on the evolution of the type-1 fimbrial major subunit (fimA) from Escherichia coli.

Fimbrial adhesins allow bacteria to interact with and attach to their environment. The bacteria possibly benefit from these interactions, but all external structures including adhesins also allow bacteria to be identified by other organisms. Thus adhesion molecules might be under multiple forms of selection including selection to constrain functional interactions or evolve novel epitopes to avoid recognition. We address these issues by studying genetic diversity in the Escherichia coli type-1 fimbrial major subunit, fimA. Overall, sequence diversity in fimA is high (pi = 0.07) relative to that in other E. coli genes. High diversity is a function of positive diversifying selection, as detected by d(N)/d(S) ratios higher than 1.0, and amino acid residuces subject to diversifying selection are nonrandomly clustered on the exterior surface of the peptide. In addition, McDonald and Kreitman tests suggest that there has been historical but not current directional selection at fimA between E. coli and Salmonella. Finally, some regions of the fimA peptide appear to be under strong structural constraint within E. coli, particularly the interior regions of the molecule that is involved in subunit to subunit interaction. Recombination also plays a major role contributing to E. coli fimA allelic variation and estimates of recombination (2N(e)c) and mutation (2N(e)mu) are about the same. Recombination may act to separate the diverse evolutionary forces in different regions of the fimA peptide.

Patterns of chromosomal duplication in maize and their implications for comparative maps of the grasses.

The maize genome contains extensive chromosomal duplications that probably were produced by an ancient tetraploid event. Comparative cereal maps have identified at least 10 duplicated, or homologous, chromosomal regions within maize. However, the methods used to document chromosomal homologies from comparative maps are not statistical, and their criteria are often unclear. This paper describes the development of a simulation method to test for the statistical significance of marker colinearity between chromosomes, and the application of the method to a molecular map of maize. The method documents colinearity among 24 pairs of maize chromosomes, suggesting homology in maize is more complex than represented by comparative cereal maps. The results also reveal that 60%-82% of the genome has been retained in colinear regions and that as much as a third of the genome could be present in multiple copies. Altogether, the complex pattern of colinearity among maize chromosomes suggests that current comparative cereal maps do not adequately represent the evolution and organization of the maize genome.

Maize as a model for the evolution of plant nuclear genomes.

The maize genome is replete with chromosomal duplications and repetitive DNA. The duplications resulted from an ancient polyploid event that occurred over 11 million years ago. Based on DNA sequence data, the polyploid event occurred after the divergence between sorghum and maize, and hence the polyploid event explains some of the difference in DNA content between these two species. Genomic rearrangement and diploidization followed the polyploid event. Most of the repetitive DNA in the maize genome is retrotransposable elements, and they comprise 50% of the genome. Retrotransposon multiplication has been relatively recent-within the last 5-6 million years-suggesting that the proliferation of retrotransposons has also contributed to differences in DNA content between sorghum and maize. There are still unanswered questions about repetitive DNA, including the distribution of repetitive DNA throughout the genome, the relative impacts of retrotransposons and chromosomal duplication in plant genome evolution, and the hypothesized correlation of duplication events with transposition. Population genetic processes also affect the evolution of genomes. We discuss how centromeric genes should, in theory, contain less genetic diversity than noncentromeric genes. In addition, studies of diversity in the wild relatives of maize indicate that different genes have different histories and also show that domestication and intensive breeding have had heterogeneous effects on genetic diversity across genes.

Evolution of genes and taxa: a primer.

The rapidly growing fields of molecular evolution and systematics have much to offer to molecular biology, but like any field have their own repertoire of terms and concepts. Homology, for example, is a central theme in evolutionary biology whose definition is complex and often controversial. Homology extends to multigene families, where the distinction between orthology and paralogy is key. Nucleotide sequence alignment is also a homology issue, and is a key stage in any evolutionary analysis of sequence data. Models based on our understanding of the processes of nucleotide substitution are used both in the estimation of the number of evolutionary changes between aligned sequences and in phylogeny reconstruction from sequence data. The three common methods of phylogeny reconstruction--parsimony, distance and maximum likelihood--differ in their use of these models. All three face similar problems in finding optimal--and reliable--solutions among the vast number of possible trees. Moreover, even optimal trees for a given gene may not reflect the relationships of the organisms from which the gene was sampled. Knowledge of how genes evolve and at what rate is critical for understanding gene function across species or within gene families. The Neutral Theory of Molecular Evolution serves as the null model of molecular evolution and plays a central role in data analysis. Three areas in which the Neutral Theory plays a vital role are: interpreting ratios of nonsynonymous to synonymous nucleotide substitutions, assessing the reliability of molecular clocks, and providing a foundation for molecular population genetics.

Neutral and nonneutral mitochondrial genetic variation in deep-sea clams from the family vesicomyidae.

Nucleotide sequences at two mitochondrial genes from 57 individuals representing eight species of deep-sea clams (Vesicomyidae) were examined for variation consistent with the neutral model of molecular evolution. One gene, cytochrome oxidase subunit I (COI), deviated from the expectations of neutrality by containing an excess of intraspecific nonsynonymous polymorphism. Additionally, one species, Calyptogena kilmeri, showed a significant excess of rare polymorphism specifically at the COI locus. In contrast, a second mitochondrial gene, the large-subunit 16S ribosomal RNA gene (16S), showed little deviation from neutrality either between or within species. Together, COI and 16S show no deviation from neutral expectations by the HKA test, produce congruent phylogenetic relationships between species, and show correlated numbers of fixed differences between species and polymorphism within species. These patterns of both neutral and nonneutral evolution within the mitochondrial genome are most consistent with a model where intraspecific nonsynonymous polymorphism at COI is near neutrality. In addition to examining the forces of molecular evolution, we extend hypotheses about interspecific relationships within this family for geographical locations previously unexamined by molecular methods including habitats near the Middle Atlantic, the Aleutian Trench, and Costa Rica.

Patterns of genetic diversification within the Adh gene family in the grasses (Poaceae).

We investigated the evolutionary dynamics of the Adh gene family within the grasses (Poaceae), with the goal of using molecular evolutionary tools to understand the process of gene family diversification. We analyzed 21 Adh sequences representing a broad array of grasses. Phylogenetic analyses suggested that Adh duplicated into Adh1 and Adh2 before the radiation of the grasses roughly 65 MYA. Gene structure, including intron length, has varied little over this period. Conservation of intron length prompted investigation into the dynamics of intron evolution, particularly the ability of intron sequences to form secondary structures. Intron sequences did not have an extremely high or low minimum free energy of folding relative to permuted sequences, suggesting that individual Adh introns do not evolve under secondary structural constraints. For coding sequences, the diversification of Adh1 and Adh2 was marked by a shift in third-position G + C content. This shift may reflect differential selection for codon use. Diversification between Adh1 and Adh2 was also typified by a shift in nonsynonymous nucleotide substitution rates, but there was no evidence that relatively fast nonsynonymous nucleotide substitution rates in the Adh2 clade were a product of diversifying selection. Gene conversion may have played a role in retarding diversification of Adh1 and Adh2 in rice, but there is no evidence of gene conversion between paralogs in other taxa. Although the reasons for retention of two functional Adh genes remain obscure, we propose that a shift in gene expression was important for the retention of the two Adh gene copies within the grasses.

Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection.

Disease resistance genes in plants are often found in complex multigene families. The largest known cluster of disease resistance specificities in lettuce contains the RGC2 family of genes. We compared the sequences of nine full-length genomic copies of RGC2 representing the diversity in the cluster to determine the structure of genes within this family and to examine the evolution of its members. The transcribed regions range from at least 7.0 to 13.1 kb, and the cDNAs contain deduced open reading frames of approximately 5. 5 kb. The predicted RGC2 proteins contain a nucleotide binding site and irregular leucine-rich repeats (LRRs) that are characteristic of resistance genes cloned from other species. Unique features of the RGC2 gene products include a bipartite LRR region with >40 repeats. At least eight members of this family are transcribed. The level of sequence diversity between family members varied in different regions of the gene. The ratio of nonsynonymous (Ka) to synonymous (Ks) nucleotide substitutions was lowest in the region encoding the nucleotide binding site, which is the presumed effector domain of the protein. The LRR-encoding region showed an alternating pattern of conservation and hypervariability. This alternating pattern of variation was also found in all comparisons within families of resistance genes cloned from other species. The Ka /Ks ratios indicate that diversifying selection has resulted in increased variation at these codons. The patterns of variation support the predicted structure of LRR regions with solvent-exposed hypervariable residues that are potentially involved in binding pathogen-derived ligands.

Speciation and domestication in maize and its wild relatives: evidence from the globulin-1 gene.

The grass genus Zea contains the domesticate maize and several wild taxa indigenous to Central and South America. Here we study the genetic consequences of speciation and domestication in this group by sampling DNA sequences from four taxa-maize (Zea mays ssp. mays), its wild progenitor (Z. mays ssp. parviglumis), a more distant species within the genus (Z. luxurians), and a representative of the sister genus (Tripsacum dactyloides). We sampled a total of 26 sequences from the glb1 locus, which encodes a nonessential seed storage protein. Within the Zea taxa sampled, the progenitor to maize contains the most sequence diversity. Maize contains 60% of the level of genetic diversity of its progenitor, and Z. luxurians contains even less diversity (32% of the level of diversity of Z. mays ssp. parviglumis). Sequence variation within the glb1 locus is consistent with neutral evolution in all four taxa. The glb1 data were combined with adh1 data from a previous study to make inferences about the population genetic histories of these taxa. Comparisons of sequence data between the two morphologically similar wild Zea taxa indicate that the species diverged approximately 700, 000 years ago from a common ancestor of intermediate size to their present populations. Conversely, the domestication of maize was a recent event that could have been based on a very small number of founding individuals. Maize retained a substantial proportion of the genetic variation of its progenitor through this founder event, but diverged rapidly in morphology.

The paleontology of intergene retrotransposons of maize.

Retrotransposons, transposable elements related to animal retroviruses, are found in all eukaryotes investigated and make up the majority of many plant genomes. Their ubiquity points to their importance, especially in their contribution to the large-scale structure of complex genomes. The nature and frequency of retro-element appearance, activation and amplification are poorly understood in all higher eukaryotes. Here we employ a novel approach to determine the insertion dates for 17 of 23 retrotransposons found near the maize adh1 gene, and two others from unlinked sites in the maize genome, by comparison of long terminal repeat (LTR) divergences with the sequence divergence between adh1 in maize and sorghum. All retrotransposons examined have inserted within the last six million years, most in the last three million years. The structure of the adh1 region appears to be standard relative to the other gene-containing regions of the maize genome, thus suggesting that retrotransposon insertions have increased the size of the maize genome from approximately 1200 Mb to 2400 Mb in the last three million years. Furthermore, the results indicate an increased mutation rate in retrotransposons compared with genes.

Xa21D encodes a receptor-like molecule with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution.

The rice Xa21 gene confers resistance to Xanthomonas oryzae pv oryzae in a race-specific manner. Analysis of the inheritance patterns and resistance spectra of transgenic plants carrying six Xa21 gene family members indicated that one member, designated Xa21D, displayed a resistance spectrum identical to that observed for Xa21 but conferred only partial resistance. Xa21D encodes a receptor-like protein carrying leucine-rich repeat (LRR) motifs in the presumed extracellular domain. The Xa21D transcript terminates shortly after the stop codon introduced by the retrotransposon Retrofit. Comparison of nucleotide substitutions in the LRR coding regions of Xa21 and Xa21D provided evidence of adaptive selection. Both functional and evolutionary evidence indicates that the Xa21D LRR domain controls race-specific pathogen recognition.

Investigation of the bottleneck leading to the domestication of maize.

Maize (Zea mays ssp. mays) is genetically diverse, yet it is also morphologically distinct from its wild relatives. These two observations are somewhat contradictory: the first observation is consistent with a large historical population size for maize, but the latter observation is consistent with strong, diversity-limiting selection during maize domestication. In this study, we sampled sequence diversity, coupled with simulations of the coalescent process, to study the dynamics of a population bottleneck during the domestication of maize. To do this, we determined the DNA sequence of a 1,400-bp region of the Adh1 locus from 19 individuals representing maize, its presumed progenitor (Z. mays ssp. parviglumis), and a more distant relative (Zea luxurians). The sequence data were used to guide coalescent simulations of population bottlenecks associated with domestication. Our study confirms high genetic diversity in maize-maize contains 75% of the variation found in its progenitor and is more diverse than its wild relative, Z. luxurians-but it also suggests that sequence diversity in maize can be explained by a bottleneck of short duration and very small size. For example, the breadth of genetic diversity in maize is consistent with a founding population of only 20 individuals when the domestication event is 10 generations in length.

Accelerated evolutionary rate in sulfur-oxidizing endosymbiotic bacteria associated with the mode of symbiont transmission.

The nearly neutral theory of molecular evolution predicts that the rate of nucleotide substitution should accelerate in small populations at sites under low selective constraint. We examined these predictions with respect to the relative population sizes for three bacterial life histories within chemolithoautotrophic sulfur-oxidizing bacteria: (1) free-living bacteria, (2) environmentally captured symbionts, and (3) maternally transmitted symbionts. Both relative rates of nucleotide substitution and relative ratios of loop, stem, and domain substitutions from 1,165 nt of the small-subunit 16S rDNA were consistent with expectations of the nearly neutral theory. Relative to free-living sulfur-oxidizing autotrophic bacteria, the maternally transmitted symbionts have faster substitution rates overall and also in low-constraint domains of 16S rDNA. Nucleotide substitition rates also differ between loop and stem positions. All of these findings are consistent with the predictions that these symbionts have relatively small effective population sizes. In contrast, the rates of nucleotide substitution in environmentally captured symbionts are slower, particularly in high-constraint domains, than in free-living bacteria.

Comparisons of the molecular evolutionary process at rbcL and ndhF in the grass family (Poaceae).

We examine rate heterogeneity among evolutionary lineages of the grass family at two plasmid loci, ndhF and rbcL, and we introduce a method to determine whether patterns of rate heterogeneity are correlated between loci. We show both that rates of synonymous evolution are heterogeneous among grass lineages and that are heterogeneity is correlated between loci at synonymous sites. At nonsynonymous sites, the pattern of rate heterogeneity is not correlated between loci, primarily due to an aberrant pattern of rate heterogeneity at nonsynonymous sites of rbcL. We compare patterns of synonymous rate heterogeneity to predictors based on the generation time effect and the speciation rate hypotheses. Although there is some evidence for generation time effects, neither generation time effects nor speciation rates appear to be sufficient to explain patterns of rate heterogeneity in the grass plastid sequences.