Codon usage is associated with the evolutionary age of genes in metazoan genomes

Background  

Codon usage may vary significantly between different organisms and between genes within the same organism. Several evolutionary processes have been postulated to be the predominant determinants of codon usage: selection, mutation, and genetic drift. However, the relative contribution of each of these factors in different species remains debatable. The availability of complete genomes for tens of multicellular organisms provides an opportunity to inspect the relationship between codon usage and the evolutionary age of genes.     

Developmental basis of evolutionary digit loss in the Australian lizard Hemiergis

Loss of limb skeletal elements is a recurring theme in tetrapod evolution, but the developmental mechanisms underlying this phenomenon remain largely unknown. The Australian lizard genus Hemiergis offers an excellent model system to study limb reduction among closely related, naturally occurring populations with different numbers of digits. Evolutionary digit loss in Hemiergis does not result from simple truncation of a pentadactyl skeletal developmental program. Rather, the duration of embryonic expression of the patterning molecule Sonic hedgehog (SHH) is shortened in limbs with reduced numbers of digits, and is correlated with decreased cell proliferation in the posterior aspect of the limb. Moreover, this comparative analysis suggests an early role for SHH in specification of digit identity and later importance in maintaining cell proliferation and survival. Subtle changes in spatial or temporal regulation of SHH may alter proliferation and patterning of the developing limb, thereby effecting divergence in adult limb morphology among closely related species. In contrast, expression of MSX and Distal-less proteins were similar among embryos from different populations.     

Phylogeny reconstruction: increasing the accuracy of pairwise distance estimation using Bayesian inference of evolutionary rates

Distance-based methods for phylogeny reconstruction are the fastest and easiest to use, and their popularity is accordingly high. They are also the only known methods that can cope with huge datasets of thousands of sequences. These methods rely on evolutionary distance estimation and are sensitive to errors in such estimations. In this study, a novel Bayesian method for estimation of evolutionary distances is developed. The proposed method enables the use of a sophisticated evolutionary model that better accounts for among-site rate variation (ASRV), thereby improving the accuracy of distance estimation. Rate variations are estimated within a Bayesian framework by extracting information from the entire dataset of sequences, unlike standard methods that can only use one pair of sequences at a time. We compare the accuracy of a cascade of distance estimation methods, starting from commonly used methods and moving towards the more sophisticated novel method. Simulation studies show significant improvements in the accuracy of distance estimation by the novel method over the commonly used ones. We demonstrate the effect of the improved accuracy on tree reconstruction using both real and simulated protein sequence alignments. An implementation of this method is available as part of the SEMPHY package.     

Bayesian inference of the metazoan phylogeny; a combined molecular and morphological approach

Metazoan phylogeny remains one of evolutionary biology's major unsolved problems. Molecular and morphological data, as well as different analytical approaches, have produced highly conflicting results due to homoplasy resulting from more than 570 million years of evolution. To date, parsimony has been the only feasible combined approach but is highly sensitive to long-branch attraction. Recent development of stochastic models for discrete morphological characters and computationally efficient methods for Bayesian inference has enabled combined molecular and morphological data analysis with rigorous statistical approaches less prone to such inconsistencies. We present the first statistically founded analysis of a metazoan data set based on a combination of morphological and molecular data and compare the results with a traditional parsimony analysis. Interestingly, the Bayesian analyses demonstrate a high degree of congruence between morphological and molecular data, and both data sets contribute to the result of the combined analysis. Additionally, they resolve several irregularities obtained in previous studies and show high credibility values for controversial groups such as the ecdysozoans and lophotrochozoans. Parsimony, on the contrary, shows conflicting results, with morphology being congruent to the Bayesian results and the molecular data set producing peculiarities that are largely reflected in the combined analysis.     

Amerind ancestry, socioeconomic status and the genetics of type 2 diabetes in a Colombian population

The "thrifty genotype" hypothesis proposes that the high prevalence of type 2 diabetes (T2D) in Native Americans and admixed Latin Americans has a genetic basis and reflects an evolutionary adaptation to a past low calorie/high exercise lifestyle. However, identification of the gene variants underpinning this hypothesis remains elusive. Here we assessed the role of Native American ancestry, socioeconomic status (SES) and 21 candidate gene loci in susceptibility to T2D in a sample of 876 T2D cases and 399 controls from Antioquia (Colombia). Although mean Native American ancestry is significantly higher in T2D cases than in controls (32% v 29%), this difference is confounded by the correlation of ancestry with SES, which is a stronger predictor of disease status. Nominally significant association (P<0.05) was observed for markers in: TCF7L2, RBMS1, CDKAL1, ZNF239, KCNQ1 and TCF1 and a significant bias (P<0.05) towards OR>1 was observed for markers selected from previous T2D genome-wide association studies, consistent with a role for Old World variants in susceptibility to T2D in Latin Americans. No association was found to the only known Native American-specific gene variant previously associated with T2D in a Mexican sample (rs9282541 in ABCA1). An admixture mapping scan with 1,536 ancestry informative markers (AIMs) did not identify genome regions with significant deviation of ancestry in Antioquia. Exclusion analysis indicates that this scan rules out ~95% of the genome as harboring loci with ancestry risk ratios >1.22 (at P < 0.05).     

Amphioxus mitochondrial DNA,chordate phylogeny,and the limits of inference based on comparisons of sequences

Analyses of both the nucleotide and amino acid sequences derived from all 13 mitochondrial protein-encoding genes (12,234 bp) of 19 metazoan species, including that of the lancelet Branchiostoma floridae ("amphioxus"), fail to yield the widely accepted phylogeny for chordates and, within chordates, for vertebrates. Given the breadth and the compelling nature of the data supporting that phylogeny, relationships supported by the mitochondrial sequence comparisons are almost certainly incorrect, despite their being supported by equally weighted parsimony, distance, and maximum-likelihood analyses. The incorrect groupings probably result in part from convergent base-compositional similarities among some of the taxa, similarities that are strong enough to overwhelm the historical signal. Comparisons among very distantly related taxa are likely to be particularly susceptible to such artifacts, because the historical signal is already greatly attenuated. Empirical results underscore the need for approaches to phylogenetic inference that go beyond simple site-by-site comparison of aligned sequences. This study and others indicate that, once a sequence sample of reasonable size has been obtained, accurate phylogenetic estimation may be better served by incorporating knowledge of molecular structures and processes into inference models and by seeking additional higher order characters embedded in those sequences, than by gathering ever larger sequence samples from the same organisms in he hope that the historical signal will eventually prevail.     

Isolation and characterization of two T-box genes from sponges,the phylogenetically oldest metazoan taxon

It is now well established that all metazoan phyla derived from one common ancestor, the hypothetical Urmetazoa. Due to the basal position of Porifera (Demospongiae) in the phylogenetic tree of Metazoa, studies on the mechanisms controlling the development of these animals can provide clues on the understanding of the origin of multicellular animals and on how the first organization of the body plan evolved. In this report we describe the isolation and genomic characterization of two T-box genes from the siliceous sponge Suberites domuncula. The phylogenetic analysis classifies one into the subfamily of Brachyury, Sd-Bra, and the second into the Tbx2 subfamily, Sd-Tbx2. Analyses of the Sd-Bra and Sd-Tbx2 sequences and their intron-exon structures demonstrate their basal position in the phylogeny of the T-box family, and allows us to hypothesize a model of the phylogenetic evolution of all T-box genes. Furthermore, we report the presence of two different products of alternative splicing of Sd-Bra, and demonstrate that they exist in different phosphorylation and glycosylation states in the sponge tissue. Sd-Bra expression in tissue and 3D-cell aggregates (primmorphs) is analyzed, suggesting that Sd-Bra might also have a role in Porifera morphogenesis.Edited by N. SatohThe sequences from Suberites domuncula reported here are deposited in the EMBL/GenBank data base: the cDNA of Brachyury (Sd-Bra; accession number AJ544242) as well as the second T-box gene Sd-Tbx2 (AJ544241).     

The role of nuclear genes in intraspecific evolutionary inference: genealogy of the transferrin gene in the brown trout

Technical and biological hurdles have precluded the retrieval of nuclear gene genealogies within most species. Among these obstacles, the possibility of intragenic recombination is one of the most demanding challenges. We studied the utility of nuclear genes for intraspecific evolutionary inferences by selecting a nuclear gene that exhibits patterns of considerable geographic differentiation in the brown trout (Salmo trutta) species complex. Haplotype variation from a nucleotide sequence of approximately 3.7 kb encompassing a portion of the transferrin (TF) gene was surveyed in 31 brown trout individuals collected across the native Eurasian range. Statistically significant recombination and gene conversion events were detected. However, we showed that the substantial cladistic structure was not disrupted by recombination or gene conversion events and the additional structure was estimated to have emerged after those events. Because loci with unusually high levels of variation might indicate the presence of selection, we tested the hypothesis of neutrality and found some evidence for directional selection. The strong geographic signal observed in the TF genealogy, coupled with the current spatial distribution of electromorphs, gave us the ability to draw empirical phylogeographic inferences. We delineated the composition of current brown trout populations on the basis of 3,625 individuals electrophoretically scored for the TF locus. We hypothesized scenarios of historical radiation and dispersal events, thus providing new insights refining previous allozyme and mtDNA inferences. We infer that the most ancestral brown trout populations inhabited tributaries from the Black, Caspian, and Aral Sea drainages. An early radiation of the species occurred throughout the Mediterranean, followed by independent dispersal events from the Adriatic to the southernmost Iberian Atlantic and, more recently, a rapid expansion throughout most of the Atlantic drainages.     

Developmental modularity and the evolutionary diversification of arthropod limbs

Segmentation is one of the most salient characteristics of arthropods, and differentiation of segments along the body axis is the basis of arthropod diversification. This article evaluates whether the evolution of segmentation involves the differentiation of already independent units, i.e., do segments evolve as modules? Because arthropod segmental differentiation is commonly equated with differential character of appendages, we analyze appendages by comparing similarities and differences in their development. The comparison of arthropod limbs, even between species, is a comparison of serially repeated structures. Arthropod limbs are not only reiterated along the body axis, but limbs themselves can be viewed as being composed of reiterated parts. The interpretation of such reiterated structures from an evolutionary viewpoint is far from obvious. One common view is that serial repetition is evidence of a modular organization, i.e., repeated structures with a common fundamental identity that develop semi-autonomously and are free to diversify independently. In this article, we evaluate arthropod limbs from a developmental perspective and ask: are all arthropod limbs patterned using a similar set of mechanisms which would reflect that they all share a generic coordinate patterning system? Using Drosophila as a basis for comparison, we find that appendage primordia, positioned along the body using segmental patterning coordinates, do indeed have elements of common identity. However, we do not find evidence of a single coordinate system shared either between limbs or among limb branches. Data concerning the other diagnostic of developmental modularity--semi-autonomy of development--are not currently available for sufficient taxa. Nonetheless, some data comparing patterns of morphogenesis provide evidence that limbs cannot always be temporally or spatially decoupled from the development of their neighbors, suggesting that segment modularity is a derived character.     

Dating the Dipsacales: comparing models, genes, and evolutionary implications

Dipsacales is an asterid angiosperm clade of ca. 1100 species, with most of its lineages occupying temperate regions of the Northern Hemisphere. A recent phylogenetic analysis based on 7593 nucleotides of chloroplast DNA recovered a well-resolved and strongly supported phylogenetic hypothesis, which we use here to estimate divergence times within the group. A molecular clock is strongly rejected, regardless of data partition. We used recently proposed methods that relax the assumption of rate constancy among lineages (local clocks, nonparametric rate smoothing, penalized likelihood, and Bayesian relaxed clock) to estimate the ages of major lineages. Age estimates for Dipsacales varied widely among markers and codon positions, and depended on the fossils used for calibration and method of analysis. Some methods yielded dates for the Dipsacales diversification that appear to be too old (prior to the presumed 125 my [million years] age of eudicots), and others suggested ages that are too young based on well-documented Dipsacales fossils. Concordant penalized likelihood and Bayesian studies imply that Dipsacales originated in the Cretaceous, as did its two major lineages, Adoxaceae and Caprifoliaceae. However, diversification of crown Adoxaceae and Caprifoliaceae mainly occurred in the Tertiary, with the origin of major lineages within these clades mainly occurring during the Eocene. Another round of diversification appears to have occurred in the Miocene. Several radiations, such as Valerianaceae in South America and Dipsacaceae around the Mediterranean, are even more recent. This study demonstrates the wide range of divergence times that can be obtained using different methods and data sets, and cautions against reliance on age estimates based on only a single gene or methodology. Despite this variance, significant conclusions can be made about the timing of Dipsacales evolution.     

Bovine genome mapping: evolutionary inference and the power of comparative genomics

All bovine chromosomes are now represented by a syntenic group, a linkage map and at least one in situ hybridization. Almost 1000 loci are mapped, about 300 of which are coding sequences useful for comparative mapping and evolutionary inference. Economically important loci are beginning to appear on bovine linkage maps and enhanced comparative maps are likely to be necessary to identify many of these genes by a comparative positional candidate gene approach.     

Developmental variability and the limits of adaptation: Interactions with stress

1. Little evolutionary change may occur at species borders since the cost of accommodating environmental stresses is high. Extreme examples of such stasis include cave animals in stable stressed environments and ‘living fossils’ in widely fluctuating stressed environments. 2. Variability from the molecular to the organismic level tends to be high under extreme stress. At the developmental level, the fitness of such variants may be low. This means that much developmental variability in natural populations may have little evolutionary significance. 3. Rapid evolutionary change of morphological traits is most likely to be based upon genes acting late in a developmental pathway under conditions which are ecologically and energetically permissive. 4. Although some increases in resistance to temperature extremes have been recorded in laboratory selection experiments, major extensions of extremes in natural populations appear difficult to achieve. The energetic costs of surviving extremes at species borders implies that the evolution of major developmental and morphological shifts is more likely to be a feature of populations of more equable habitats.     

On inference in ecology and evolutionary biology: the problem of multiple causes

Summary If one investigates a process that has several causes but assumes that it has only one cause, one risks ruling out important causal factors. Three mechanisms account for this mistake: either the significance of the single cause under test is masked by noise contributed by the unsuspected and uncontrolled factors, or the process appears only when two or more causes interact, or the process appears when there are present any of a number of sufficient causes which are not mutally exclusive. In ecology and evolutionary biology, experiments usually test single factor hypotheses, and many scientists apparently believe that hypotheses incorporating several factors are so much more difficult to test that to do so would not be practical. We discuss several areas in ecology and evolutionary biology in which the presupposition of simple causation has apparently impeded progress. We also examine a more mature field, the study of atherosclerosis, in which single factor studies did significantly delay progress towards understanding what now appears to be a multifactor process. The problem has three solutions: either factorial experiments, dynamic models that make quantitative predictions, response-surface methods, or all three. In choosing a definition for cause, we make a presupposition that profoundly influences subsequent observations and experimental designs. Alternative definitions of causation should be considered as contributing to potential cures for research problems.Order of authorship decided by the flip of a coin.     

Developmental and evolutionary implications of labial, Deformed and engrailed expression in the Drosophila head.

Prior developmental genetic analyses have shown that labial (lab) and Deformed (Dfd) are homeotic genes that function in the development of the embryonic (larval) and adult head. Using antibody probes to reveal the spatial distribution of the lab and Dfd proteins in embryonic and imaginal tissues, we have assessed the respective roles of these genes through an analysis of the correspondence of their expression patterns with their mutant phenotypes. With regard to imaginal development, lab and Dfd occupy adjacent non-overlapping expression domains in the peripodial cell layer of the eye-antennal disc, in patterns that are consistent with their adult mutant phenotypes and published fate maps. During embryogenesis, lab and Dfd exhibit limited overlapping expression in areas that are of no obvious significance to the development of larval head structures, but also in areas that may have consequences for imaginal development. The head of Drosophila and other cyclorrhaphous Dipterans is characterized by an extreme morphological difference between the larval and adult stages. Given this unique ontogenetic and phylogenetic history and the observation that homeotic transformations produced by the lab, Dfd, and proboscipedia (pb) loci are manifested only in the adult, we suggest that distinct regulatory paradigms evolved for homeotic gene function in the development of the larval versus adult head. Finally, a detailed examination of the engrailed (en) expression pattern in the embryonic head strengthens the view of insect morphologists that the clypeolabrum evolved from the fusion of paired labral appendages.     

The different limits of weak selection and the evolutionary dynamics of finite populations

Evolutionary theory often resorts to weak selection, where different individuals have very similar fitness. Here, we relate two ways to introduce weak selection. The first considers evolutionary games described by payoff matrices with similar entries. This approach has recently attracted a lot of interest in the context of evolutionary game dynamics in finite populations. The second way to introduce weak selection is based on small distances in phenotype space and is a standard approach in kin-selection theory. Whereas both frameworks are interchangeable for constant fitness, frequency-dependent selection shows significant differences between them. We point out the difference between both limits of weak selection and discuss the condition under which the differences vanish. It turns out that this condition is fulfilled by the popular parametrization of the prisoner's dilemma in benefits and costs. However, for general payoff matrices differences between the two frameworks prevail.