Contrasting the efficacy of selection on the X and autosomes in Drosophila

To investigate the relative efficacy of both positive and purifying natural selection on the X chromosome and the autosomes in Drosophila, we compared rates and patterns of molecular evolution between these chromosome sets using the newly available alignments of orthologous genes from 12 species. Parameters that may influence the relative X versus autosomal substitution rates include the relative effective population sizes, the male and female germline mutation rates, the distribution of allelic effects on fitness, and the degree of dominance of novel mutations. Our analysis reveals that codon usage bias is consistently greater for X-linked genes, suggesting that purifying selection consistently has greater efficacy on the X chromosome than on the autosomes across the Drosophila phylogeny. However, our results are less consistent with respect to the efficacy of positive selection, with only some lineages showing a higher substitution rate on the X chromosome. This suggests that either the distribution of selective effects of mutations or other relevant parameters are sufficiently variable across species to tip the balance in different ways in individual lineages. These data suggest that rates of substitution are not solely governed by adaptive evolution. This genome-wide analysis provides a clear picture that the efficacy of selection varies intragenomically and that this effect is markedly more consistent across the phylogeny in the case of purifying selection. Our results also suggest that simple models that predict systematic differences in rates of evolution between the X and the autosomes can only be made to be compatible with these Drosophila data if the relevant population genetic parameters that drive substitution rates differ among species and chromosomal contexts.     

Overdispersion of the molecular clock: temporal variation of gene-specific substitution rates in Drosophila

Simple models of molecular evolution assume that sequences evolve by a Poisson process in which nucleotide or amino acid substitutions occur as rare independent events. In these models, the expected ratio of the variance to the mean of substitution counts equals 1, and substitution processes with a ratio greater than 1 are called overdispersed. Comparing the genomes of 10 closely related species of Drosophila, we extend earlier evidence for overdispersion in amino acid replacements as well as in four-fold synonymous substitutions. The observed deviation from the Poisson expectation can be described as a linear function of the rate at which substitutions occur on a phylogeny, which implies that deviations from the Poisson expectation arise from gene-specific temporal variation in substitution rates. Amino acid sequences show greater temporal variation in substitution rates than do four-fold synonymous sequences. Our findings provide a general phenomenological framework for understanding overdispersion in the molecular clock. Also, the presence of substantial variation in gene-specific substitution rates has broad implications for work in phylogeny reconstruction and evolutionary rate estimation.     

Body mass‐corrected molecular rate for bird mitochondrial DNA

Mitochondrial DNA remains one of the most widely used molecular markers to reconstruct the phylogeny and phylogeography of closely related birds. It has been proposed that bird mitochondrial genomes evolve at a constant rate of ~0.01 substitution per site per million years, that is that they evolve according to a strict molecular clock. This molecular clock is often used in studies of bird mitochondrial phylogeny and molecular dating. However, rates of mitochondrial genome evolution vary among bird species and correlate with life history traits such as body mass and generation time. These correlations could cause systematic biases in molecular dating studies that assume a strict molecular clock. In this study, we overcome this issue by estimating corrected molecular rates for birds. Using complete or nearly complete mitochondrial genomes of 475 species, we show that there are strong relationships between body mass and substitution rates across birds. We use this information to build models that use bird species’ body mass to estimate their substitution rates across a wide range of common mitochondrial markers. We demonstrate the use of these corrected molecular rates on two recently published data sets. In one case, we obtained molecular dates that are twice as old as the estimates obtained using the strict molecular clock. We hope that this method to estimate molecular rates will increase the accuracy of future molecular dating studies in birds.     

Insights into the historical construction of species-rich biomes from dated plant phylogenies, neutral ecological theory and phylogenetic community structure

Analytical methods are now available that can date all nodes in a molecular phylogenetic tree with one calibration, and which correct for variable rates of DNA substitution in different lineages. Although these techniques are approximate, they offer a new tool to investigate the historical construction of species-rich biomes. Dated phylogenies of globally distributed plant families often indicate that dispersal, even across oceans, rather than plate tectonics, has generated their wide distributions. By contrast, there are indications that animal lineages have undergone less long distance dispersal. Dating the origin of biome-specific plant groups offers a means of estimating the age of the biomes they characterize. However, rather than a simple emphasis on biome age, we stress the importance of studies that seek to unravel the processes that have led to the accumulation of large numbers of species in some biomes. The synthesis of biological inventory, systematics and evolutionary biology offered by the frameworks of neutral ecological theory and phylogenetic community structure offers a promising route for future work.     

Generation time,life history and the substitution rate of neutral mutations

Our understanding of molecular evolution is hampered by a lack of quantitative predictions about how life-history (LH) traits should correlate with substitution rates. Comparative studies have shown that neutral substitution rates vary substantially between species, and evidence shows that much of this diversity is associated with variation in LH traits. However, while these studies often agree, some unexplained and contradictory results have emerged. Explaining these results is difficult without a clear theoretical understanding of the problem. In this study, we derive predictions for the relationships between LH traits and substitution rates in iteroparous species by using demographic theory to relate commonly measured life-history traits to genetic generation time, and by implication to neutral substitution rates. This provides some surprisingly simple explanations for otherwise confusing patterns, such as the association between fecundity and substitution rates. The same framework can be applied to more complex life histories if full life-tables are available.     

Energy and the tempo of evolution in amphibians

Aim The evolutionary speed hypothesis (ESH) attempts to explain global patterns of species richness on the basis that rates of molecular evolution and speciation in warmer climates have led to a greater accumulation of taxa at lower latitudes. A substantial alternative hypothesis to the ESH is the tropical conservatism hypothesis (TCH). However, recent tests of the TCH, using amphibians as the model taxon, have relied on the assumption that rates of molecular evolution are stable across latitudes and elevations. Here, we test for the first time for systematic variation in rates of molecular evolution across latitude and elevation among amphibians. Location The dataset is geographically diverse with samples from all continents except Antarctica and also from many of the earth's major tropical–warm temperate archipelagos. Methods We tested for substitution rate heterogeneity across climatically varying habitats with the mitochondrial RNA genes 12S and 16S. Thus, we report here on our findings for amphibians – a taxon whose phylogenetic and trophic contexts are remote from those previously tested – using genes that have also not been examined before. The study utilized paired contrasts of sister species (188 species across 18 families, including both caudates and anurans) that are spatially separated in either latitudinal or elevational dimensions. Results We found substantially faster substitution rates for species living in warmer habitats (P= 0.001–0.002) at both lower latitudes (P < 0.02) and lower elevations (P < 0.01). Main conclusions The consistency of these results with the previous studies that used quite different organisms – and in this instance also using different genes – suggests that this is a ubiquitous pattern in nature consistent with the predictions of the ESH. Recent tests of the TCH that, in estimating diversification rates, have relied on the assumption that DNA evolution occurs at a constant rate across latitudes and elevations, require reconsideration in light of the findings presented here. Our results indicate that greater caution is required when estimating dates of divergence using DNA sequence data.     

Ancestral inference and the study of codon bias evolution: implications for molecular evolutionary analyses of the Drosophila melanogaster subgroup

Reliable inference of ancestral sequences can be critical to identifying both patterns and causes of molecular evolution. Robustness of ancestral inference is often assumed among closely related species, but tests of this assumption have been limited. Here, we examine the performance of inference methods for data simulated under scenarios of codon bias evolution within the Drosophila melanogaster subgroup. Genome sequence data for multiple, closely related species within this subgroup make it an important system for studying molecular evolutionary genetics. The effects of asymmetric and lineage-specific substitution rates (i.e., varying levels of codon usage bias and departures from equilibrium) on the reliability of ancestral codon usage was investigated. Maximum parsimony inference, which has been widely employed in analyses of Drosophila codon bias evolution, was compared to an approach that attempts to account for uncertainty in ancestral inference by weighting ancestral reconstructions by their posterior probabilities. The latter approach employs maximum likelihood estimation of rate and base composition parameters. For equilibrium and most non-equilibrium scenarios that were investigated, the probabilistic method appears to generate reliable ancestral codon bias inferences for molecular evolutionary studies within the D. melanogaster subgroup. These reconstructions are more reliable than parsimony inference, especially when codon usage is strongly skewed. However, inference biases are considerable for both methods under particular departures from stationarity (i.e., when adaptive evolution is prevalent). Reliability of inference can be sensitive to branch lengths, asymmetry in substitution rates, and the locations and nature of lineage-specific processes within a gene tree. Inference reliability, even among closely related species, can be strongly affected by (potentially unknown) patterns of molecular evolution in lineages ancestral to those of interest.     

Population size and molecular evolution on islands

The nearly neutral theory predicts that the rate and pattern of molecular evolution will be influenced by effective population size (Ne), because in small populations more slightly deleterious mutations are expected to drift to fixation. This important prediction has not been widely empirically tested, largely because of the difficulty of comparing rates of molecular evolution in sufficient numbers of independent lineages which differ only in Ne. Island endemic species provide an ideal test of the effect of Ne on molecular evolution because species restricted to islands frequently have smaller Ne than closely related mainland species, and island endemics have arisen from mainland lineages many times in a wide range of taxa. We collated a dataset of 70 phylogenetically independent comparisons between island and mainland taxa, including vertebrates, invertebrates and plants, from 19 different island groups. The rate of molecular evolution in these lineages was estimated by maximum likelihood using two measures: overall substitution rate and the ratio of non-synonymous to synonymous substitution rates. We show that island lineages have significantly higher ratios of non-synonymous to synonymous substitution rates than mainland lineages, as predicted by the nearly neutral theory, although overall substitution rates do not differ significantly.     

The determinants of the molecular substitution process in turtles

Neutral rates of molecular evolution vary across species, and this variation has been shown to be related to biological traits. One of the first patterns to be observed in vertebrates has been an inverse relationship between body mass (BM) and substitution rates. The effects of three major life‐history traits (LHT) that covary with BM – metabolic rate, generation time and longevity (LON) – have been invoked to explain this relationship. However, most of the theoretical and empirical evidence supporting this relationship comes from endothermic vertebrates, that is, mammals and birds, in which the environmental conditions, especially temperature, do not have a direct impact on cellular and molecular biology. We analysed the variations in mitochondrial and nuclear rates of synonymous substitution across 224 turtle species and examined their correlation with two LHT (LON and BM) and two environmental variables [latitude (LAT) and habitat]. Our analyses indicate that in turtles, neutral rates of molecular evolution are hardly correlated with LON or BM. Rather, both the mitochondrial and nuclear substitution rates are significantly correlated with LAT – faster evolution in the tropics – and especially so for aquatic species. These results question the generality of the relationships reported in mammals and birds and suggest that environmental factors might be the strongest determinants of the mutation rate in ectotherms.     

Energy and spatial order in niche and community

The concept of a varying evolutionary tempo that is regulated by energy was first suggested in the 1950s. It was based on the observation that energy‐rich habitats appear to be the centres of evolutionary change, producing novel characters more frequently and having greater speciation rates. Subsequently, a number of studies have found positive relationships between evolutionary rate and energy. Gradients of energy occur across a range of scales and these have been invoked to explain, for example, higher tropical species richness. Precipitation has also been found to influence evolutionary rate, suggesting that biologically available energy and productivity are the important variables in the relationship rather than solar energy alone. Here, we take the theoretical step of investigating at smaller scales the implications of faster evolutionary tempo where productivity is greater: first at the level of the species population and, subsequently, for the same‐guild co‐habitants in a community. To facilitate, this we begin by applying the concept of gradients of available energy, from more productive to less productive sectors within the species niche, in the context of source‐sink theory. We then propose that a species population will have its highest rate of evolution, for changes that confer a positive selection coefficient throughout the niche, in that sector where it has best adaptive fit and greatest per capita energy flux. We also posit that, where it conferred a shift in fitness, an evolutionary change at niche optimum could subsequently affect conspecific populations occupying lower energy niche sectors via the selection‐mediated dispersal of the apomorphy into the more marginal components of the niche. We then infer that this type of change in a species with a generally higher per capita energy flux might negatively affect adjacent more slowly evolving species (living in less productive peripheral niches) in situations where the increased fitness conferred by a particular apomorphy was relevant to conditions occurring beyond the limits of the progenitor niche hypervolume. We therefore suggest a directional component to evolution at the compressed scales of niche and community level microevolution whereby populations and species occupying more productive conditions have greater tempos of change with attendant enhancements of both their competitive influence and their evolutionary potential. In this manner, previously recorded macro‐evolutionary patterns indicating faster evolution with increased energy at larger scales are interpreted in the context of proposed micro‐evolutionary relationships at intraspecific and locally interspecific scales. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 696–714.     

Exploring the correlations between sequence evolution rate and phenotypic divergence across the Mammalian tree provides insights into adaptive evolution

Sequence evolution behaves in a relatively consistent manner, leading to one of the fundamental paradigms in biology, the existence of a ??molecular clock??. The molecular clock can be distilled to the concept of accumulation of substitutions, through time yielding a stable rate from which we can estimate lineage divergence. Over the last 50?years, evolutionary biologists have obtained an in-depth understanding of this clock??s nuances. It has been fine-tuned by taking into account the vast heterogeneity in rates across lineages and genes, leading to ??relaxed?? molecular clock methods for timetree reconstruction. Sequence rate varies with life history traits including body size, generation time and metabolic rate, and we review recent studies on this topic. However, few studies have explicitly examined correlates between molecular evolution and morphological evolution. The patterns observed across diverse lineages suggest that rates of molecular and morphological evolution are largely decoupled. We discuss how identifying the molecular mechanisms behind rapid functional radiations are central to understanding evolution. The vast functional divergence within mammalian lineages that have relatively ??slow?? sequence evolution refutes the hypotheses that pulses in diversification yielding major phenotypic change are the result of steady accumulation of substitutions. Patterns rather suggest phenotypic divergence is likely caused by regulatory alterations mediated through mechanisms such as insertions/deletions in functional regions. These can rapidly arise and sweep to fixation faster than predicted from a lineage??s sequence neutral substitution rate, enabling species to leapfrog between phenotypic ??islands??. We suggest research directions that could illuminate mechanisms behind the functional diversity we see today.     

Inconsistencies in estimating the age of HIV-1 subtypes due to heterotachy

Rate heterogeneity among lineages is a common feature of molecular evolution, and it has long impeded our ability to accurately estimate the age of evolutionary divergence events. The development of relaxed molecular clocks, which model variable substitution rates among lineages, was intended to rectify this problem. Major subtypes of pandemic HIV-1 group M are thought to exemplify closely related lineages with different substitution rates. Here, we report that inferring the time of most recent common ancestor of all these subtypes in a single phylogeny under a single (relaxed) molecular clock produces significantly different dates for many of the subtypes than does analysis of each subtype on its own. We explore various methods to ameliorate this problem. We conclude that current molecular dating methods are inadequate for dealing with this type of substitution rate variation in HIV-1. Through simulation, we show that heterotachy causes root ages to be overestimated.     

Biomic specialization and speciation rates in ruminants (Cetartiodactyla, Mammalia): a test of the resource-use hypothesis at the global scale

The resource-use hypothesis proposed by E.S. Vrba predicts that specialist species have higher speciation and extinction rates than generalists because they are more susceptible to environmental changes and vicariance. In this work, we test some of the predictions derived from this hypothesis on the 197 extant and recently extinct species of Ruminantia (Cetartiodactyla, Mammalia) using the biomic specialization index (BSI) of each species, which is based on its distribution within different biomes. We ran 10000 Monte Carlo simulations of our data in order to get a null distribution of BSI values against which to contrast the observed data. Additionally, we drew on a supertree of the ruminants and a phylogenetic likelihood-based method (QuaSSE) for testing whether the degree of biomic specialization affects speciation rates in ruminant lineages. Our results are consistent with the predictions of the resource-use hypothesis, which foretells a higher speciation rate of lineages restricted to a single biome (BSI = 1) and higher frequency of specialist species in biomes that underwent high degree of contraction and fragmentation during climatic cycles. Bovids and deer present differential specialization across biomes; cervids show higher specialization in biomes with a marked hydric seasonality (tropical deciduous woodlands and schlerophyllous woodlands), while bovids present higher specialization in a greater variety of biomes. This might be the result of divergent physiological constraints as well as a different biogeographic and evolutionary history.     

Body mass is less important than bird order in determining the molecular rate for bird mitochondrial DNA

A negative relationship between body mass and molecular evolution rates has been suggested, and recently a correlation equation has been published based on mitochondrial genomic data of 475 bird species and their body masses. Here, we re‐analysed these data and show that the bird order as a proxy of monophyletic groups was a stronger predictor of the molecular rate than the body mass. We provide order‐specific molecular substitution rates. Only three orders (Galliformes, Gruiformes, Pelecaniformes) showed a very clear negative correlation, and specific correlation equations are given for these. The molecular rates of bird orders differed strongly at similar mean body masses, and we suggest that the previously described trend across all birds may arise as smaller species also tend to have characteristic life histories, namely faster turnover of generations, higher fecundity and shorter lifespans.     

The chromosomes of Leishmania

Chromosome size polymorphisms occur in Leishmania such that each strain of a given species has a distinctive molecular karyotype. Despite this variability, the chromosomal similarities among closely related strains of Leishmania are sufficiently characteristic to permit classification of unidentified clinical isolates. Mechanisms generating chromosome size polymorphisms are related to chromosomal evolution. In this review, Geoffrey Lighthall and Suzanne Giannini explain that the chromosomal profiles of members of different species may be diverging from a conserved 'consensus' karyotype at different rates, and present a current understanding of the genomic organization of Leishmania with emphasis on chromosomal elements.     

Molecular evolution of PISTILLATA-like genes in the dogwood genus Cornus (Cornaceae)

The MADS-box gene family encodes critical regulators determining floral organ development. Understanding evolutionary patterns and processes of MADS-box genes is an important step toward unraveling the molecular basis of floral morphological evolution. In this study, we investigated the evolution of PI-like genes of the MADS-box family in the dogwood genus Cornus (Cornaceae). Cornus is a eudicot lineage in the asterids clade, and is intriguing in evolving petaloid bract morphology in two major lineages within the genus. The gene genealogy reconstructed using genomic DNA and cDNA sequences suggests multiple PI-like gene duplication events in Cornus. An ancient duplication event resulted in two ancient paralogs, CorPI-A and CorPI-B, which have highly diverged intron regions. Duplication of CorPI-A further resulted in two paralogs in one subgroup of Cornus, the BW group that does not produce modified bracts. Most species analyzed were found to contain more than one copy of the PI-like gene with most copies derived recently within species. Estimation and comparison of dN/dS ratios revealed relaxed selection in the PI-like gene in Cornus in comparison with the gene in the closely related outgroups Alangium and Davidia, and in other flowering plants. Selection also differed among major gene copies, CorPI-A and CorPI-B, and among different morphological subgroups of Cornus. Variation in selection pressures may indicate functional changes in PI-like genes after gene duplication and among different lineages. Strong positive selection at three amino acid sites of CorPI was also detected from a region critical for dimerization activity. Total substitution rates of the CorPI gene also differ among lineages of Cornus, showing a trend similar to that found in dN/dS ratios. We also found that the CorPI-A copy contains informative phylogenetic information when compared across species of Cornus.     

Sociality and the rate of molecular evolution

The molecular clock does not tick at a uniform rate in all taxa but may be influenced by species characteristics. Eusocial species (those with reproductive division of labor) have been predicted to have faster rates of molecular evolution than their nonsocial relatives because of greatly reduced effective population size; if most individuals in a population are nonreproductive and only one or few queens produce all the offspring, then eusocial animals could have much lower effective population sizes than their solitary relatives, which should increase the rate of substitution of "nearly neutral" mutations. An earlier study reported faster rates in eusocial honeybees and vespid wasps but failed to correct for phylogenetic nonindependence or to distinguish between potential causes of rate variation. Because sociality has evolved independently in many different lineages, it is possible to conduct a more wide-ranging study to test the generality of the relationship. We have conducted a comparative analysis of 25 phylogenetically independent pairs of social lineages and their nonsocial relatives, including bees, wasps, ants, termites, shrimps, and mole rats, using a range of available DNA sequences (mitochondrial and nuclear DNA coding for proteins and RNAs, and nontranslated sequences). By including a wide range of social taxa, we were able to test whether there is a general influence of sociality on rates of molecular evolution and to test specific predictions of the hypothesis: (1) that social species have faster rates because they have reduced effective population sizes; (2) that mitochondrial genes would show a greater effect of sociality than nuclear genes; and (3) that rates of molecular evolution should be correlated with the degree of sociality. We find no consistent pattern in rates of molecular evolution between social and nonsocial lineages and no evidence that mitochondrial genes show faster rates in social taxa. However, we show that the most highly eusocial Hymenoptera do have faster rates than their nonsocial relatives. We also find that social parasites (that utilize the workers from related species to produce their own offspring) have faster rates than their social relatives, which is consistent with an effect of lower effective population size on rate of molecular evolution. Our results illustrate the importance of allowing for phylogenetic nonindependence when conducting investigations of determinants of variation in rate of molecular evolution.     

Molecular evolution of the neurotrophin family members and their Trk receptors

Neurotrophins are structurally related proteins regulating brain development and function. Molecular evolution studies of neurotrophins and their receptors are essential for understanding the mechanisms underlying the coevolution processes of these gene families and how they correlate with the increased complexity of the vertebrate nervous system. In order to improve our current knowledge of the molecular evolution of neurotrophins and receptors, we have collected all information available in the literature and analyzed the genome database for each of them. Statistical analysis of aminoacid and nucleotide sequences of the neurotrophin and Trk family genes was applied to both complete genes and mature sequences, and different phylogenetic methods were used to compare aminoacid and nucleotide sequences variability among the different species. All collected data favor a model in which several rounds of genome duplications might have facilitated the generation of the many different neurotrophins and the acquisition of specific different functions correlated with the increased complexity of the vertebrate nervous system during evolution. We report findings that refine the structure of the evolutionary trees for neurotrophins and Trk receptors families, indicate different rates of evolution for each member of the two families, and newly demonstrate that the NGF-like genes found in Fowlpox and Canarypox viruses are closely related to reptile NGF.     

Substitution bias, rapid saturation, and the use of mtDNA for nematode systematics

Only relatively recently have researchers turned to molecular methods for nematode phylogeny reconstruction. Thus, we lack the extensive literature on evolutionary patterns and phylogenetic usefulness of different DNA regions for nematodes that exists for other taxa. Here, we examine the usefulness of mtDNA for nematode phylogeny reconstruction and provide data that can be used for a priori character weighting or for parameter specification in models of sequence evolution. We estimated the substitution pattern for the mitochondrial ND4 gene from intraspecific comparisons in four species of parasitic nematodes from the family Trichostrongylidae (38-50 sequences per species). The resulting pattern suggests a strong mutational bias toward A and T, and a lower transition/transversion ratio than is typically observed in other taxa. We also present information on the relative rates of substitution at first, second, and third codon positions and on relative rates of saturation of different types of substitutions in comparisons ranging from intraspecific to interordinal. Silent sites saturate extremely quickly, presumably owing to the substitution bias and, perhaps, to an accelerated mutation rate. Results emphasize the importance of using only the most closely related sequences in order to infer patterns of substitution accurately for nematodes or for other taxa having strongly composition-biased DNA. ND4 also shows high amino acid polymorphism at both the intra- and interspecific levels, and in higher level comparisons, there is evidence of saturation at variable amino acid sites. In general, we recommend using mtDNA coding genes only for phylogenetics of relatively closely related nematode species and, even then, using only nonsynonymous substitutions and the more conserved mitochondrial genes (e.g., cytochrome oxidases). On the other hand, the high substitution rate in genes such as ND4 should make them excellent for population genetics studies, identifying cryptic species, and resolving relationships among closely related congeners when other markers show insufficient variation.