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120 results for “evolutionary rate”
Data from: Lineage-specific sequence evolution and exon edge conservation partially explain the relationship of evolutionary rate and expression level in A. thaliana
Rapidly evolving proteins can aid the identification of genes underlying phenotypic adaptation across taxa, but functional and structural elements of genes can also affect evolutionary rates. In plants, the 'edges' of exons, flanking intron junctions, are known to contain splice enhancers and to have a higher degree of conservation compared to the remainder of the coding region. However, the extent to which these regions may be masking indicators of positive selection or account for the relationship between dN/dS and other genomic parameters is unclear. We investigate the effects of exon edge conservation on the relationship of dN/dS to various sequence characteristics and gene expression parameters in the model plant Arabidopsis thaliana. We also obtain lineage-specific dN/dS estimates, making use of the recently sequenced genome of Thellungiella parvula, the second closest sequenced relative after the sister species Arabidopsis lyrata. Overall, we find that the effect of exon edge conservation, as well as the use of lineage-specific substitution estimates, upon dN/dS ratios partly explains the relationship between the rates of protein evolution and expression level. Furthermore, the removal of exon edges shifts dN/dS estimates upwards, increasing the proportion of genes potentially under adaptive selection. We conclude that lineage-specific substitutions and exon edge conservation have an important effect on dN/dS ratios and should be considered when assessing their relationship with other genomic parameters..
Data from: A comment on the use of stochastic character maps to estimate evolutionary rate variation in a continuously valued trait
Phylogenetic comparative biology has progressed considerably in recent years. One of the most important developments has been the application of likelihood-based methods to fit alternative models for trait evolution in a phylogenetic tree with branch lengths proportional to time. An important example of this type of method is O'Meara et al.'s (2006) "noncensored" test for variation in the evolutionary rate for a continuously valued character trait through time or across the branches of a phylogenetic tree. According to this method, we first hypothesize evolutionary rate regimes on the tree (called "painting" in Butler and King, 2004); and then we fit an evolutionary model, specifically the popular Brownian model, in which the instantaneous variance of the Brownian random diffusion process has different values in different parts of the phylogeny. The authors suggest that to test a hypothesis that the state of a discrete character influenced the rate of a continuous character, one could use the approach of Neilsen (2002) to first stochastically map the discretely valued trait, and then "test to see whether the portions of the tree with one state for the discrete character have a different rate of evolution for the continuous character than portions of the tree to which the other discrete state has been mapped" (O'Meara et al., 2006, p. 931). Indeed, this has become common practice for this and other closely related methods. Here, I examine this practice. In particular, I show that evolutionary rates estimated this way (i.e., by using maximum likelihood [ML] to fit a multirate model on each stochastically mapped tree; and then averaging across trees) are systematically biased to be more similar to each other than are the underlying generating parameters. My analysis also reveals that this effect is dependent on the rate of evolution for the discrete trait. Specifically, if the rate of evolution for the discrete character is low then the difference between the true history and any stochastically mapped 1 history is generally small. This results in evolutionary rates for the continuous trait that are estimated with little bias. Conversely, if the rate of evolution for the discrete character is very high, then the true and hypothesized character histories are often extremely dissimilar, evolutionary rate estimates are biased to be more similar to each other than their underlying generating values, and we lose power to distinguish evolutionary rates on the tree.
Data from: Evolutionary rates for multivariate traits: the role of selection and genetic variation
A fundamental question in evolutionary biology is the relative importance of selection and genetic architecture in determining evolutionary rates. Adaptive evolution can be described by the multivariate breeders' equation, which predicts evolutionary change for a suite of phenotypic traits as a product of directional selection acting on them (β) and the genetic variance–covariance matrix for those traits (G). Despite being empirically challenging to estimate, there are enough published estimates of G and β to allow for synthesis of general patterns across species. We use published estimates to test the hypotheses that there are systematic differences in the rate of evolution among trait types, and that these differences are, in part, due to genetic architecture. We find some evidence that sexually selected traits exhibit faster rates of evolution compared with life-history or morphological traits. This difference does not appear to be related to stronger selection on sexually selected traits. Using numerous proposed approaches to quantifying the shape, size and structure of G, we examine how these parameters relate to one another, and how they vary among taxonomic and trait groupings. Despite considerable variation, they do not explain the observed differences in evolutionary rates.
Data from: Selection, genome-wide fitness effects and evolutionary rates in the model legume Medicago truncatula
Sequence data for >20 000 annotated genes from 56 accessions of Medicago truncatula were used to identify potential targets of positive selection, the determinants of evolutionary rate variation and the relative importance of positive and purifying selection in shaping nucleotide diversity. Based upon patterns of intraspecific diversity and interspecific divergence, c. 50–75% of nonsynonymous polymorphisms are subject to strong purifying selection and 1% of the sampled genes harbour a signature of positive selection. Combining polymorphism with expression data, we estimated the distribution of fitness effects and found that the proportion of deleterious mutations is significantly greater for expressed genes than for genes with undetected transcripts (nonexpressed) in a previous RNA-seq experiment and greater for broadly expressed genes than those expressed in only a single tissue. Expression level is the strongest correlate of evolutionary rates at nonsynonymous sites, and despite multiple genomic features being significantly correlated with evolutionary rates, they explain less than 20% of the variation in nonsynonymous rates (dN) and <15% of the variation in either synonymous rates (dS) or dN:dS. Among putative targets of selection were genes involved in defence against pathogens and herbivores, genes with roles in mediating the relationship with rhizobial symbionts and one-third of annotated histone-lysine methyltransferases. Adaptive evolution of the methyltransferases suggests that positive selection in gene expression may have occurred through evolution of enzymes involved in epigenetic modification.
Data from: Molecular dating, evolutionary rates, and the age of the grasses
Many questions in evolutionary biology require an estimate of divergence times but, for groups with a sparse fossil record, such estimates rely heavily on molecular dating methods. The accuracy of these methods depends on both an adequate underlying model and the appropriate implementation of fossil evidence as calibration points. We explore the effect of these in Poaceae (grasses), a diverse plant lineage with a very limited fossil record, focusing particularly on dating the early divergences in the group. We show that molecular dating based on a dataset of plastid markers is strongly dependent on the model assumptions. In particular, an acceleration of evolutionary rates at the base of Poaceae followed by a deceleration in the descendants strongly biases methods that assume an autocorrelation of rates. This problem can be circumvented by using markers that have lower rate variation, and we show that phylogenetic markers extracted from complete nuclear genomes can be a useful complement to the more commonly used plastid markers. However, estimates of divergence times remain strongly affected by different implementations of fossil calibration points. Analyses calibrated with only macrofossils lead to estimates for the age of core Poaceae around 51-55 Ma, but the inclusion of microfossil evidence pushes this age to 74-82 Ma and leads to lower estimated evolutionary rates in grasses. These results emphasize the importance of considering markers from multiple genomes and alternative fossil placements when addressing evolutionary issues that depend on ages estimated for important groups.
Data from: Diversity, disparity, and evolutionary rate estimation for unresolved Yule trees
The branching structure of biological evolution confers statistical dependencies on phenotypic trait values in related organisms. For this reason, comparative macroevolutionary studies usually begin with an inferred phylogeny that describes the evolutionary relationships of the organisms of interest. The probability of the observed trait data can be computed by assuming a model for trait evolution, such as Brownian motion, over the branches of this fixed tree. However, the phylogenetic tree itself contributes statistical uncertainty to estimates of other evolutionary quantities, and many comparative evolutionary biologists regard the tree as a nuisance parameter. In this paper, we present a framework for analytically integrating over unknown phylogenetic trees in comparative evolutionary studies by assuming that the tree arises from a continuous-time Markov branching model called the Yule process. To do this, we derive a closed-form expression for the distribution of phylogenetic diversity, which is the sum of branch lengths connecting a set of taxa. We then present a generalization of phylogenetic diversity which is equivalent to the expected trait disparity in a set of taxa whose evolutionary relationships are generated by a Yule process and whose traits evolve by Brownian motion. We derive expressions for the distribution of expected trait disparity under a Yule tree. Given one or more observations of trait disparity in a clade, we perform fast likelihood-based estimation of the Brownian variance for unresolved clades. Our method does not require simulation or a fixed phylogenetic tree. We conclude with a brief example illustrating Brownian rate estimation for thirteen taxonomic families in order Carnivora, in which the phylogenetic tree for each family is unresolved.
Data from: Ploidy tug-of-war: evolutionary and genetic environments influence the rate of ploidy drive in a human fungal pathogen
Variation in baseline ploidy is seen throughout the tree of life, yet the factors that determine why one ploidy level is maintained over another remain poorly understood. Experimental evolution studies using asexual fungal microbes with manipulated ploidy levels intriguingly reveals a propensity to return to the historical baseline ploidy, a phenomenon that we term 'ploidy drive'. We evolved haploid, diploid, and polyploid strains of the human fungal pathogen Candida albicans under three different nutrient limitation environments to test whether these conditions, hypothesized to select for low ploidy levels, could counteract ploidy drive. Strains generally maintained or acquired smaller genome sizes size (measured as total nuclear DNA through flow cytometry) in minimal medium and under phosphorus depletion compared to in a complete medium, while mostly maintained or acquired increased genome sizes under nitrogen depletion. Improvements in fitness often ran counter to changes in genome size; in a number of scenarios lines that maintained their original genome size often increased in fitness more than lines that converged towards diploidy. Combined, this work demonstrates a role for both the environment and genotype in determination of the rate of ploidy drive, and highlights questions that remain about the force(s) that cause genome size variation.
Data from: Evolutionary rescue and local adaptation under different rates of temperature increase: a combined analysis of changes in phenotype expression and genotype frequency in Paramecium microcosms
Evolutionary Rescue (ER) occurs when populations, which have declined due to rapid environmental change, recover through genetic adaptation. The success of this process and the evolutionary trajectory of the population strongly depend on the rate of environmental change. Here we investigated how different rates of temperature increase (from 23°C to 32°C) affect population persistence and evolutionary change in experimental microcosms of the protozoan Paramecium caudatum. Consistent with theory on ER, we found that those populations experiencing the slowest rate of temperature increase were the least likely to become extinct and tended to be the best adapted to the new temperature environment. All high-temperature populations were more tolerant to severe heat stress (35°C, 37°C), indicating a common mechanism of heat protection. High-temperature populations also had superior growth rates at optimum temperatures, leading to the absence of a pattern of local adaptation to control (23°C) and high-temperature (32°C) environments. However, high-temperature populations had reduced growth at low temperatures (5-9°C), causing a shift in the temperature niche. In part, the observed evolutionary change can be explained by selection from standing variation. Using mitochondrial markers, we found complete divergence between control and high-temperature populations in the frequencies of six initial founder genotypes. Our results confirm basic predictions of ER and illustrate how adaptation to an extreme local environment can produce positive as well as negative correlated responses to selection over the entire range of the ecological niche.
Data from: Meta‐analysis of chromosome‐scale crossover rate variation in eukaryotes and its significance to evolutionary genomics
Understanding the distribution of crossovers along chromosomes is crucial to evolutionary genomics because the crossover rate determines how strongly a genome region is influenced by natural selection. Nevertheless, generalities in the chromosome-scale distribution of crossovers have not been investigated formally. We fill this gap by synthesizing joint information on genetic and physical maps across 62 animal, plant, and fungal species. Our quantitative analysis reveals a strong and taxonomically wide-spread reduction of the crossover rate in the center of chromosomes relative to their peripheries. We demonstrate that this pattern is poorly explained by the position of the centromere, but find that the magnitude of the relative reduction in the crossover rate in chromosome centers increases with chromosome length. That is, long chromosomes often display a dramatically low crossover rate in their center whereas short chromosomes exhibit a relatively homogeneous crossover rate. This observation is compatible with a model in which crossovers are initiated from the chromosome tips, an idea with preliminary support from mechanistic investigations of meiotic recombination. Consequently, we show that organisms achieve a higher genome-wide crossover rate by evolving smaller chromosomes. Summarizing theory and providing empirical examples, we finally highlight that taxonomically wide-spread and systematic heterogeneity in crossover rate along chromosomes generates predictable broad-scale trends in genetic diversity and population differentiation by modifying the impact of natural selection among regions within a genome. We conclude by emphasizing that chromosome-scale heterogeneity in crossover rate should urgently be incorporated into analytical tools in evolutionary genomics, and in the interpretation of emerging patterns.
Data from: Diversity-dependent evolutionary rates in early Paleozoic zooplankton
The extent to which biological diversity affects rates of diversification is central to understanding macroevolutionary dynamics, yet no consensus has emerged on the importance of diversity-dependence of evolutionary rates. Here we analyse the species-level fossil record of early Paleozoic graptoloids, documented with high temporal resolution, to test directly whether rates of diversification were influenced by levels of standing diversity within this major clade of marine zooplankton. To circumvent the statistical regression-to-the-mean artefact, whereby higher- and lower-than-average values of diversity tend to be followed by negative and positive diversification rates, we construct a non-parametric, empirically scaled, diversity-independent null model by randomizing the observed diversification rates with respect to time. Comparing observed correlations between diversity and diversification rate to those expected from this diversity-independent model, we find evidence for negative diversity-dependence, accounting for up to 12% of the variance in diversification rate, with maximal correlation at a temporal lag of ~1 million years. Diversity-dependence persists throughout the Ordovician and Silurian, despite a major increase in the strength and frequency of extinction and speciation pulses in the Silurian. In contrast to some previous work, we find that diversity-dependence affects rates of speciation and extinction nearly equally on average, although subtle differences emerge when we compare the Ordovician and Silurian.
Data from: Is specialization an evolutionary dead-end? Testing for differences in speciation, extinction and trait transition rates across diverse phylogenies of specialists and generalists.
Specialization has often been claimed to be an evolutionary dead end, with specialist lineages having a reduced capacity to persist or diversify. In a phylogenetic comparative framework, an evolutionary dead end may be detectable from the phylogenetic distribution of specialists, if specialists rarely give rise to large, diverse clades. Previous phylogenetic studies of the influence of specialization on macroevolutionary processes have demonstrated a range of patterns, including examples where specialists have both higher and lower diversification rates than generalists, as well as examples where the rates of evolutionary transitions from generalists to specialists are higher, lower or equal to transitions from specialists to generalists. Here, we wish to ask whether these varied answers are due to the differences in macroevolutionary processes in different clades, or partly due to differences in methodology. We analysed ten phylogenies containing multiple independent origins of specialization and quantified the phylogenetic distribution of specialists by applying a common set of metrics to all datasets. We compared the tip branch lengths of specialists to generalists, the size of specialist clades arising from each evolutionary origin of a specialized trait and whether specialists tend to be clustered or scattered on phylogenies. For each of these measures, we compared the observed values to expectations under null models of trait evolution and expected outcomes under alternative macroevolutionary scenarios. We found that specialization is sometimes an evolutionary dead end: in two of the ten case studies (pollinator-specific plants and host-specific flies), specialization is associated with a reduced rate of diversification or trait persistence. However, in the majority of studies, we could not distinguish the observed phylogenetic distribution of specialists from null models in which specialization has no effect on diversification or trait persistence.
Data from: Rate of evolutionary change in cranial morphology of the marsupial genus Monodelphis is constrained by the availability of additive genetic variation
We tested the hypothesis that the rate of marsupial cranial evolution is dependent on the distribution of genetic variation in multivariate space. To do so, we carried out a genetic analysis of cranial morphological variation in laboratory strains of Monodelphis domestica and used estimates of genetic covariation to analyze the morphological diversification of the Monodelphis brevicaudata species group. We found that within-species genetic variation is concentrated in only a few axes of the morphospace and that this strong genetic covariation influenced the rate of morphological diversification of the brevicaudata group, with between-species divergence occurring fastest when occurring along the genetic line of least resistance. Accounting for the geometric distribution of genetic variation also increased our ability to detect the selective regimen underlying species diversification, with several instances of selection only being detected when genetic covariances were taken into account. Therefore, this work directly links patterns of genetic covariation among traits to macroevolutionary patterns of morphological divergence. Our findings also suggest that the limited distribution of Monodelphis species in morphospace is the result of a complex interplay between the limited dimensionality of available genetic variation and strong stabilizing selection along two major axes of genetic variation.
Data from: Population persistence under high mutation rate: from evolutionary rescue to lethal mutagenesis
Populations may genetically adapt to severe stress that would otherwise cause their extirpation. Recent theoretical work, combining stochastic demography with Fisher's Geometric Model of adaptation, has shown how evolutionary rescue becomes unlikely beyond some critical intensity of stress. Increasing mutation rates may however allow adaptation to more intense stress, raising concerns about the effectiveness of treatments against pathogens. This previous work assumes that populations are rescued by the rise of a single resistance mutation. However, even in asexual organisms, rescue can also stem from the accumulation of multiple mutations in a single genome. Here, we extend this model to study the rescue process in an asexual population where the mutation rate is sufficiently high so that such events may be common. We predict both the ultimate extinction probability of the population and the distribution of extinction times. We compare the accuracy of different approximations covering a large range of mutation rates. Moderate increase in mutation rates favors evolutionary rescue. However, larger increase leads to extinction by the accumulation of a large mutation load, a process called lethal mutagenesis. We discuss how these results could help design "evolution-proof" anti-pathogen treatments that even highly mutable strains could not overcome.
Data from: Investigating the timing of origin and evolutionary processes shaping regional species diversity: insights from simulated data and Neotropical butterfly diversification rates
Different diversification scenarios have been proposed to explain the origin of extant biodiversity. However, most existing meta-analyses of time-calibrated phylogenies rely on approaches that do not quantitatively test alternative diversification processes. Here, I highlight the shortcomings of using species divergence ranks, which is a method widely used in meta-analyses. Divergence ranks consist of categorizing cladogenetic events to certain periods of time, typically to either Pleistocene or to pre-Pleistocene ages. This approach has been claimed to shed light on the origin of most extant species and the timing and dynamics of diversification in any biogeographical region. However, interpretations drawn from such method often confound two fundamental questions in macroevolutionary studies, tempo (timing of evolutionary rate shifts) and mode ("how" and "why" of speciation). By using simulated phylogenies under four diversification scenarios, constant-rate, diversity-dependence, high extinction, and high speciation rates in the Pleistocene, I showed that interpretations based on species divergence ranks might have been seriously misleading. Future meta-analyses of dated phylogenies need to be aware of the impacts of incomplete taxonomic sampling, tree topology, and divergence time uncertainties, as well as they might be benefited by including quantitative tests of alternative diversification models that acknowledge extinction and diversity dependence.
Data from: Relationships of diversity, disparity and their evolutionary rates in squirrels (Sciuridae)
Several theories predict that rapidly diversifying clades will also rapidly diverge phenotypically; yet, there are also reasons for suspecting that diversification and divergence might not be correlated. In the widely distributed squirrel clade (Sciuridae), we test for correlations between per-lineage speciation rates, species richness, disparity and a time-invariant measure of disparity that allows for comparing rates when evolutionary modes differ, as they do in squirrels. We find that species richness and speciation rates are not correlated with clade age or with each other. Disparity appears to be positively correlated with clade age because young, rapidly diversifying Nearctic grassland clades are strongly pulled to a single stable optimum but older, slowly diversifying Paleotropical forest clades contain lineages that diverge along multiple ecological and morphological lines. That contrast is likely due to both the environments they inhabit and their phylogenetic community structure. Our results argue against a shared explanation for diversity and disparity in favor of geographically mediated modes of speciation and ecologically mediated modes of phenotypic evolution.
Data from: A call for more transparent reporting of error rates: the quality of AFLP data in ecological and evolutionary research
Despite much discussion of the importance of quantifying and reporting genotyping error in molecular studies, it is still not standard practice in the literature. This is particularly a concern for amplified fragment length polymorphism (AFLP) studies, where differences in laboratory, peak-calling and locus-selection protocols can generate data sets varying widely in genotyping error rate, the number of loci used and potentially estimates of genetic diversity or differentiation. In our experience, papers rarely provide adequate information on AFLP reproducibility, making meaningful comparisons among studies difficult. To quantify the extent of this problem, we reviewed the current molecular ecology literature (470 recent AFLP articles) to determine the proportion of studies that report an error rate and follow established guidelines for assessing error. Fifty-four per cent of recent articles do not report any assessment of data set reproducibility. Of those studies that do claim to have assessed reproducibility, the majority (~90%) either do not report a specific error rate or do not provide sufficient details to allow the reader to judge whether error was assessed correctly. Even of the papers that do report an error rate and provide details, many (≥23%) do not follow recommended standards for quantifying error. These issues also exist for other marker types such as microsatellites, and next-generation sequencing techniques, particularly those which use restriction enzymes for fragment generation. Therefore, we urge all researchers conducting genotyping studies to estimate and more transparently report genotyping error using existing guidelines and encourage journals to enforce stricter standards for the publication of genotyping studies.
Data from: High mutation rates limit evolutionary adaptation in Escherichia coli
Mutation is fundamental to evolution, because it generates the genetic variation on which selection can act. In nature, genetic changes often increase the mutation rate in systems that range from viruses and bacteria to human tumors. Such an increase promotes the accumulation of frequent deleterious or neutral alleles, but it can also increase the chances that a population acquires rare beneficial alleles. Here, we study how up to 100-fold increases in Escherichia coli's genomic mutation rate affect adaptive evolution. To do so, we evolved multiple replicate populations of asexual E. coli strains engineered to have four different mutation rates for 3000 generations in the laboratory. We measured the ability of evolved populations to grow in their original environment and in more than 90 novel chemical environments. In addition, we subjected the populations to whole genome population sequencing. Although populations with higher mutation rates accumulated greater genetic diversity, this diversity conveyed benefits only for modestly increased mutation rates, where populations adapted faster and also thrived better than their ancestors in some novel environments. In contrast, some populations at the highest mutation rates showed reduced adaptation during evolution, and failed to thrive in all of the 90 alternative environments. In addition, they experienced a dramatic decrease in mutation rate. Our work demonstrates that the mutation rate changes the global balance between deleterious and beneficial mutational effects on fitness. In contrast to most theoretical models, our experiments suggest that this tipping point already occurs at the modest mutation rates that are found in the wild.
Data from: Phylogenetic ANCOVA: estimating changes in evolutionary rates as well as relationships between traits
We present a new phylogenetic comparative method—phylogenetic analysis of covariance (PANCOVA)—that uses interspecific data and a phylogeny to estimate the effects of major events on both the rate of phenotypic evolution and the association between traits. It could be used, for example, to model the impact of a key innovation, colonization of a new habitat, or environmental change. The approach is optimized with maximum likelihood and is formulated under the familiar phylogenetic generalized least squares framework, which is flexible and easily extended to incorporate other factors and parameters. As an example, we explore the relationship between parental investment and relative telencephalon size in birds and contrast the results of PANCOVA with those from other phylogenetic comparative methods.
Evolutionary rates are correlated between cockroach symbiont and mitochondrial genomes
<p>Bacterial endosymbionts evolve under strong host-driven selection. Factors influencing host evolution might affect symbionts in similar ways, potentially leading to correlations between the molecular evolutionary rates of hosts and symbionts. Although there is evidence of rate correlations between mitochondrial and nuclear genes, similar investigations of hosts and symbionts are lacking. Here we demonstrate a correlation in molecular rates between the genomes of an endosymbiont (<i>Blattabacterium cuenoti</i>) and the mitochondrial genomes of their hosts (cockroaches). We used partial genome data for multiple strains of <i>B. cuenoti</i>to compare phylogenetic relationships and evolutionary rates for 55 cockroach/symbiont pairs. The phylogenies inferred for <i>B. cuenoti </i>and the mitochondrial genomes of their hosts were largely congruent, as expected from their identical maternal and cytoplasmic mode of inheritance. We found a correlation between evolutionary rates of the two genomes, based on comparisons of root-to-tip distances and on comparisons of branch lengths of phylogenetically independent species pairs. Our results underscore the profound effects that long-term symbiosis can have on the biology of each symbiotic partner.</p>
Data from: Mechanistic model of evolutionary rate variation en route to a nonphotosynthetic lifestyle in plants
Because novel environmental conditions alter the selection pressure on genes or entire subgenomes, adaptive and nonadaptive changes will leave a measurable signature in the genomes, shaping their molecular evolution. We present herein a model of the trajectory of plastid genome evolution under progressively relaxed functional constraints during the transition from autotrophy to a nonphotosynthetic parasitic lifestyle. We show that relaxed purifying selection in all plastid genes is linked to obligate parasitism, characterized by the parasite's dependence on a host to fulfill its life cycle, rather than the loss of photosynthesis. Evolutionary rates and selection pressure coevolve with macrostructural and microstructural changes, the extent of functional reduction, and the establishment of the obligate parasitic lifestyle. Inferred bursts of gene losses coincide with periods of relaxed selection, which are followed by phases of intensified selection and rate deceleration in the retained functional complexes. Our findings suggest that the transition to obligate parasitism relaxes functional constraints on plastid genes in a stepwise manner. During the functional reduction process, the elevation of evolutionary rates reaches several new rate equilibria, possibly relating to the modified protein turnover rates in heterotrophic plastids.
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