Biology subjects

Salamin, N.

Publications and source records attributed to Salamin, N..

At least 37 records · Page 2Linked to original sources

bioRxiv2023

Mammalian protein-coding genes exhibit widespread beneficial mutations that are not adaptive

Mutations can be beneficial by bringing innovation to their bearer, allowing them to adapt to environmental change. These mutations are typically unpredictable since they respond to an unforeseen change in the environment. However, mutations can also be beneficial because they are simply restoring a state of higher fitness that was lost due to genetic drift in a stable environment. In contrast to adaptive mutations, these beneficial non-adaptive mutations can be predicted if the underlying fitness landscape is stable and known. The contribution of such non-adaptive mutations to molecular evolution has been widely neglected mainly because their detection is very challenging. We have here reconstructed protein-coding-gene fitness landscapes shared between mammals, using mutation-selection models and a multi-species alignments across 87 mammals. These fitness landscapes have allowed us to predict the fitness effect of polymorphisms found in 28 mammalian populations. Using methods that quantify selection at the population level, we have confirmed that beneficial non-adaptive mutations are indeed positively selected in extant populations. Our work confirms that deleterious substitutions are accumulating in mammals and are being reverted, generating a balance in which genomes are damaged and restored simultaneously at different loci. We observe that beneficial non-adaptive mutations represent between 15% and 45% of all beneficial mutations in 24 of 28 populations analyzed, suggesting that a substantial part of ongoing positive selection is not driven solely by adaptation to environmental change in mammals. Significance statementThe extent to which adaptation to changing environments is shaping genomes is a central question in molecular evolution. To quantify the rate of adaptation, population geneticists have typically used signatures of positive selection. However, mutations restoring an ancestral state of higher fitness lost by genetic drift are also positively selected, but they do not respond to a change in the environment. In this study, we have managed to distinguish beneficial mutations that are due to changing environments and those that are restoring pre-existing functions in mammals. We show that a substantial proportion of beneficial mutations cannot be interpreted as adaptive.

evolutionary biology↗

bioRxiv2023

Implementation of biotic interactions in niche analyses unravels the patterns underneath community composition in clownfishes

Biotic interactions shape the ecology of species and communities, yet their integration into ecological niche modeling methods remains challenging. Despite being a central topic of research for the past decade, the impact of biotic interactions on species distributions and community composition is often overlooked. Mutualistic systems offer ideal case studies for examining the effects of biotic I nteractions on species niches and community dynamics. This study presents a novel approach to incorporating mutualistic interactions into niche modeling, using the clownfish-sea anemone system. By adapting existing niche quantification frameworks, we developed a method to estimate the partial effects of known interactions and refine ecological niche estimates. This approach allows for a more comprehensive understanding of how mutualistic relationships influence species distributions and community assembly patterns. We also used mutualistic information to investigate the resource-use overlap, identitying patterns of competition within clownfish communities. Our results reveal significant deviations in niche estimates when biotic interactions are considered, particularly for specialist species. Host partitioning among clownfish species reduces resource-use overlap, facilitating coexistence in species-rich habitats and highlighting mutualisms role in promoting and maintaining diversity. We uncover complex dynamics in resource-use overlap among clownfish species, influenced by factors such as species richness, ecological niche overlap, and host specialization. Specialist-generalist interactions strike an optimal balance, supporting high species richness while minimizing competition. These insights enhance our understanding of clownfish biodiversity patterns, demonstrating how diverse mutualistic strategies contribute to diversity build-up and mitigate competitive exclusion in saturated communities. The analytical framework presented has broad applications beyond the clownfish-sea anemone system, potentially extending to a broader range of interactions. It enables a more comprehensive understanding of biodiversity maintenance in complex ecosystems and constitutes a valuable tool for conservation planning and ecosystem management.

ecology↗

bioRxiv2023

Exploring the Macroevolutionary Signature of Asymmetric Inheritance at Speciation

AO_SCPLOWBSTRACTC_SCPLOWPopular comparative phylogenetic models such as Brownian Motion, Ornstein-Ulhenbeck, and their extensions, assume that, at speciation, a trait value is inherited identically by the two descendant species. This assumption contrasts with models of speciation at the micro-evolutionary scale where phenotypic distributions of the descendants are sub-samples of the ancestral distribution. Various described mechanisms of speciation can lead to a displacement of the ancestral phenotypic mean among descendants and an asymmetric inheritance of the ancestral phenotypic variance. In contrast, even macro-evolutionary models that account for intraspecific variance assume symmetrically conserved inheritance of the ancestral phenotypic distribution at speciation. Here we develop an Asymmetric Brownian Motion model (ABM) that relaxes the hypothesis of symmetric and conserved inheritance of the ancestral distribution at the time of speciation. The ABM jointly models the evolution of both intra- and inter-specific phenotypic variation. It also allows the mode of phenotypic inheritance at speciation to be inferred, ranging from a symmetric and conserved inheritance, where descendants inherit the ancestral distribution, to an asymmetric and displaced inheritance, where descendants inherit divergent phenotypic means and variances. To demonstrate this model, we analyze the evolution of beak morphology in Darwin finches, finding evidence of character displacement at speciation. The ABM model helps to bridge micro- and macro-evolutionary models of trait evolution by providing a more robust framework for testing the effects of ecological speciation, character displacement, and niche partitioning on trait evolution at the macro-evolutionary scale.

evolutionary biology↗

bioRxiv2022

Extensive hybridisation throughout clownfishes evolutionary history

The contribution of hybridisation in the generation of global species diversity has long been controversial among evolutionary biologists. However, it is now increasingly accepted that hybridisation has many impacts on the process of speciation. Notably, it is an important mechanism fostering adaptive radiation since it can generate new phenotypic combinations enabling the occupancy of new niches. Here, we focused on clownfish (Pomacentridae), a clade of 28 coral reef fishes displaying a mutualistic interaction with sea anemones. This behaviour is the key innovation that triggered adaptive radiation of clownfishes, as each species is able to occupy a different combination of host anemone species and habitat. Previous work suggested that hybridisation might be responsible for the extant diversity of clownfish species. To test this hypothesis, we analysed whole-genome datasets for each clownfish species. First, we reconstructed the phylogeny of the clade based on topology weighting methods, which enables the visualisation of the relationships between taxa across the genome. Then, we highlighted possible ancient hybridisation events based on a comparative genomic framework for detecting introgression in genomes. The resulting phylogeny is consistent with previous works based on a few mitochondrial and nuclear genes, and shallow nodes are now well supported in contrast to past studies. Furthermore, we detected multiple past hybridisation events throughout the evolutionary history of clownfishes, corroborating the potential role of hybridisation in the clownfish adaptive radiation. This study adds to the growing number of studies investigating the genomic mechanisms behind species diversification, drawing us closer to understanding how Earth biodiversity is generated.

evolutionary biology↗

bioRxiv2022

Insights into the genomics of clownfish adaptive radiation: the genomic substrate of the diversification

Clownfishes are an iconic group of coral reef fishes that evolved a mutualistic interaction with sea anemones, which triggered the rapid diversification of the group. We investigated the genomic architecture underlying this process to determine the genomic characteristics associated with the adaptive radiation of the group and assess the mechanisms of parallel evolution in clownfishes. We took advantage of the available genomic data of five pairs of closely related but ecologically divergent clownfish species to perform comparative genomic analyses. We found that clownfish genomes show two bursts of transposable elements, overall accelerated coding evolution, and topology inconsistencies potentially resulting from hybridization events. These characteristics possibly facilitated the rapid diversification of the group. We also detected a signature of positive selection throughout the radiation in 5.4 % of the clownfish genes. Among them, five presented functions associated with social behavior and ecology. They could have potentially played a role in the evolution of size-based hierarchical social structure so particular to clownfishes. Finally, we found genes with patterns of either relaxation or intensification of purifying selection and signals of positive selection linked with clownfish ecological divergence, suggesting some level of parallel evolution during the diversification of the group. Altogether, these results provide the first insights into the genomic substrate of clownfish adaptive radiation. This work integrates the growing collection of studies investigating the genomic mechanisms governing species diversification, which brings us a step closer to understanding how biodiversity on Earth is created

evolutionary biology↗

bioRxiv2020

Shedding light on the underlying characteristics of genomes using Kronecker model families of codon evolution

The mechanistic models of codon evolution rely on some simplistic assumptions in order to reduce the computational complexity of estimating the high number of parameters of the models. This paper is an attempt to investigate how much these simplistic assumptions are misleading when they violate the nature of the biological dataset in hand. We particularly focus on three simplistic assumptions made by most of the current mechanistic codon models including: 1) only single substitutions between nucleotides within codons in the codon transition rate matrix are allowed. 2) mutation is homogenous across nucleotides within a codon. 3) assuming HKY nucleotide model is good enough at the nucleotide level. For this purpose, we developed a framework of mechanistic codon models, each model in the framework hold or relax some of the mentioned simplifying assumptions. Holding or relaxing the three simplistic assumptions results in total to eight different mechanistic models in the framework. Through several experiments on biological datasets and simulations we show that the three simplistic assumptions are unrealistic for most of the biological datasets and relaxing these assumptions lead to accurate estimation of evolutionary parameters such as selection pressure.

bioinformatics↗

bioRxiv2020

A cautionary note on the use of haplotype callers in Phylogenomics

Next-generation-sequencing haplotype callers are commonly used in studies to call variants from newly-sequenced species. However, due to the current availability of genomic resources, it is still common practice to use only one reference genome for a given genus, or even one reference for an entire clade of a higher taxon. The problem with traditional haplotype callers such as the one from GATK, is that they are optimized for variant calling at the population level, but not at the phylogenetic level. Thus, the consequences for downstream analyses can be substantial. Here, through simulations, we compare the performance between the haplotype callers of GATK and ATLAS, and present their differences at various phylogenetic scales. We show how the haplotype caller of GATK substantially underestimates the number of variants at the phylogenetic level, but not at the population level. We also quantified the level at which the accuracy of heterozygote calls declines with increasing distance to the reference genome. Such decrease is very sharp in GATK, while ATLAS maintains a high accuracy in variant calling, even at moderately-divergent species from the reference. We further suggest that efforts should be taken towards acquiring more reference genomes per species, before pursuing high-scale phylogenomic studies.

evolutionary biology↗

bioRxiv2019

Prototypic SNARE proteins are encoded in the genomes of Heimdallarchaeota, potentially bridging the gap between the prokaryotes and eukaryotes

A defining feature of eukaryotic cells is the presence of numerous membrane-bound organelles that subdivide the intracellular space into distinct compartments. How the eukaryotic cell acquired its internal complexity is still poorly understood. Material exchange among most organelles occurs via vesicles that bud off from a source and specifically fuse with a target compartment. Central players in the vesicle fusion process are the Soluble N-ethylmaleimide-sensitive factor Attachment protein REceptor (SNARE) proteins. These small tail-anchored (TA) membrane proteins zipper into elongated four-helix bundles that pull membranes together1-3. SNARE proteins are highly conserved among eukaryotes but are thought to be absent in prokaryotes. Here, we identified SNARE-like factors in the genomes of uncultured organisms of Asgard archaea of the Heimdallarchaeota clade4,5, which are thought to be the closest living relatives of eukaryotes. Biochemical experiments show that the archaeal SNARE-like proteins can interact with eukaryotic SNARE proteins. We did not detect SNAREs in -proteobacteria, the closest relatives of mitochondria, but identified several genes encoding for SNARE proteins in {gamma}-proteobacteria of the order Legionellales, pathogens that live inside eukaryotic cells. Very probably, their SNAREs stem from lateral gene transfer from eukaryotes. Together, this suggests that the diverse set of eukaryotic SNAREs evolved from an archaeal precursor. However, whether Heimdallarchaeota actually have a simplified endomembrane system will only be seen when we succeed studying these organisms under the microscope.

evolutionary biology↗

bioRxiv2019

On the effect of asymmetrical trait inheritance on models of trait evolution

Current phylogenetic comparative methods modeling quantitative trait evolution generally assume that, during speciation, phenotypes are inherited identically between the two daughter species. This, however, neglects the fact that species consist of a set of individuals, each bearing its own trait value. Indeed, because descendent populations after speciation are samples of a parent population, we can expect their mean phenotypes to randomly differ from one another potentially generating a "jump" of mean phenotypes due to asymmetrical trait inheritance at cladogenesis. Here, we aim to clarify the effect of asymmetrical trait inheritance at speciation on macroevolutionary analyses, focusing on model testing and parameter estimation using some of the most common models of quantitative trait evolution. We developed an individual-based simulation framework in which the evolution of species phenotypes is determined by trait changes at the individual level accumulating across generations and cladogenesis occurs then by separation of subsets of the individuals into new lineages. Through simulations, we assess the magnitude of phenotypic jumps at cladogenesis under different modes of trait inheritance at speciation. We show that even small jumps can strongly alter both the results of model selection and parameter estimations, potentially affecting the biological interpretation of the estimated mode of evolution of a trait. Our results call for caution when interpreting analyses of trait evolution, while highlighting the importance of testing a wide range of alternative models. In the light of our findings, we propose that future methodological advances in comparative methods should more explicitly model the intra-specific variability around species mean phenotypes and how it is inherited at speciation.

evolutionary biology↗

bioRxiv2019

Convergent changes in gene expression associated with repeated transitions between hummingbird and bee pollinated flowers

The repeated evolution of convergent floral shapes and colors in angiosperms has been largely interpreted as the response to pollinator-mediated selection to maximize attraction and efficiency of specific groups of pollinators. The genetic mechanisms contributing to certain flower traits have been studied in detail for model system species, but the extent by which flowers are free to vary and how predictable are the genetic changes underlying flower adaptation to pollinator shifts still remain largely unknown.\n\nHere, we aimed at detecting the genetic basis of the repeated evolution of flower phenotypes associated with pollinator shifts. We assembled and compared de novo transcriptomes of three phylogenetic independent pairs of Gesneriaceae species, each with contrasting flower phenotype adapted to either bee or hummingbird pollination. We assembled and analyzed a total of 14,059 genes and we showed that changes in expression in 550 of them was associated with the pollination syndromes. Among those, we observed genes with function linked to floral color, scent, shape and symmetry, as well as nectar composition. These genes represent candidates genes involved in the build-up of the convergent floral phenotypes.\n\nThis study provides the first insights into the molecular mechanisms underlying the repeated evolution of pollination syndromes. Although the presence of additional lineage-specific responses cannot be excluded, these results suggest that the convergent evolution of genes expression is involved in the convergent build-up of the pollination syndromes. Future studies aiming to directly manipulate certain genes will integrate our knowledge on the key genes for floral transitions and the pace of floral evolution.\n\nData availabilityRaw Illumina reads will be available in the Sequence Read Archive (SRA) in NCBI database. The assembled transcriptomes and their annotation will by available in DRYAD repository. Details and accession ID will be provided at the time of the manuscript acceptance.

evolutionary biology↗

bioRxiv2019

Functional diversification enabled grassy biomes to fill global climate space

Global change impacts on the Earth System are typically evaluated using biome classifications based on trees and forests. However, during the Cenozoic, many terrestrial biomes were transformed through the displacement of trees and shrubs by grasses. While grasses comprise 3% of vascular plant species, they are responsible for more than 25% of terrestrial photosynthesis. Critically, grass dominance alters ecosystem dynamics and function by introducing new ecological processes, especially surface fires and grazing. However, the large grassy component of many global biomes is often neglected in their descriptions, thereby ignoring these important ecosystem processes. Furthermore, the functional diversity of grasses in vegetation models is usually reduced to C3 and C4 photosynthetic plant functional types, omitting other relevant traits. Here, we compile available data to determine the global distribution of grassy vegetation and key traits related to grass dominance. Grassy biomes (where > 50% of the ground layer is covered by grasses) occupy almost every part of Earths vegetated climate space, characterising over 40% of the land surface. Major evolutionary lineages of grasses have specialised in different environments, but species from only three grass lineages occupy 88% of the land area of grassy vegetation, segregating along gradients of temperature, rainfall and fire. The environment occupied by each lineage is associated with unique plant trait combinations, including C3 and C4 photosynthesis, maximum plant height, and adaptations to fire and aridity. There is no single global climatic limit where C4 grasses replace C3 grasses. Instead this ecological transition varies biogeographically, with continental disjunctions arising through contrasting evolutionary histories.\n\nSignificance statementWorldviews of vegetation generally focus on trees and forests but grasses characterize the ground layer over 40% of the Earths vegetated land surface. This omission is important because grasses transform surface-atmosphere exchanges, biodiversity and disturbance regimes. We looked beneath the trees to produce the first global map of grass-dominated biomes. Grassy biomes occur in virtually every climate on Earth. However, three lineages of grasses are much more successful than others, characterizing 88% of the land area of grassy biomes. Each of these grass lineages evolved ecological specializations related to aridity, freezing and fire. Recognizing the extent and causes of grass dominance beneath trees is important because grassy vegetation plays vital roles in the dynamics of our biosphere and human wellbeing.

ecology↗

bioRxiv2019

Evolution of life cycles and reproductive traits: insights from 1 the brown algae

Brown algae are characterized by a remarkable diversity of life cycles, sexual systems, and reproductive modes, and these traits seem to be very labile across the whole group. This diversity makes them ideal models to test existing theories on the evolution of alternation between generations, and to examine correlations between life cycle and reproductive life history traits. In this study, we investigate the dynamics of trait evolution for four life-history traits: life cycle, sexual system, level of gamete dimorphism and gamete parthenogenetic capacity. We assign states to up to 70 species in a multi-gene phylogeny of brown algae, and use maximum likelihood and Bayesian analyses of correlated evolution, taking phylogeny into account, to test for correlations between life history traits and sexual systems, and to investigate the sequence of trait acquisition. Our analyses are consistent with the prediction that diploid growth may evolve because it allows the complementation of deleterious mutations, and that haploid sex determination is ancestral in relation to diploid sex determination. However, the idea that increased zygotic and diploid growth is associated with increased sexual dimorphism is not supported by our analysis. Finally, it appears that in the brown algae isogamous species evolved from anisogamous ancestors.

evolutionary biology↗

bioRxiv2018

Genomic footprints of repeated evolution of CAM photosynthesis in tillandsioid bromeliads

The adaptive radiation of Bromeliaceae (pineapple family) is one of the most diverse among Neotropical flowering plants. Diversification in this group was facilitated by several key innovations including the transition from C3 to CAM photosynthesis. We used a phylogenomic approach complemented by differential gene expression (RNA-seq) and targeted metabolite profiling to address the patterns and mechanisms of C3/CAM evolution in the extremely species-rich bromeliad genus Tillandsia and related taxa. Evolutionary analyses at a range of different levels (selection on protein-coding genes, gene duplication and loss, regulatory evolution) revealed three common themes driving the evolution of CAM: response to heat and drought, alterations to basic carbohydrate metabolism, and regulation of organic acid storage. At the level of genes and their products, CAM/C3 shifts were accompanied by gene expansion of a circadian regulator, re-programming of ABA-related gene expression, and adaptive sequence evolution of an enolase, effectively linking carbohydrate metabolism to ABA-mediated stress response. These changes include several pleiotropic regulators, which facilitated the evolution of correlated adaptive traits during a textbook adaptive radiation.

genomics↗

bioRxiv2018

Linking micro and macroevolution in the presence of migration

1. The process of speciation is of key importance in evolutionary biology because it shapes macroevolutionary patterns. This process starts at the microevolutionary level, for instance, when two subpopulations evolve towards different phenotypic optima. The speed at which these optima are reached is controlled by the degree of stabilising selection, which pushes a mean trait towards an optimum within subpopulations, and ongoing migration that pulls the mean phenotype away from that optimum. Traditionally, macro phenotypic evolution with selection has been modelled by Ornstein-Uhlenbeck (OU) processes, but these models have ignored the role of migration within species.\n\n2. Here, our goal is to reconcile the processes of micro and macroevolution by modelling migration during speciation. More precisely, we introduce an OU model where migration happens between two subpopulations within a branch of a phylogeny and this migration decreases over time as it happens during speciation. We then use this model to study the evolution of trait means along a phylogeny, as well as the way phenotypic disparity between species changes with successive epochs.\n\n3. We show that ignoring the effect of migration in sampled time-series data leads to a significant underestimation of the selective forces acting upon it. We also show that migration decreases the expected phenotypic disparity between species and we show the effect of migration in the particular case of niche filling. We further introduce a method to jointly estimate selection and migration from time-series data.\n\n4. Our model extends standard results of interactions selection-migration in a microevolutionary time frame across multiple speciation events at a macroevolutionary scale. Our results further proof that not accounting for gene flow has important consequences in inferences at both the micro and macroevolutionary scale.

evolutionary biology↗

bioRxiv2018

Improved estimation of macroevolutionary rates from fossil data using a Bayesian framework

The estimation of origination and extinction rates and their temporal variation is central to understanding diversity patterns and the evolutionary history of clades. The fossil record provides the most direct evidence of extinction and biodiversity changes through time and has long been used to infer the dynamics of diversity changes in deep time. The software PyRate implements a Bayesian framework to analyze fossil occurrence data to estimate the rates of preservation, origination and extinction while incorporating several sources of uncertainty. This fully probabilistic approach allows us to explicitly assess the statistical support of alternative macroevolutionary hypotheses and to infer credible intervals around parameter estimates. Here, we present a major update of the software, which implements substantial methodological advancements, including more complex and realistic models of preservation, a reversible jump Markov chain Monte Carlo algorithm to estimate origination and extinction rates and their temporal variation, and a substantial boost in performance. We demonstrate the new functionalities through extensive simulations and with the analysis of a large dataset of Cenozoic marine mammals. We identify several significant shifts in origination and extinction rates of marine mammals, underlying a late Miocene diversity peak and a subsequent 50% diversity decline towards the present. Our analyses indicate that explicit statistical model testing, which is often neglected in fossil-based macroevolutionary analyses, is crucial to obtain accurate and robust results. PyRate provides a flexible, statistically sound analytical framework, which we think can serve as a useful toolkit for many future studies in paleobiology.

paleontology↗

bioRxiv2017

First draft genome assembly of an iconic clownfish species (Amphiprion frenatus)

Clownfishes (or anemonefishes) form an iconic group of coral reef fishes, particularly known for their mutualistic interaction with sea anemones. They are characterized by particular life history traits, such as a complex social structure and mating system involving sequential hermaphroditism, coupled with an exceptionally long lifespan. Additionally, clownfishes are considered to be one of the rare group to have experienced an adaptive radiation in the marine environment.\n\nHere, we assembled and annotated the first genome of a clownfish species, the tomato clownfish (Amphiprion frenatus). We obtained a total of 17,801 assembled scaffolds, containing a total of 26,917 genes. The completeness of the assembly and annotation was satisfying, with 96.5% of the Actinopterygii BUSCOs (Benchmarking Universal Single-Copy Orthologs) being retrieved in A. frenatus assembly. The quality of the resulting assembly is comparable to other bony fish assemblies.\n\nThis resource is valuable for the advancing of studies of the particular life-history traits of clownfishes, as well as being useful for population genetic studies and the development of new phylogenetic markers. It will also open the way to comparative genomics. Indeed, future genomic comparison among closely related fishes may provide means to identify genes related to the unique adaptations to different sea anemone hosts, as well as better characterize the genomic signatures of an adaptive radiation.

genomics↗

bioRxiv2017

Evolutionary history of New World monkeys revealed by molecular and fossil data

New World monkeys (parvorder Platyrrhini) are one of the most diverse groups of primates, occupying today a wide range of ecosystems in the American tropics and exhibiting large variations in ecology, morphology, and behavior. Although the relationships among the almost 200 living species are relatively well understood, we lack robust estimates of the timing of origin, the ancestral morphology, and the evolution of the distribution of the clade. Here we integrate paleontological and molecular evidence to investigate the evolutionary dynamics of extinct and extant platyrrhines. We develop an analytical framework to infer ancestral states, the evolution of body mass, and changes in latitudinal ranges through time. Our results show that extant platyrrhines originated some 5-10 million years earlier than previously assumed, likely dating back to the Middle Eocene ([~] 43 million years ago, Ma). The estimated ancestral platyrrhine was strikingly small - weighing [~] 0.4 kg, as compared to the largest modern species over 10 kg - matching the size of their presumed Eocene North African ancestors. Small-sized callitrichines (marmosets and tamarins) retained a small body mass throughout their evolutionary history, thus challenging the hypothesis of phyletic dwarfism as an explanation to their adaptive traits. In contrast, a rapid change in body mass range took place as the three families diverged between the Late Oligocene and the Early Miocene. That period also marks a peak in diversity of fossil platyrrhines and is associated with their widest latitudinal range, expanding as far to the South as Patagonia. This geographic expansion is temporally coincident with a significant increase in platyrrhine population size inferred from genomic data, and with warm and humid climatic conditions linked to the Miocene Climatic Optimum and the lower elevation of the Andes. These results unveil the early evolution of an iconic group of monkeys and showcase the advantages of integrating fossil and molecular data for estimating evolutionary rates and trends.

evolutionary biology↗

bioRxiv2017

Modeling codon rate variation improves protein positive selection inference and detects nucleotide selection

There are numerous sources of variation in the rate of synonymous substitutions inside genes, such as direct selection on the nucleotide sequence, or mutation rate variation. Yet scans for positive selection rely on codon models which incorporate an assumption of effectively neutral synonymous substitution rate, constant between sites of each gene. Here we perform a large-scale comparison of approaches which incorporate codon substitution rate variation and propose our own simple yet effective modification of existing models. We find strong effects of substitution rate variation on positive selection inference. More than 70% of the genes detected by the classical branch-site model are presumably false positives caused by the incorrect assumption of uniform synonymous substitution rate. We propose a new model which is strongly favored by the data while remaining computationally tractable. With the new model we can capture signatures of nucleotide level selection acting on translation initiation and on splicing sites within the coding region. Finally, we show that rate variation is highest in the highly recombining regions, and we propose that recombination and mutation rate variation, such as high CpG mutation rate, are the two main sources of nucleotide rate variation. While we detect fewer genes under positive selection in Drosophila than without rate variation, the genes which we detect contain a stronger signal of adaptation of dynein, which could be associated with Wolbachia infection. We provide software to perform positive selection analysis using the new model.

bioinformatics↗