Publications by authors named "Nicolas Salamin"

105 Publications

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

J Evol Biol 2021 Jun 7. Epub 2021 Jun 7.

Sorbonne Université, UPMC Univ Paris 06, CNRS, Algal Genetics Group, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, F-29688, Roscoff, France.

A vast diversity of types of life cycles exists in nature, and several theories have been advanced to explain how this diversity has evolved and how each type of life cycle is retained over evolutionary time. Here, we exploited the diversity of life cycles and reproductive traits of the brown algae (Phaeophyceae) to test several hypotheses on the evolution of life cycles. We investigated the evolutionary dynamics of four life-history traits: life cycle, sexual system, level of gamete dimorphism and gamete parthenogenetic capacity. We assigned states to up to 77 representative species of the taxonomic diversity of the brown algal group, in a multi-gene phylogeny. We used maximum likelihood and Bayesian analyses of correlated evolution, while taking the phylogeny into account, to test for correlations between traits, and to investigate the chronological sequence of trait acquisition. Our analyses are consistent with the prediction that diploid growth evolves when sexual reproduction is preferred over asexual reproduction, possibly because it allows the complementation of deleterious mutations. We also found that haploid sex determination is ancestral in relation to diploid sex determination. However, our results could not address whether increased zygotic and diploid growth are associated with increased sexual dimorphism. Our analyses suggest that in the brown algae, isogamous species evolved from anisogamous ancestors, contrary to the commonly reported pattern where evolution proceeds from isogamy to anisogamy.
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http://dx.doi.org/10.1111/jeb.13880DOI Listing
June 2021

Thyroid hormones regulate the formation and environmental plasticity of white bars in clownfishes.

Proc Natl Acad Sci U S A 2021 Jun;118(23)

Marine Eco-Evo-Devo Unit, Okinawa Institute of Science and Technology, Onna son, Okinawa 904-0495 Japan;

Determining how plasticity of developmental traits responds to environmental conditions is a challenge that must combine evolutionary sciences, ecology, and developmental biology. During metamorphosis, fish alter their morphology and color pattern according to environmental cues. We observed that juvenile clownfish () modulate the developmental timing of their adult white bar formation during metamorphosis depending on the sea anemone species in which they are recruited. We observed an earlier formation of white bars when clownfish developed with () than with (). As these bars, composed of iridophores, form during metamorphosis, we hypothesized that timing of their development may be thyroid hormone (TH) dependent. We treated clownfish larvae with TH and found that white bars developed earlier than in control fish. We further observed higher TH levels, associated with rapid white bar formation, in juveniles recruited in than in , explaining the faster white bar formation. Transcriptomic analysis of recruits revealed higher expression of , a dual oxidase implicated in TH production as compared to recruits. Finally, we showed that is an essential regulator of iridophore pattern timing in zebrafish. Taken together, our results suggest that TH controls the timing of adult color pattern formation and that shifts in expression and TH levels are associated with ecological differences resulting in divergent ontogenetic trajectories in color pattern development.
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http://dx.doi.org/10.1073/pnas.2101634118DOI Listing
June 2021

Fossil-informed models reveal a Boreotropical origin and divergent evolutionary trajectories in the walnut family (Juglandaceae).

Syst Biol 2021 May 8. Epub 2021 May 8.

Department of Biology, University of Fribourg, 1700 Fribourg, Switzerland.

Temperate woody plants in the Northern Hemisphere have long been known to exhibit high species richness in East Asia and North America and significantly lower diversity in Europe, but the causes of this pattern remain debated. Here, we quantify the roles of dispersal, niche evolution, and extinction in shaping the geographic diversity of the temperate woody plant family Juglandaceae (walnuts and their relatives). Integrating evidence from molecular, morphological, fossil, and (paleo)environmental data, we find strong support for a Boreotropical origin of the family with contrasting evolutionary trajectories between the temperate subfamily Juglandoideae and the tropical subfamily Engelhardioideae. Juglandoideae rapidly evolved frost tolerance when the global climate shifted to ice-house conditions from the Oligocene, with diversification at high latitudes especially in Europe and Asia during the Miocene. Subsequent range contraction at high latitudes and high levels of extinction in Europe driven by global cooling led to the current regional disparity in species diversity. Engelhardioideae showed temperature conservatism while adapting to increased humidity, tracking tropical climates to low latitudes since the middle Eocene with comparatively little diversification, perhaps due to high competition in the tropical zone. The biogeographic history of Juglandaceae shows that the North Atlantic land bridge and Europe played more critical roles than previously thought in linking the floras of East Asia and North America, and showcases the complex interplay among climate change, niche evolution, dispersal, and extinction that shaped the modern disjunct pattern of species richness in temperate woody plants.
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http://dx.doi.org/10.1093/sysbio/syab030DOI Listing
May 2021

Phylogenomics of Gesneriaceae using targeted capture of nuclear genes.

Mol Phylogenet Evol 2021 04 7;157:107068. Epub 2021 Jan 7.

Conservatoire et Jardin botaniques de la Ville de Genève and Department of Botany and Plant Biology, University of Geneva, 1292 Chambésy, Switzerland. Electronic address:

Gesneriaceae (ca. 3400 species) is a pantropical plant family with a wide range of growth form and floral morphology that are associated with repeated adaptations to different environments and pollinators. Although Gesneriaceae systematics has been largely improved by the use of Sanger sequencing data, our understanding of the evolutionary history of the group is still far from complete due to the limited number of informative characters provided by this type of data. To overcome this limitation, we developed here a Gesneriaceae-specific gene capture kit targeting 830 single-copy loci (776,754 bp in total), including 279 genes from the Universal Angiosperms-353 kit. With an average of 557,600 reads and 87.8% gene recovery, our target capture was successful across the family Gesneriaceae and also in other families of Lamiales. From our bait set, we selected the most informative 418 loci to resolve phylogenetic relationships across the entire Gesneriaceae family using maximum likelihood and coalescent-based methods. Upon testing the phylogenetic performance of our baits on 78 taxa representing 20 out of 24 subtribes within the family, we showed that our data provided high support for the phylogenetic relationships among the major lineages, and were able to provide high resolution within more recent radiations. Overall, the molecular resources we developed here open new perspectives for the study of Gesneriaceae phylogeny at different taxonomical levels and the identification of the factors underlying the diversification of this plant group.
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http://dx.doi.org/10.1016/j.ympev.2021.107068DOI Listing
April 2021

A Cautionary Note on the Use of Genotype Callers in Phylogenomics.

Syst Biol 2021 Jun;70(4):844-854

Department of Computational Biology, University of Lausanne, Quartier Sorge, 1015 Lausanne, Switzerland.

Next-generation-sequencing genotype 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 genotype callers, such as the one from GATK, is that they are optimized for variant calling at the population level. However, when these callers are used at the phylogenetic level, the consequences for downstream analyses can be substantial. Here, we performed simulations to compare the performance between the genotype callers of GATK and ATLAS, and present their differences at various phylogenetic scales. We show that the genotype caller of GATK substantially underestimates the number of variants at the phylogenetic level, but not at the population level. We also found that the accuracy of heterozygote calls declines with increasing distance to the reference genome. We quantified this decline and found that it is very sharp in GATK, while ATLAS maintains high accuracy 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. [ATLAS; efficiency of SNP calling; GATK; heterozygote calling; next-generation sequencing; reference genome; variant calling.].
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http://dx.doi.org/10.1093/sysbio/syaa081DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8208803PMC
June 2021

Rapid climate change results in long-lasting spatial homogenization of phylogenetic diversity.

Nat Commun 2020 09 16;11(1):4663. Epub 2020 Sep 16.

Swiss Federal Research Institute WSL, 8903, Birmensdorf, Switzerland.

Scientific understanding of biodiversity dynamics, resulting from past climate oscillations and projections of future changes in biodiversity, has advanced over the past decade. Little is known about how these responses, past or future, are spatially connected. Analyzing the spatial variability in biodiversity provides insight into how climate change affects the accumulation of diversity across space. Here, we evaluate the spatial variation of phylogenetic diversity of European seed plants among neighboring sites and assess the effects of past rapid climate changes during the Quaternary on these patterns. Our work shows a marked homogenization in phylogenetic diversity across Central and Northern Europe linked to high climate change velocity and large distances to refugia. Our results suggest that the future projected loss in evolutionary heritage may be even more dramatic, as homogenization in response to rapid climate change has occurred among sites across large landscapes, leaving a legacy that has lasted for millennia.
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http://dx.doi.org/10.1038/s41467-020-18343-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7495423PMC
September 2020

Population Genetic Structure and Demographic History of in Southwest China.

Front Plant Sci 2020 2;11:986. Epub 2020 Jul 2.

Department of Computational Biology, Biophore, University of Lausanne, Lausanne, Switzerland.

Understanding the factors that drive the genetic structure of a species and its responses to past climatic changes is an important first step in modern population management. The response to the last glacial maximum (LGM) has been well studied, however, the effect of previous glaciation periods on plant demographic history is still not well studied. Here we investigated the population structure and demographic history of that widely occurs in the Hengduan Mountains and Qinghai-Tibetan Plateau. We obtained genomic data for 234 samples of the species using restriction site-associated DNA (RAD) sequencing and combined approximate Bayesian computation (ABC) and species distribution modeling (SDM) to evaluate the effects of multiple glaciation periods by testing several population divergence models and demographic scenarios. The analyses of population structure showed that displays a striking population structure with six groups that could be identified genetically. Our ABC modeling suggested that the current groups diverged from ancestral populations located in the eastern Hengduan Mountains after the largest glaciation occurred in the region (~ 0.8-0.5 million years ago), which is consistent with the result of SDMs. Each current group has survived in different glacial refugia during the LGM and experienced expansions and/or bottlenecks since their divergence during or across the following Quaternary glacial cycles. Our study demonstrates the usefulness of population genomics for evaluating the effects of past climatic changes in alpine plant species with shallow population structure.
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http://dx.doi.org/10.3389/fpls.2020.00986DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7351516PMC
July 2020

On the Effect of Asymmetrical Trait Inheritance on Models of Trait Evolution.

Syst Biol 2021 Feb;70(2):376-388

Department of Biology, University of Fribourg, 1700 Fribourg, Switzerland Nicolas Salamin and Daniele Silvestro contributed equally to this article.

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 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 intraspecific variability around species mean phenotypes and how it is inherited at speciation.
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http://dx.doi.org/10.1093/sysbio/syaa055DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7875446PMC
February 2021

Genomic footprints of repeated evolution of CAM photosynthesis in a Neotropical species radiation.

Plant Cell Environ 2020 12 25;43(12):2987-3001. Epub 2020 Aug 25.

Department of Botany and Biodiversity Research, Division of Systematic and Evolutionary Botany, Faculty of Life Sciences, University of Vienna, Vienna, Austria.

The adaptive radiation of Bromeliaceae (pineapple family) is one of the most diverse among Neotropical flowering plants. Diversification in this group was facilitated by shifts in several adaptive traits or "key innovations" including the transition from C to CAM photosynthesis associated with xeric (heat/drought) adaptation. We used phylogenomic approaches, complemented by differential gene expression (RNA-seq) and targeted metabolite profiling, to address the mechanisms of C /CAM evolution in the extremely species-rich bromeliad genus, Tillandsia, and related taxa. Evolutionary analyses of whole-genome sequencing and RNA-seq data suggest that evolution of CAM is associated with coincident changes to different pathways mediating xeric adaptation in this group. At the molecular level, C /CAM shifts were accompanied by gene expansion of XAP5 CIRCADIAN TIMEKEEPER homologs, a regulator involved in sugar- and light-dependent regulation of growth and development. Our analyses also support the re-programming of abscisic acid-related gene expression via differential expression of ABF2/ABF3 transcription factor homologs, and adaptive sequence evolution of an ENO2/LOS2 enolase homolog, effectively tying carbohydrate flux to abscisic acid-mediated abiotic stress response. By pinpointing different regulators of overlapping molecular responses, our results suggest plausible mechanistic explanations for the repeated evolution of correlated adaptive traits seen in a textbook example of an adaptive radiation.
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http://dx.doi.org/10.1111/pce.13847DOI Listing
December 2020

Prototypic SNARE Proteins Are Encoded in the Genomes of Heimdallarchaeota, Potentially Bridging the Gap between the Prokaryotes and Eukaryotes.

Curr Biol 2020 07 21;30(13):2468-2480.e5. Epub 2020 May 21.

Department of Fundamental Neurosciences, University of Lausanne, Rue du Bugnon 9, 1005 Lausanne, Switzerland; Department of Computational Biology, University of Lausanne, Génopode, 1015 Lausanne, Switzerland. Electronic address:

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 together. 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 clade, 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 α-proteobacteria, the closest relatives of mitochondria, but identified several genes encoding for SNARE proteins in γ-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.
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http://dx.doi.org/10.1016/j.cub.2020.04.060DOI Listing
July 2020

Evolution of a supergene that regulates a trans-species social polymorphism.

Nat Ecol Evol 2020 02 20;4(2):240-249. Epub 2020 Jan 20.

Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland.

Supergenes are clusters of linked genetic loci that jointly affect the expression of complex phenotypes, such as social organization. Little is known about the origin and evolution of these intriguing genomic elements. Here we analyse whole-genome sequences of males from native populations of six fire ant species and show that variation in social organization is under the control of a novel supergene haplotype (termed Sb), which evolved by sequential incorporation of three inversions spanning half of a 'social chromosome'. Two of the inversions interrupt protein-coding genes, resulting in the increased expression of one gene and modest truncation in the primary protein structure of another. All six socially polymorphic species studied harbour the same three inversions, with the single origin of the supergene in their common ancestor inferred by phylogenomic analyses to have occurred half a million years ago. The persistence of Sb along with the ancestral SB haplotype through multiple speciation events provides a striking example of a functionally important trans-species social polymorphism presumably maintained by balancing selection. We found that while recombination between the Sb and SB haplotypes is severely restricted in all species, a low level of gene flux between the haplotypes has occurred following the appearance of the inversions, potentially mitigating the evolutionary degeneration expected at genomic regions that cannot freely recombine. These results provide a detailed picture of the structural genomic innovations involved in the formation of a supergene controlling a complex social phenotype.
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http://dx.doi.org/10.1038/s41559-019-1081-1DOI Listing
February 2020

Linking micro and macroevolution in the presence of migration.

J Theor Biol 2020 02 20;486:110087. Epub 2019 Nov 20.

Department of Computational Biology, University of Lausanne, Lausanne, Switzerland.

Understanding macroevolutionary patterns is central to evolutionary biology. This involves the process of divergence within a species, which 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 the mean trait towards different optima in the different subpopulations, and ongoing migration that pulls the mean phenotype away from that optimum. Traditionally, macro phenotypic evolution is modelled by directional selection processes, but these models usually ignore the role of migration within species. Here, our goal is to reconcile the processes of micro and macroevolution by modelling migration as part of the speciation process. More precisely, we introduce an Ornstein-Uhlenbeck (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. We show that ignoring the effect of migration in sampled time-series data biases significantly the estimation of the selective forces acting upon it. We also show that migration decreases the expected phenotypic disparity between species and we analyse 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. Our model extends traditional quantitative genetics results of selection and migration from a microevolutionary time frame to multiple speciation events at a macroevolutionary scale. Our results further support that not accounting for gene flow has important consequences in inferences at both the micro and macroevolutionary scale.
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http://dx.doi.org/10.1016/j.jtbi.2019.110087DOI Listing
February 2020

Slowly but surely: gradual diversification and phenotypic evolution in the hyper-diverse tree fern family Cyatheaceae.

Ann Bot 2020 01;125(1):93-103

Department of Computational Biology, University of Lausanne, 1015 Lausanne, Switzerland.

Background And Aims: The tremendously unbalanced distribution of species richness across clades in the tree of life is often interpreted as the result of variation in the rates of diversification, which may themselves respond to trait evolution. Even though this is likely a widespread pattern, not all diverse groups of organisms exhibit heterogeneity in their dynamics of diversification. Testing and characterizing the processes driving the evolution of clades with steady rates of diversification over long periods of time are of importance in order to have a full understanding of the build-up of biodiversity through time.

Methods: We studied the macroevolutionary history of the species-rich tree fern family Cyatheaceae and inferred a time-calibrated phylogeny of the family including extinct and extant species using the recently developed fossilized birth-death method. We tested whether the high diversity of Cyatheaceae is the result of episodes of rapid diversification associated with phenotypic and ecological differentiation or driven by stable but low rates of diversification. We compared the rates of diversification across clades, modelled the evolution of body size and climatic preferences and tested for trait-dependent diversification.

Key Results: This ancient group diversified at a low and constant rate during its long evolutionary history. Morphological and climatic niche evolution were found to be overall highly conserved, although we detected several shifts in the rates of evolution of climatic preferences, linked to changes in elevation. The diversification of the family occurred gradually, within limited phenotypic and ecological boundaries, and yet resulted in a remarkable species richness.

Conclusions: Our study indicates that Cyatheaceae is a diverse clade which slowly accumulated morphological, ecological and taxonomic diversity over a long evolutionary period and provides a compelling example of the tropics as a museum of biodiversity.
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http://dx.doi.org/10.1093/aob/mcz145DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6948215PMC
January 2020

Duplication history and molecular evolution of the rbcS multigene family in angiosperms.

J Exp Bot 2019 11;70(21):6127-6139

Department of Computational Biology, Génopode, University of Lausanne, Lausanne, Switzerland.

Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) is considered to be the main enzyme determining the rate of photosynthesis. The small subunit of the protein, encoded by the rbcS gene, has been shown to influence the catalytic efficiency, CO2 specificity, assembly, activity, and stability of RuBisCO. However, the evolution of the rbcS gene remains poorly studied. We inferred the phylogenetic tree of the rbcS gene in angiosperms using the nucleotide sequences and found that it is composed of two lineages that may have existed before the divergence of land plants. Although almost all species sampled carry at least one copy of lineage 1, genes of lineage 2 were lost in most angiosperm species. We found the specific residues that have undergone positive selection during the evolution of the rbcS gene. We detected intensive coevolution between each rbcS gene copy and the rbcL gene encoding the large subunit of RuBisCO. We tested the role played by each rbcS gene copy on the stability of the RuBisCO protein through homology modelling. Our results showed that this evolutionary constraint could limit the level of divergence seen in the rbcS gene, which leads to the similarity among the rbcS gene copies of lineage 1 within species.
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http://dx.doi.org/10.1093/jxb/erz363DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6859733PMC
November 2019

Targeted Capture of Hundreds of Nuclear Genes Unravels Phylogenetic Relationships of the Diverse Neotropical Palm Tribe Geonomateae.

Front Plant Sci 2019 12;10:864. Epub 2019 Jul 12.

Department of Computational Biology, University of Lausanne, Lausanne, Switzerland.

The tribe Geonomateae is a widely distributed group of 103 species of Neotropical palms which contains six ecologically important understory or subcanopy genera. Although it has been the focus of many studies, our understanding of the evolutionary history of this group, and in particular of the taxonomically complex genus , is far from complete due to a lack of molecular data. Specifically, the previous Sanger sequencing-based studies used a few informative characters and partial sampling. To overcome these limitations, we used a recently developed Arecaceae-specific target capture bait set to undertake a phylogenomic analysis of the tribe Geonomateae. We sequenced 3,988 genomic regions for 85% of the species of the tribe, including 84% of the species of the largest genus, . Phylogenetic relationships were inferred using both concatenation and coalescent methods. Overall, our phylogenetic tree is highly supported and congruent with taxonomic delimitations although several morphological taxa were revealed to be non-monophyletic. It is the first time that such a large genomic dataset is provided for an entire tribe within the Arecaceae. Our study lays the groundwork not only for detailed macro- and micro-evolutionary studies within the group, but also sets a workflow for understanding other species complexes across the tree of life.
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http://dx.doi.org/10.3389/fpls.2019.00864DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6640726PMC
July 2019

Large-Scale Comparative Analysis of Codon Models Accounting for Protein and Nucleotide Selection.

Mol Biol Evol 2019 06;36(6):1316-1332

Department of Ecology and Evolution, Biophore, University of Lausanne, Lausanne, Switzerland.

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. Although 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.
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http://dx.doi.org/10.1093/molbev/msz048DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6526913PMC
June 2019

Insights into the Genomics of Clownfish Adaptive Radiation: Genetic Basis of the Mutualism with Sea Anemones.

Genome Biol Evol 2019 03;11(3):869-882

Department of Computational Biology, Génopode, University of Lausanne, Switzerland.

Clownfishes are an iconic group of coral reef fishes, especially known for their mutualism with sea anemones. This mutualism is particularly interesting as it likely acted as the key innovation that triggered clownfish adaptive radiation. Indeed, after the acquisition of the mutualism, clownfishes diversified into multiple ecological niches linked with host and habitat use. However, despite the importance of this mutualism, the genetic mechanisms allowing clownfishes to interact with sea anemones are still unclear. Here, we used a comparative genomics and molecular evolutionary analyses to investigate the genetic basis of clownfish mutualism with sea anemones. We assembled and annotated the genome of nine clownfish species and one closely related outgroup. Orthologous genes inferred between these species and additional publicly available teleost genomes resulted in almost 16,000 genes that were tested for positively selected substitutions potentially involved in the adaptation of clownfishes to live in sea anemones. We identified 17 genes with a signal of positive selection at the origin of clownfish radiation. Two of them (Versican core protein and Protein O-GlcNAse) show particularly interesting functions associated with N-acetylated sugars, which are known to be involved in sea anemone discharge of toxins. This study provides the first insights into the genetic mechanisms of clownfish mutualism with sea anemones. Indeed, we identified the first candidate genes likely to be associated with clownfish protection form sea anemones, and thus the evolution of their mutualism. Additionally, the genomic resources acquired represent a valuable resource for further investigation of the genomic basis of clownfish adaptive radiation.
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http://dx.doi.org/10.1093/gbe/evz042DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6430985PMC
March 2019

Simultaneous Bayesian inference of phylogeny and molecular coevolution.

Proc Natl Acad Sci U S A 2019 03 26;116(11):5027-5036. Epub 2019 Feb 26.

Department of Computational Biology, University of Lausanne, 1015 Lausanne, Switzerland.

Patterns of molecular coevolution can reveal structural and functional constraints within or among organic molecules. These patterns are better understood when considering the underlying evolutionary process, which enables us to disentangle the signal of the dependent evolution of sites (coevolution) from the effects of shared ancestry of genes. Conversely, disregarding the dependent evolution of sites when studying the history of genes negatively impacts the accuracy of the inferred phylogenetic trees. Although molecular coevolution and phylogenetic history are interdependent, analyses of the two processes are conducted separately, a choice dictated by computational convenience, but at the expense of accuracy. We present a Bayesian method and associated software to infer how many and which sites of an alignment evolve according to an independent or a pairwise dependent evolutionary process, and to simultaneously estimate the phylogenetic relationships among sequences. We validate our method on synthetic datasets and challenge our predictions of coevolution on the 16S rRNA molecule by comparing them with its known molecular structure. Finally, we assess the accuracy of phylogenetic trees inferred under the assumption of independence among sites using synthetic datasets, the 16S rRNA molecule and 10 additional alignments of protein-coding genes of eukaryotes. Our results demonstrate that inferring phylogenetic trees while accounting for dependent site evolution significantly impacts the estimates of the phylogeny and the evolutionary process.
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http://dx.doi.org/10.1073/pnas.1813836116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6421416PMC
March 2019

Environment and evolutionary history shape phylogenetic turnover in European tetrapods.

Nat Commun 2019 01 16;10(1):249. Epub 2019 Jan 16.

Swiss Federal Research Institute WSL, 8903, Birmensdorf, Switzerland.

Phylogenetic turnover quantifies the evolutionary distance among species assemblages and is central to understanding the main drivers shaping biodiversity. It is affected both by geographic and environmental distance between sites. Therefore, analyzing phylogenetic turnover in environmental space requires removing the effect of geographic distance. Here, we apply a novel approach by deciphering phylogenetic turnover of European tetrapods in environmental space after removing geographic land distance effects. We demonstrate that phylogenetic turnover is strongly structured in environmental space, particularly in ectothermic tetrapods, and is well explained by macroecological characteristics such as niche size, species richness and relative phylogenetic diversity. In ectotherms, rather recent evolutionary processes were important in structuring phylogenetic turnover along environmental gradients. In contrast, early evolutionary processes had already shaped the current structure of phylogenetic turnover in endotherms. Our approach enables the disentangling of the idiosyncrasies of evolutionary processes such as the degree of niche conservatism and diversification rates in structuring biodiversity.
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http://dx.doi.org/10.1038/s41467-018-08232-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6335467PMC
January 2019

Developmental and comparative transcriptomic identification of iridophore contribution to white barring in clownfish.

Pigment Cell Melanoma Res 2019 05 29;32(3):391-402. Epub 2019 Jan 29.

Observatoire Océanologique de Banyuls-sur-Mer, UMR CNRS 7232 BIOM, Sorbonne Université, Banyuls-sur-Mer, France.

Actinopterygian fishes harbor at least eight distinct pigment cell types, leading to a fascinating diversity of colors. Among this diversity, the cellular origin of the white color appears to be linked to several pigment cell types such as iridophores or leucophores. We used the clownfish Amphiprion ocellaris, which has a color pattern consisting of white bars over a darker body, to characterize the pigment cells that underlie the white hue. We observe by electron microscopy that cells in white bars are similar to iridophores. In addition, the transcriptomic signature of clownfish white bars exhibits similarities with that of zebrafish iridophores. We further show by pharmacological treatments that these cells are necessary for the white color. Among the top differentially expressed genes in white skin, we identified several genes (fhl2a, fhl2b, saiyan, gpnmb, and apoD1a) and show that three of them are expressed in iridophores. Finally, we show by CRISPR/Cas9 mutagenesis that these genes are critical for iridophore development in zebrafish. Our analyses provide clues to the genomic underpinning of color diversity and allow identification of new iridophore genes in fish.
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http://dx.doi.org/10.1111/pcmr.12766DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6483885PMC
May 2019

CoevDB: a database of intramolecular coevolution among protein-coding genes of the bony vertebrates.

Nucleic Acids Res 2019 01;47(D1):D50-D54

Department of Computational Biology, University of Lausanne, Biophore, 1015 Lausanne, Switzerland.

The study of molecular coevolution, due to its potential to identify gene regions under functional or structural constraints, has recently been subject to numerous scientific inquiries. Particular efforts have been conducted to develop methods predicting the presence of coevolution in molecular sequences. Among these methods, a few aim to model the underlying evolutionary process of coevolution, which enable to differentiate the shared history of genes to coevolution and thus improve their accuracy. However, the usage of such methods remains sparse due to their expensive computational cost and the lack of resources alleviating this issue. Here we present CoevDB (http://phylodb.unil.ch/CoevDB), a database containing the result of a large-scale analysis of intramolecular coevolution of 8201 protein-coding genes of bony vertebrates. The web interface of CoevDB gives access to the results to 800 millions of statistical tests corresponding to all the pairs of sites analyzed. Several type of queries enable users to explore the database by either targeting specific genes or by discovering genes having promising estimations of coevolution.
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http://dx.doi.org/10.1093/nar/gky986DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6324051PMC
January 2019

A dedicated target capture approach reveals variable genetic markers across micro- and macro-evolutionary time scales in palms.

Mol Ecol Resour 2019 Jan 3;19(1):221-234. Epub 2018 Nov 3.

Department of Biology, Unit Ecology and Evolution, University of Fribourg, Fribourg, Switzerland.

Understanding the genetics of biological diversification across micro- and macro-evolutionary time scales is a vibrant field of research for molecular ecologists as rapid advances in sequencing technologies promise to overcome former limitations. In palms, an emblematic, economically and ecologically important plant family with high diversity in the tropics, studies of diversification at the population and species levels are still hampered by a lack of genomic markers suitable for the genotyping of large numbers of recently diverged taxa. To fill this gap, we used a whole genome sequencing approach to develop target sequencing for molecular markers in 4,184 genome regions, including 4,051 genes and 133 non-genic putatively neutral regions. These markers were chosen to cover a wide range of evolutionary rates allowing future studies at the family, genus, species and population levels. Special emphasis was given to the avoidance of copy number variation during marker selection. In addition, a set of 149 well-known sequence regions previously used as phylogenetic markers by the palm biological research community were included in the target regions, to open the possibility to combine and jointly analyse already available data sets with genomic data to be produced with this new toolkit. The bait set was effective for species belonging to all three palm sub-families tested (Arecoideae, Ceroxyloideae and Coryphoideae), with high mapping rates, specificity and efficiency. The number of high-quality single nucleotide polymorphisms (SNPs) detected at both the sub-family and population levels facilitates efficient analyses of genomic diversity across micro- and macro-evolutionary time scales.
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http://dx.doi.org/10.1111/1755-0998.12945DOI Listing
January 2019

Howling from the past: historical phylogeography and diversity losses in European grey wolves.

Proc Biol Sci 2018 08 1;285(1884). Epub 2018 Aug 1.

Laboratory for Conservation Biology, Department of Ecology and Evolution University of Lausanne, Biophore Building, CH-1015 Lausanne, Switzerland

Genetic bottlenecks resulting from human-induced population declines make alarming symbols for the irreversible loss of our natural legacy worldwide. The grey wolf () is an iconic example of extreme declines driven by anthropogenic factors. Here, we assessed the genetic signatures of 150 years of wolf persecution throughout the Western Palaearctic by high-throughput mitochondrial DNA sequencing of historical specimens in an unprecedented spatio-temporal framework. Despite Late Pleistocene bottlenecks, we show that historical genetic variation had remained high throughout Europe until the last several hundred years. In Western Europe, where wolves nearly got fully exterminated, diversity dramatically collapsed at the turn of the twentieth century and recolonization from few homogeneous relict populations induced drastic shifts of genetic composition. By contrast, little genetic displacement and steady levels of diversity were maintained in Eastern European regions, where human persecution had lesser effects on wolf demography. By comparing prehistoric, historic and modern patterns of genetic diversity, our study hence traces the timeframe and the active human role in the decline of the grey wolf, an emblematic yet controversial animal which symbolizes the complex relationship between human societies and nature conservation.
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http://dx.doi.org/10.1098/rspb.2018.1148DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6111155PMC
August 2018

Early Arrival and Climatically-Linked Geographic Expansion of New World Monkeys from Tiny African Ancestors.

Syst Biol 2019 01;68(1):78-92

Department of Computational Biology, University of Lausanne, 1015 Lausanne, Switzerland.

New World Monkeys (NWM) (platyrrhines) 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, ancestral morphology, and geographic range evolution of the clade. Herein, we integrate paleontological and molecular evidence to assess the evolutionary dynamics of extinct and extant platyrrhines. We develop novel analytical frameworks to infer the evolution of body mass, changes in latitudinal ranges through time, and species diversification rates using a phylogenetic tree of living and fossil taxa. Our results show that platyrrhines originated 5-10 million years earlier than previously assumed, dating back to the Middle Eocene. The estimated ancestral platyrrhine was small-weighing 0.4 kg-and matched the size of their presumed African ancestors. As the three platyrrhine families diverged, we recover a rapid change in body mass range. During the Miocene Climatic Optimum, fossil diversity peaked and platyrrhines reached their widest latitudinal range, expanding as far South as Patagonia, favored by warm and humid climate and the lower elevation of the Andes. Finally, global cooling and aridification after the middle Miocene triggered a geographic contraction of NWM and increased their extinction rates. These results unveil the full evolutionary trajectory of an iconic and ecologically important radiation of monkeys and showcase the necessity of integrating fossil and molecular data for reliably estimating evolutionary rates and trends.
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http://dx.doi.org/10.1093/sysbio/syy046DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6292484PMC
January 2019

Polymorphic sites preferentially avoid co-evolving residues in MHC class I proteins.

PLoS Comput Biol 2018 05 21;14(5):e1006188. Epub 2018 May 21.

Department of Oncology, Ludwig Institute for Cancer Research, University of Lausanne, Switzerland.

Major histocompatibility complex class I (MHC-I) molecules are critical to adaptive immune defence mechanisms in vertebrate species and are encoded by highly polymorphic genes. Polymorphic sites are located close to the ligand-binding groove and entail MHC-I alleles with distinct binding specificities. Some efforts have been made to investigate the relationship between polymorphism and protein stability. However, less is known about the relationship between polymorphism and MHC-I co-evolutionary constraints. Using Direct Coupling Analysis (DCA) we found that co-evolution analysis accurately pinpoints structural contacts, although the protein family is restricted to vertebrates and comprises less than five hundred species, and that the co-evolutionary signal is mainly driven by inter-species changes, and not intra-species polymorphism. Moreover, we show that polymorphic sites in human preferentially avoid co-evolving residues, as well as residues involved in protein stability. These results suggest that sites displaying high polymorphism may have been selected during vertebrates' evolution to avoid co-evolutionary constraints and thereby maximize their mutability.
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http://dx.doi.org/10.1371/journal.pcbi.1006188DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5983860PMC
May 2018

Clownfishes evolution below and above the species level.

Proc Biol Sci 2018 02;285(1873)

Department of Computational Biology, University of Lausanne, Biophore, Quartier-Sorge, 1015 Lausanne, Switzerland.

The difference between rapid morphological evolutionary changes observed in populations and the long periods of stasis detected in the fossil record has raised a decade-long debate about the exact role played by intraspecific mechanisms at the interspecific level. Although they represent different scales of the same evolutionary process, micro- and macroevolution are rarely studied together and few empirical studies have compared the rates of evolution and the selective pressures between both scales. Here, we analyse morphological, genetic and ecological traits in clownfishes at different evolutionary scales and demonstrate that the tempo of molecular and morphological evolution at the species level can be, to some extent, predicted from parameters estimated below the species level, such as the effective population size or the rate of evolution within populations. We also show that similar codons in the gene of the rhodopsin , a light-sensitive receptor protein, are under positive selection at the intra and interspecific scales, suggesting that similar selective pressures are acting at both levels.
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http://dx.doi.org/10.1098/rspb.2017.1796DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5832698PMC
February 2018

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

Mol Ecol Resour 2018 Feb 17. Epub 2018 Feb 17.

Department of Computational Biology, Biophore, University of Lausanne, Lausanne, Switzerland.

Clownfishes (or anemonefishes) form an iconic group of coral reef fishes, principally 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 groups to have experienced an adaptive radiation in the marine environment. Here, we assembled and annotated the first genome of a clownfish species, the tomato clownfish (Amphiprion frenatus). We obtained 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 Benchmarking Universal Single-Copy Orthologs (BUSCOs) being retrieved in A. frenatus assembly. The quality of the resulting assembly is comparable to other bony fish assemblies. This resource is valuable for advancing 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.
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http://dx.doi.org/10.1111/1755-0998.12772DOI Listing
February 2018

Publisher Correction: The impact of endothermy on the climatic niche evolution and the distribution of vertebrate diversity.

Nat Ecol Evol 2018 03;2(3):578

Department of Computational Biology, Biophore, University of Lausanne, Lausanne, Switzerland.

In the version of this Article originally published, in Fig. 3a the first boundary was incorrectly labelled the "K/T boundary"; it should have read the "K/Pg boundary". The two equations in the main text were incorrectly omitted from the HTML. In the description of the posterior distribution of an ancestral state, the normal distribution was incorrectly described as being "assigned as prior to the node value"; it should have read "assigned as calibration to the node value". In the associated equation (the second equation in the text), the denominator of the last term was incorrectly given as "Node prior"; it should have read "Node calibration". In the same equation, the numerator of the third term on the right-hand side of the equation contained incorrect superscript notation on the x and this is shown in the full equation in the notice below.In the Acknowledgements, the following two sentences were incorrectly omitted: "The authors thank the Vital-IT facilities of the Swiss Institute of Bioinformatics for the computational support" and "This work was funded by the University of Lausanne and the Swiss National Science Foundation (CRSIII3-147630) to N.S." In the Author contributions section, the first sentence was incorrectly given as "J.R. designed the study. J.R., N.S. and D. Silvestro designed the methodology and ran the analyses"; it should have read "J.R., D.S. and N.S. designed the study and the methodology". In the Supplementary Information, all three instances of the word "prior" were incorrect and should have read "calibration".These errors have now been corrected in all versions of the Article.
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http://dx.doi.org/10.1038/s41559-018-0492-8DOI Listing
March 2018

The impact of endothermy on the climatic niche evolution and the distribution of vertebrate diversity.

Nat Ecol Evol 2018 03 29;2(3):459-464. Epub 2018 Jan 29.

Department of Computational Biology, Biophore, University of Lausanne, Lausanne, Switzerland.

Understanding the mechanisms by which the abiotic and biotic requirements of species, or ecological niches, change over time is a central issue in evolutionary biology. Niche evolution is poorly understood at both the macroecological and macroevolutionary scales, as niches can shift over short periods of time but appear to change more slowly over longer timescales. Although reconstructing past niches has always been a major concern for palaeontologists and evolutionary biologists, only a few recent studies have successfully determined the factors that affect niche evolution. Here, we compare the evolution of climatic niches in four main groups of terrestrial vertebrates using a modelling approach integrating both palaeontological and neontological data, and large-scale datasets that contain information on the current distributions, phylogenetic relationships and fossil records for a total of 11,465 species. By reconstructing historical shifts in geographical ranges and climatic niches, we show that niche shifts are significantly faster in endotherms (birds and mammals) than in ectotherms (squamates and amphibians). We further demonstrate that the diversity patterns of the four clades are directly affected by the rate of niche evolution, with fewer latitudinal shifts in ectotherms.
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http://dx.doi.org/10.1038/s41559-017-0451-9DOI Listing
March 2018

Selection on the Major Color Gene Melanocortin-1-Receptor Shaped the Evolution of the Melanocortin System Genes.

Int J Mol Sci 2017 Dec 5;18(12). Epub 2017 Dec 5.

Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland.

Modular genetic systems and networks have complex evolutionary histories shaped by selection acting on single genes as well as on their integrated function within the network. However, uncovering molecular coevolution requires the detection of coevolving sites in sequences. Detailed knowledge of the functions of each gene in the system is also necessary to identify the selective agents driving coevolution. Using recently developed computational tools, we investigated the effect of positive selection on the coevolution of ten major genes in the melanocortin system, responsible for multiple physiological functions and human diseases. Substitutions driven by positive selection at the melanocortin-1-receptor () induced more coevolutionary changes on the system than positive selection on other genes in the system. Contrarily, selection on the highly pleiotropic POMC gene, which orchestrates the activation of the different melanocortin receptors, had the lowest coevolutionary influence. and possibly its main function, melanin pigmentation, seems to have influenced the evolution of the melanocortin system more than functions regulated by s such as energy homeostasis, glucocorticoid-dependent stress and anti-inflammatory responses. Although replication in other regulatory systems is needed, this suggests that single functional aspects of a genetic network or system can be of higher importance than others in shaping coevolution among the genes that integrate it.
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http://dx.doi.org/10.3390/ijms18122618DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5751221PMC
December 2017