Author: Nicolas Salamin

Paper by Duchen et al. on “Linking micro and macroevolution in the presence of migration”.

Abstract: 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.

Paper by Yamada et al. on “Duplication history and molecular evolution of the rbcS multigene family in angiosperms” published in Journal of Experimental Botany.

Abstract: Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) is considered to be the main molecule determining the rate of photosynthesis. The small subunit of the protein, encoded by the rbcS gene, was shown to influence the catalytic efficiency, CO2 specificity, assembly, activity, and stability of RuBisCO. However, the evolution of the rbcS gene is yet 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 the intensive coevolution between each rbcS gene copies 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.

Paper by Silvestro et al. on “Improved estimation of macroevolutionary rates from fossil data using a Bayesian framework” published in Paleobiology.

Abstract: 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 only 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. Building upon this framework, we present a suite of methodological advances including more complex and realistic models of preservation and the first likelihood-based test to compare the fit across different models. Further, we develop a new reversible jump Markov chain Monte Carlo algorithm to estimate origination and extinction rates and their temporal variation, which provides more reliable results and includes an explicit estimation of the number and temporal placement of statistically significant rate changes. Finally, we implement a new C++ library that speeds up the analyses by orders of magnitude, therefore facilitating the application of the PyRate methods to large data sets. We demonstrate the new functionalities through extensive simulations and with the analysis of a large data set of Cenozoic marine mammals. We compare our analytical framework against two widely used alternative methods to infer origination and extinction rates, revealing that PyRate decisively outperforms them across a range of simulated data sets. 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.

Alberto is starting a PhD project on the evolution of ecological preferences and population genomics of clownfishes.

Paper published by Davydov et al. on “Large-scale comparative analysis of codon models accounting for protein and nucleotide selection” published in Molecular Biology and Evolution.

Abstract: 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.

Sara is starting a PhD project in the group on the metabolomics and transcriptomics of the clownfish adaptation to sea anemone.

Paper by Marcionetti et al. on “?Insights into the genomics of clownfish adaptive radiation: genetic basis of the mutualism with sea anemones” just accepted in Genome Biology and Evolution.

Abstract: 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.

New paper by Meyer et al. on “Simultaneous Bayesian inference of phylogeny and molecular coevolution” in PNAS.

Abstract: 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.

New paper by Salis et al. on “Developmental and comparative transcriptomic identification of iridophore contribution to white barring in clownfish” in Pigment Cell Melanoma Res.

Abstract: 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.