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Delsuc, F.

Publications and source records attributed to Delsuc, F..

11 recordsLinked to original sources

Loss of the cytosolic DNA-sensing genes cGAS and STING1 inarmadillos (Cingulata)

The principal sensor of intracellular double-stranded DNA (dsDNA) is cyclic GMP-AMP synthase (CGAS), which generates the second messenger cyclic GMP-AMP that binds stimulator of interferon genes (STING1), leading to the expression of type I interferon genes. CGAS and STING1 also play essential roles in maintaining genome integrity and the initiation and progression of cancer. Here we show that CGAS and STING1 were pseudogenized in the ancestral armadillo branch 45 to 70 million years ago. The complete loss of the CGAS-STING1 pathway in armadillos suggests this lineage has evolved alternate ways to sense intracellular double-stranded DNA, which may be related to their extreme cancer resistance.

evolutionary biology↗

Pseudogenes document protracted parallel regression of oral anatomy in myrmecophagous mammals

Adaptation to ant and/or termite consumption (myrmecophagy) in mammals constitutes a textbook example of convergent evolution, being independently derived in several mammalian lineages. Myrmecophagous species are characterized by striking convergent morphological adaptations such as skull elongation, enlargement of salivary glands, and long claws to dig into ant and termite nests. These evolutionary modifications also include anatomical regression, such as dental simplification or loss, reduction of masticatory muscles, and possessing a reduced set of taste buds. To gain insights into the molecular changes underlying the regression of these morpho-anatomical traits, we investigated the functionality of candidate genes related to dentition, gustation, and mastication in nine convergent myrmecophagous mammalian lineages. We examined these genes in a comparative phylogenetic context, paired with molecular evolutionary analyses, to estimate the relative timing of loss of gene function over the evolutionary history of each convergent lineage. We found that gustatory reduction and pseudogenization of masticatory myosin often were associated with the regression of dental genes. Evidence of pseudogenization events linked to oral anatomy dates to as early as the Cretaceous/Paleogene boundary, and is an ongoing process including examples of incipient gene inactivations. Whereas we found evidence for gene inactivations across all three functional categories occurring during distinct temporal intervals, there was variation in the sets of genes lost and the relative timing of inactivation events. The combined evidence suggests that the convergent evolution of myrmecophagy has occurred as a protracted process with distinct phases of anatomical evolution, over timescales as long as 60 Myr.

evolutionary biology↗

Metagenomics uncovers dietary adaptations for chitin digestion in the gut microbiota of convergent myrmecophagous mammals

In mammals, myrmecophagy (ant and termite consumption) represents a striking example of dietary convergence. This trait evolved independently at least five times in placentals with myrmecophagous species comprising aardvarks, anteaters, some armadillos, pangolins, and aardwolves. The gut microbiome plays an important role in dietary adaptation, and previous analyses of 16S rRNA metabarcoding data have revealed convergence in the composition of the gut microbiota among some myrmecophagous species. However, the functions performed by these gut bacterial symbionts and their potential role in the digestion of prey chitinous exoskeletons remain open questions. Using long- and short-read sequencing of fecal samples, we generated 29 gut metagenomes from nine myrmecophagous and closely related insectivorous species sampled in French Guiana, South Africa, and the USA. From these, we reconstructed 314 high-quality bacterial genome bins of which 132 carried chitinase genes, highlighting their potential role in insect prey digestion. These chitinolytic bacteria belonged mainly to the family Lachnospiraceae, and some were likely convergently recruited in the different myrmecophagous species as they were detected in several host orders (i.e., Enterococcus faecalis, Blautia sp), suggesting that they could be directly involved in the adaptation to myrmecophagy. Others were found to be more host-specific, possibly reflecting phylogenetic constraints and environmental influences. Overall, our results highlight the potential role of the gut microbiome in chitin digestion in myrmecophagous mammals and provide the basis for future comparative studies performed at the mammalian scale to further unravel the mechanisms underlying the convergent adaptation to myrmecophagy. ImportanceMyrmecophagous mammals are specialized in the consumption of ants and/or termites. They do not share a direct common ancestor and evolved convergently in five distinct placental orders raising questions about the underlying adaptive mechanisms involved and the relative contribution of natural selection and phylogenetic constraints. Understanding how these species digest their prey can help answer these questions. More specifically, the role of their gut microbial symbionts in the digestion of the insect chitinous exoskeleton has not been investigated in all myrmecophagous orders. We generated 29 new gut metagenomes from nine myrmecophagous species to reconstruct more than 300 bacterial genomes in which we identified chitin-degrading enzymes. Studying the distribution of these chitinolytic bacteria among hosts revealed both shared and specific bacteria between ant-eating species. Overall, our results highlight the potential role of gut symbionts in the convergent dietary adaptation of myrmecophagous mammals and the evolutionary mechanisms shaping their gut microbiota.

evolutionary biology↗

Pangolin genomes offer key insights and resources for the world's most trafficked wild mammals

Pangolins form a group of scaly mammals that are trafficked at record numbers for their meat and medicinal properties. Despite their great conservation concern, knowledge of their evolution is limited by a paucity of genomic data. We aim to produce exhaustive genomic resources that include 3 238 orthologous genes and whole-genome polymorphisms to assess the evolution of all eight pangolin species. Robust orthologous gene-based phylogenies recovered the monophyly of the three genera of pangolins, and highlighted the existence of an undescribed species closely related to South-East Asian pangolins. Signatures of middle Miocene admixture between an extinct, possibly European, lineage and the ancestor of South-East Asian pangolins, provides new insights into the early evolutionary history of the group. Demographic trajectories and genome-wide heterozygosity estimates revealed contrasts between continental vs. island populations and species lineages, suggesting that conservation planning should consider intra-specific patterns. With the expected loss of genomic diversity from recent, extensive trafficking not yet been realized in pangolins, we recommend that populations are genetically surveyed to anticipate any deleterious impact of the illegal trade. Finally, we produce a complete set of genomic resources that will be integral for future conservation management and forensic endeavors required for conserving pangolins, including tracing their illegal trade. These include the completion of whole-genomes for pangolins through the first reference genome with long reads for the giant pangolin (Smutsia gigantea) and new draft genomes (~43x-77x) for four additional species, as well as a database of orthologous genes with over 3.4 million polymorphic sites.

genomics↗

PhylteR: efficient identification of outlier sequences in phylogenomic datasets

In phylogenomics, incongruences between gene trees, resulting from both artifactual and biological reasons, can decrease the signal-to-noise ratio and complicate species tree inference. The amount of data handled today in classical phylogenomic analyses precludes manual error detection and removal. However, a simple and efficient way to automate the identification of outliers from a collection of gene trees is still missing. Here, we present PhylteR, a method that allows a rapid and accurate detection of outlier sequences in phylogenomic datasets, i.e. species from individual gene trees that do not follow the general trend. PhylteR relies on DISTATIS, an extension of multidimensional scaling to 3 dimensions to compare multiple distance matrices at once. In PhylteR, these distance matrices extracted from individual gene phylogenies represent evolutionary distances between species according to each gene. On simulated datasets, we show that PhylteR identifies outliers with more sensitivity and precision than a comparable existing method. We also show that PhylteR is not sensitive to ILS-induced incongruences, which is a desirable feature. On a biological dataset of 14,463 genes for 53 species previously assembled for Carnivora phylogenomics, we show (i) that PhylteR identifies as outliers sequences that can be considered as such by other means, and (ii) that the removal of these sequences improves the concordance between the gene trees and the species tree. Thanks to the generation of numerous graphical outputs, PhylteR also allows for the rapid and easy visual characterisation of the dataset at hand, thus aiding in the precise identification of errors. PhylteR is distributed as an R package on CRAN and as containerized versions (docker and singularity).

evolutionary biology↗

Genomic data suggest parallel dental vestigialization within the xenarthran radiation

AO_SCPLOWBSTRACTC_SCPLOWThe recent influx of genomic data has provided greater insights into the molecular basis for regressive evolution, or vestigialization, through gene loss and pseudogenization. As such, the analysis of gene degradation patterns has the potential to provide insights into the evolutionary history of regressed anatomical traits. We specifically applied these principles to the xenarthran radiation (anteaters, sloths, armadillos), which is characterized by taxa with a gradation in regressed dental phenotypes. Whether the pattern among extant xenarthrans is due to an ancient and gradual decay of dental morphology or occurred repeatedly in parallel is unknown. We tested these competing hypotheses by examining 11 core dental genes in most living species of Xenarthra, characterizing shared inactivating mutations and patterns of relaxed selection during their radiation. Here we report evidence of independent and distinct events of dental gene loss in the major xenarthran subclades. First, we found strong evidence of complete enamel loss in the common ancestor of sloths and anteaters, suggested by the inactivation of five enamel-associated genes (AMELX, AMTN, MMP20, ENAM, ACP4). Next, whereas dental regression appears to have halted in sloths, presumably a critical event that ultimately permitted adaptation to an herbivorous lifestyle, anteaters continued losing genes on the path towards complete tooth loss. Echoes of this event are recorded in the genomes of all living anteaters, being marked by a 2-bp deletion in a gene critical for dentinogenesis (DSPP) and a putative shared 1-bp insertion in a gene linked to tooth retention (ODAPH). By contrast, in the two major armadillo clades, genes pertaining to the dento-gingival junction and amelogenesis appear to have been independently inactivated prior to losing all or some enamel. These genomic data provide evidence for multiple pathways and rates of anatomical regression, and underscore the utility of using pseudogenes to reconstruct evolutionary history when fossils are sparse.

evolutionary biology↗

Comparative transcriptomics reveals divergent paths of chitinase evolution underlying dietary convergence in ant-eating mammals

Ant-eating mammals represent a textbook example of convergent evolution. Among them, anteaters and pangolins exhibit the most extreme convergent phenotypes with complete tooth loss, elongated skulls, protruding tongues, hypertrophied salivary glands producing large amounts of saliva, and powerful claws for ripping open ant and termite nests. However, comparative genomic analyses have shown that anteaters and pangolins differ in their chitinase acidic gene (CHIA) repertoires, which potentially degrade the chitinous exoskeletons of ingested ants and termites. While the southern tamandua (Tamandua tetradactyla) harbors four functional CHIA paralogs (CHIA1-4), Asian pangolins (Manis spp.) have only one functional paralog (CHIA5). Here, we performed a comparative transcriptomic analysis of salivary glands in 33 placental species, including 16 novel transcriptomes from ant-eating species and close relatives. Our results suggest that salivary glands play an important role in adaptation to an insect-based diet, as expression of different CHIA paralogs is observed in insectivorous species. Furthermore, convergently-evolved pangolins and anteaters express different chitinases in their digestive tracts. In the Malayan pangolin, CHIA5 is overexpressed in all major digestive organs, whereas in the southern tamandua, all four functional paralogs are expressed, at very high levels for CHIA1 and CHIA2 in the pancreas, and for CHIA3 and CHIA4 in the salivary glands, stomach, liver, and pancreas. Overall, our results demonstrate that divergent molecular mechanisms within the chitinase acidic gene family underlie convergent adaptation to the ant-eating diet in pangolins and anteaters. This study highlights the role of historical contingency and molecular tinkering of the chitin-digestive enzyme toolkit in this classic example of convergent evolution.

evolutionary biology↗

The origin and drivers of Neotropical plant and tetrapod diversification

The origins and evolution of the outstanding Neotropical biodiversity are still debated. A comprehensive understanding is hindered by the lack of deep-time comparative data across wide phylogenetic and ecological contexts. Here, we evaluate four evolutionary scenarios assuming different diversification trajectories and drivers of Neotropical diversification, and assess their variation across Neotropical regions and taxa. Our analysis of 150 phylogenies (12,512 species) of seed plants and tetrapods reveals that Neotropical diversity has mostly expanded through time (70% of the clades), while scenarios of saturated and declining diversity also account for 21% and 9% of Neotropical diversity, respectively. We identify five biogeographic areas that represent distinctive units of long-term Neotropical evolution (Pan-Amazonia, Dry Diagonal, Bahama-Antilles, Galapagos, and an elsewhere region) and find that diversity dynamics do not differ across these areas, suggesting no geographic structure in long-term Neotropical diversification. In contrast, diversification dynamics differ substantially across taxa: plant diversity mostly expanded through time (88%), while a substantial fraction (43%) of tetrapod diversity accumulated at a slower pace or declined toward the present. These opposite evolutionary patterns may reflect different capacities for plants and tetrapods to cope with climate change, with potential implications for future adaptation and ecosystem resilience.

evolutionary biology↗

High-quality carnivore genomes from roadkill samples enable species delimitation in aardwolf and bat-eared fox

In a context of ongoing biodiversity erosion, obtaining genomic resources from wildlife is becoming essential for conservation. The thousands of yearly mammalian roadkill could potentially provide a useful source material for genomic surveys. To illustrate the potential of this underexploited resource, we used roadkill samples to sequence reference genomes and study the genomic diversity of the bat-eared fox (Otocyon megalotis) and the aardwolf (Proteles cristata) for which subspecies have been defined based on similar disjunct distributions in Eastern and Southern Africa. By developing an optimized DNA extraction protocol, we successfully obtained long reads using the Oxford Nanopore Technologies (ONT) MinION device. For the first time in mammals, we obtained two reference genomes with high contiguity and gene completeness by combining ONT long reads with Illumina short reads using hybrid assembly. Based on re-sequencing data from few other roakill samples, the comparison of the genetic differentiation between our two pairs of subspecies to that of pairs of well-defined species across Carnivora showed that the two subspecies of aardwolf might warrant species status (P. cristata and P. septentrionalis), whereas the two subspecies of bat-eared fox might not. Moreover, using these data, we conducted demographic analyses that revealed similar trajectories between Eastern and Southern populations of both species, suggesting that their population sizes have been shaped by similar environmental fluctuations. Finally, we obtained a well resolved genome-scale phylogeny for Carnivora with evidence for incomplete lineage sorting among the three main arctoid lineages. Overall, our cost-effective strategy opens the way for large-scale population genomic studies and phylogenomics of mammalian wildlife using roadkill.

evolutionary biology↗

MitoFinder: efficient automated large-scale extraction of mitogenomic data in target enrichment phylogenomics

Thanks to the development of high-throughput sequencing technologies, target enrichment sequencing of nuclear ultraconserved DNA elements (UCEs) now allows routinely inferring phylogenetic relationships from thousands of genomic markers. Recently, it has been shown that mitochondrial DNA (mtDNA) is frequently sequenced alongside the targeted loci in such capture experiments. Despite its broad evolutionary interest, mtDNA is rarely assembled and used in conjunction with nuclear markers in capture-based studies. Here, we developed MitoFinder, a user-friendly bioinformatic pipeline, to efficiently assemble and annotate mitogenomic data from hundreds of UCE libraries. As a case study, we used ants (Formicidae) for which 501 UCE libraries have been sequenced whereas only 29 mitogenomes are available. We compared the efficiency of four different assemblers (IDBA-UD, MEGAHIT, MetaSPAdes, and Trinity) for assembling both UCE and mtDNA loci. Using MitoFinder, we show that metagenomic assemblers, in particular MetaSPAdes, are well suited to assemble both UCEs and mtDNA. Mitogenomic signal was successfully extracted from all 501 UCE libraries allowing confirming species identification using COI barcoding. Moreover, our automated procedure retrieved 296 cases in which the mitochondrial genome was assembled in a single contig, thus increasing the number of available ant mitogenomes by an order of magnitude. By leveraging the power of metagenomic assemblers, MitoFinder provides an efficient tool to extract complementary mitogenomic data from UCE libraries, allowing testing for potential mito-nuclear discordance. Our approach is potentially applicable to other sequence capture methods, transcriptomic data, and whole genome shotgun sequencing in diverse taxa.

evolutionary biology↗

A phylogenomic framework and timescale for comparative genomics and evolutionary developmental biology of tunicates

BackgroundTunicates are the closest relatives of vertebrates and are widely used as models to study the evolutionary developmental biology of chordates. Their phylogeny, however, remains poorly understood and to date, only the 18S rRNA nuclear gene and mitogenomes have been used to delineate the major groups of tunicates. To resolve their evolutionary relationships and provide a first estimate of their divergence times, we used a transcriptomic approach to build a phylogenomic dataset including all major tunicate lineages, consisting of 258 evolutionarily conserved orthologous genes from representative species.\n\nResultsPhylogenetic analyses using site-heterogeneous CAT mixture models of amino acid sequence evolution resulted in a strongly supported tree topology resolving the relationships among four major tunicate clades: 1) Appendicularia, 2) Thaliacea + Phlebobranchia + Aplousobranchia, 3) Molgulidae, and 4) Styelidae + Pyuridae. Notably, the morphologically derived Thaliacea are confirmed as the sister-group of the clade uniting Phlebobranchia + Aplousobranchia within which the precise position of the model ascidian genus Ciona remains uncertain. Relaxed molecular clock analyses accommodating the accelerated evolutionary rate of tunicates reveal ancient diversification (~450-350 million years ago) among the major groups and allow comparing their evolutionary age with respect to the major vertebrate model lineages.\n\nConclusionsOur study represents the most comprehensive phylogenomic dataset for the main tunicate lineages. It offers a reference phylogenetic framework and first tentative timescale for tunicates, allowing the direct comparison with vertebrate model species in comparative genomics and evolutionary developmental biology studies.

evolutionary biology↗