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Romiguier, J.

Publications and source records attributed to Romiguier, J..

11 recordsLinked to original sources

Phylogenomics of Messor harvester ants (Hymenoptera: Formicidae: Stenammini) unravels their biogeographical origin and diversification patterns

As a major abiotic factor, climate change is expected to profoundly alter biological communities. On this basis, identifying how past temperature variations affected species diversification and distribution can help to predict the effects of the ongoing climate change. In this study, we focused on the harvester ant genus Messor which is mostly adapted to dry environments dominated by seed-producing plants. The phylogenetic analysis of 2,524 markers obtained from 58 Messor species/subspecies, supports their emergence in the Irano-Indian area approximately 20 Mya. Phylogenetic relationships uncovered in this study enabled us to redefine historical taxonomic groups, providing a solid basis for future revisions that encompass the entire genus diversity. Their diversification appears to be affected by temperature, with a higher speciation rate during warmer periods. This confirms that the ecological specialization of Messor makes them strongly dependent on thermal conditions. Our results highlight the importance of abiotic factors on diversification processes, especially for highly specialized species that may exhibit predictable evolutionary responses to climate changes.

evolutionary biology↗

Social evolution in termites reduces natural selection efficacy

In eusocial species, reproduction is monopolized by a few reproductive individuals. From the perspective of population genetics, this implies that the effective population size (Ne) of these organisms is likely to be smaller compared to solitary species, as has been proposed in the literature for eusocial hymenoptera. In this study, we investigate the genomic consequences of eusociality in termites (Isoptera) on two different timescales. First, by analyzing transcriptome data from 66 Blattodea species, we focus on the ratio of non-synonymous to synonymous mutations (dN/dS) as a marker of natural selection efficiency and effective population size. Our results demonstrate an elevated dN/dS ratio in termites compared to other members of Blattodea, further generalizing the idea that convergent evolution toward eusociality strongly reduces the effective population size and the genome-wide efficiency of natural selection. Then, by comparing 68 termite transcriptomes, we show that this decrease in natural selection efficiency is even more pronounced in termites displaying high levels of social complexity. This study contributes to understanding the complex interplay between social structures and natural selection patterns, highlighting the genetic footprint of eusociality in shaping the evolution of termites.

evolutionary biology↗

Detection of F1 hybrids from single-genome data reveals frequent hybridization in Hymenoptera and particularly ants

Hybridization occupies a central role in many fundamental evolutionary processes, such as speciation or adaptation. Yet, despite its pivotal importance in evolution, little is known about the actual prevalence and distribution of hybridization across the tree of life. Here we develop and implement a new statistical method enabling the detection of F1 hybrids from single-individual genome sequencing data. Using simulations and sequencing data from known hybrid systems, we first demonstrate the specificity of the method, and identify its statistical limits. Next, we showcase the method by applying it to available sequencing data from more than 1500 species of Arthropods, including Hymenoptera, Hemiptera, Coleoptera, Diptera and Archnida. Among these taxa, we find Hymenoptera, and especially ants, to display the highest number of candidate F1 hybrids, suggesting higher rates of recent hybridization in these groups. The prevalence of F1 hybrids was heterogeneously distributed across ants, with taxa including many candidates tending to harbor specific ecological and life history traits. This work shows how large-scale genomic comparative studies of recent hybridization can be implemented, uncovering the determinants of hybridization frequency across whole taxa.

evolutionary biology↗

Hybridization enables the fixation of selfish queen genotypes in eusocial colonies

A eusocial colony typically consists of two main castes: queens that reproduce and sterile workers that help them. This division of labour however is vulnerable to genetic elements that favour the development of their carriers into queens. Several factors, such as intra-colonial relatedness, can modulate the spread of such caste-biasing genotypes. Here we investigate the effects of a notable yet understudied ecological setting: where larvae produced by hybridization develop into sterile workers. Using mathematical modelling, we show that the coevolution of hybridization with caste determination readily triggers an evolutionary arms race between non-hybrid larvae that increasingly develop into queens, and queens that increasingly hybridize to produce workers. Even where hybridization reduces worker function and colony fitness, this race can lead to the loss of developmental plasticity and to genetically hard-wired caste determination. Overall, our results may help understand the repeated evolution towards remarkable reproductive systems (e.g. social hybridogenesis) observed in many ant species.

evolutionary biology↗

DILS : Demographic Inferences with Linked Selection by using ABC

We present DILS, a deployable statistical analysis platform for conducting demographic inferences with linked selection from population genomic data using an Approximate Bayesian Computation framework. DILS takes as input single-population or two-population datasets (multilocus fasta sequences) and performs three types of analyses in a hierarchical manner, identifying: 1) the best demographic model to study the importance of gene flow and population size change on the genetic patterns of polymorphism and divergence, 2) the best genomic model to determine whether the effective size Ne and migration rate N.m are heterogeneously distributed along the genome (implying linked selection) and 3) loci in genomic regions most associated with barriers to gene flow. Also available via a web interface, an objective of DILS is to facilitate collaborative research in speciation genomics. Here, we show the performance and limitations of DILS by using simulations, and finally apply the method to published data on a divergence continuum composed by 28 pairs of Mytilus mussel populations/species.

evolutionary biology↗

Relaxation of purifying selection suggests low effective population size in eusocial Hymenoptera and pollinating bees

With one of the highest number of parasitic, eusocial and pollinator species among all insect orders, Hymenoptera features a great diversity of lifestyles. At the population genetic level, such life-history strategies are expected to decrease effective population size and the efficiency of purifying selection. In this study, we tested this hypothesis by estimating the relative rate of non-synonymous substitution in 169 species to investigate the variation in natural selection efficiency throughout the hymenopteran tree of life. We found no effect of parasitism, but we show that relaxed selection is associated with eusociality, suggesting that the division of reproductive labour decreases effective population size in ants, bees and wasps. Unexpectedly, the effect of eusociality is marginal compared to a striking and widespread relaxation of selection in both social and non social bees, which indicates that these keystone pollinator species generally feature low effective population sizes. This widespread pattern suggests specific constraints in pollinating bees potentially linked to limited resource availability and high parental investment. The particularly high load of deleterious mutations we report in the genome of these crucial ecosystem engineer species also raises new concerns about their ongoing population decline. This article has been peer-reviewed and recommended by Peer Community in Evolutionary Biology https://doi.org/10.24072/pci.evolbiol.100120

evolutionary biology↗

Vulnerability correlates with life history traits and the load of deleterious mutations in fish.

Understanding why some species accumulate more deleterious substitutions than others is an important question relevant in evolutionary biology and conservation sciences. Previous studies conducted in terrestrial taxa suggest that life history traits correlate with the efficiency of purifying selection and accumulation of deleterious mutations. Using a large genome dataset of 76 species of fishes, we show that the rate of deleterious mutation accumulation (measured via dN/dS, i.e. non-synonymous over synonymous substitution rate) is associated to the vulnerability, the life-history strategies, and the latitude of species. Our results, focusing on a large clade of aquatic species, generalizes previous patterns found so far in few clades of terrestrial vertebrates. These results also suggest that vulnerable species accumulate more deleterious substitutions than non-threatened ones, which give insights in how life-history traits, populations sizes and genetic risk of extinction can be tightly interconnected.

molecular biology↗

Evolutionary history of the porpoises (Phocoenidae) across the speciation continuum: a mitogenome phylogeographic perspective

Historical changes affecting food resources are a major driver of cetacean evolution. Small cetaceans like porpoises (Phocoenidae) are among the most metabolically challenged marine mammals and are particularly sensitive to changes in their food resources. The seven species of this family inhabit mostly temperate waters and constitute a textbook example of antitropical distribution. Yet, their evolutionary history remains poorly known despite major conservation issues threatening the survival of some porpoises (e.g., vaquita and Yangzte finless porpoises). Here, we reconstructed their evolutionary history across the speciation continuum, from intraspecific subdivisions to species divergence. Phylogenetic analyses of 63 mitochondrial genomes suggest that, like other toothed whales, porpoises radiated during the Pliocene in response to deep environmental changes. However, all intra-specific phylogeographic patterns were shaped during the Quaternary Glaciations. We observed analogous evolutionary patterns in both hemispheres associated with convergent adaptations to coastal versus oceanic environments. This result suggests that the mechanism(s) driving species diversification in the relatively well-known species from the northern hemisphere may apply also to the poorly-known southern species. In contrast to previous studies, we showed that the spectacled and Burmeisters porpoises share a more recent common ancestor than with the vaquita that diverged from southern species during the Pliocene. The low genetic diversity observed in the vaquita carried signatures of a very low population size throughout at least the last 5,000 years, leaving one single relict mitochondrial lineage. Finally, we observed unreported subspecies level divergence within Dalls, spectacled and Pacific harbor porpoises, suggesting a richer evolutionary history than previously suspected. These results provide a new perspective on the mechanism driving the adaptation and speciation processes involved in the diversification of cetacean species. This knowledge can illuminate their demographic trends and provide an evolutionary framework for their conservation.

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↗

Assessing the impact of high-throughput sequencing strategy and model complexity on ABC-inferred demographic history in mussels

Genome-scale diversity data are increasingly available in a variety of biological systems, and can be used to reconstruct the past evolutionary history of species divergence. However, extracting the full demographic information from these data is not trivial, and requires inferential methods that account for the diversity of coalescent histories throughout the genome. Here, we evaluate the potential and limitations of one such approach. We reexamine a well-known system of mussel sister species, using the joint site frequency spectrum (jSFS) of synonymous mutations computed either from exome capture or RNA-seq, in an Approximate Bayesian Computation (ABC) framework. We first assess the best sampling strategy (number of: individuals, loci, and bins in the jSFS), and show that model selection is robust to variation in the number of individuals and loci. In contrast, different binning choices when summarizing the joint site frequency spectrum, strongly affect the results: including classes of low and high frequency shared polymorphisms can more effectively reveal recent migration events. We then take advantage of the flexibility of ABC to compare more realistic models of speciation, including variation in migration rates through time (i.e. periodic connectivity) and across genes (i.e. genome-wide heterogeneity in migration rates). We show that these models were consistently selected as the most probable, suggesting that mussels have experienced a complex history of gene flow during divergence and that the species boundary is semi-permeable. Our work provides a comprehensive evaluation of ABC demographic inference in mussels based on the coding site frequency spectrum, and supplies guidelines for employing different sequencing techniques and sampling strategies. We emphasize, perhaps surprisingly, that inferences are less limited by the volume of data, than by the way in which they are analyzed.

evolutionary biology↗

Codon usage bias in animals: disentangling the effects of natural selection, effective population size and GC-biased gene conversion

Selection on codon usage bias is well documented in a number of microorganisms. Whether codon usage is also generally shaped by natural selection in large organisms, despite their relatively small effective population size (Ne), is unclear. Codon usage bias in animals has only been studied in a handful of model organisms so far, and can be affected by confounding, non-adaptive processes such as GC-biased gene conversion and experimental artefacts. Using population transcriptomics data we analysed the relationship between codon usage, gene expression, allele frequency distribution and recombination rate in 31 non-model species of animals, each from a different family, covering a wide range of effective population sizes. We disentangled the effects of translational selection and GC-biased gene conversion on codon usage by separately analysing GC-conservative and GC-changing mutations. We report evidence for effective translational selection on codon usage in large-Ne species of animals, but not in small-Ne ones, in agreement with the nearly neutral theory of molecular evolution. C- and T-ending codons are generally preferred over synonymous G- and A-ending ones, for reasons that remain to be determined. In contrast, we uncovered a conspicuous effect of GC-biased gene conversion, which is widespread in animals and the main force determining the fate of AT{leftrightarrow}GC mutations. Intriguingly, the strength of its effect was uncorrelated with Ne.

evolutionary biology↗