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Bierne, N.

Publications and source records attributed to Bierne, N..

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Analysis of genome-wide differentiation between native and introduced populations of the cupped oysters Crassostrea gigas and Crassostrea angulata

The Pacific cupped oyster is genetically subdivided into two sister taxa, Crassostrea gigas and C. angulata, which are in contact in the north-western Pacific. The nature and origin of their genetic and taxonomic differentiation remains controversial due the lack of known reproductive barriers and morphologic similarity. In particular, whether ecological and/or intrinsic isolating mechanisms participate to species divergence remains unknown. The recent co-introduction of both taxa into Europe offers a unique opportunity to test how genetic differentiation maintains under new environmental and demographic conditions. We generated a pseudo-chromosome assembly of the Pacific oyster genome using a combination of BAC-end sequencing and scaffold anchoring to a new high-density linkage map. We characterized genome-wide differentiation between C. angulata and C. gigas in both their native and introduced ranges, and showed that gene flow between species has been facilitated by their recent co-introductions in Europe. Nevertheless, patterns of genomic divergence between species remain highly similar in Asia and Europe, suggesting that the environmental transition caused by the co-introduction of the two species did not affect the genomic architecture of their partial reproductive isolation. Increased genetic differentiation was preferentially found in regions of low recombination. Using historical demographic inference, we show that the heterogeneity of differentiation across the genome is well explained by a scenario whereby recent gene flow has eroded past differentiation at different rates across the genome after a period of geographical isolation. Our results thus support the view that low-recombining regions help in maintaining intrinsic genetic differences between the two species.

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

Fine-grained genetic-environment association in an admixed population of mussels in the small isolated Kerguelen island

Reticulated evolution -i.e. secondary introgression / admixture between sister taxa-is increasingly recognized as a key evolutionary process that may play a role in structuring infra-specific genetic variation, and possibly promoting adaptation. Mytilus spp. is an ideal system to assess its importance, because these marine mussels form semi-isolated species that remain reproductively compatible over large time-scales. It includes three taxa that hybridize in the Northern Hemisphere (M. edulis, M. galloprovincialis and M. trossulus) and two taxa of uncertain ancestry in the Southern Hemisphere (M. platensis: South America and the Kerguelen Islands; and M. planulatus: Australasia). The Kerguelen mussels are of particular interest to investigate the potential role of admixture in enhancing micro-geographic structure, as they inhabit a small and isolated island in the Southern Ocean characterized by a highly heterogeneous environment, and genomic reticulation between Northern and Southern lineages has been suspected. Here, we extended a previous analysis by using targeted-sequencing data (51,878 SNPs) across the three Northern species and the Kerguelen population, coupled with a panel of 33 SNPs genotyped on 695 mussels across 35 sites in the Kerguelen Islands. The panel was enriched with ancestry-informative SNPs, i.e. SNPs that were more differentiated than the genomic average between Northern lineages, to evaluate whether reticulated evolution contributed to micro-geographic structure. We first showed that the Kerguelen population belongs to a divergent Southern lineage, most related to M. edulis mussels, that experienced secondary admixture with non-indigenous Northern species. We then demonstrated that the Kerguelen mussels were significantly differentiated over small spatial distance, and that this local genetic structure was associated with environmental variation and mostly revealed by ancestry-informative markers. Although local adaptation can explain the association with the environment we believe it more likely that environment variables better describe population connectivity than geographic distance. Our study highlights genetic connectivity of populations is more easily revealed by non-equilibrium secondary introgression clines at a subset of loci, while association with the environment should not be hastily advocated to support adaptation from admixture variation.

evolutionary biology

Coadapted genomes and selection on hybrids: Fisher’s geometric model explains a variety of empirical patterns

Natural selection plays a variety of roles in hybridization, speciation and admixture. Most research has focused on two extreme cases: crosses between closely-related inbred lines, where hybrids are fitter than their parents, or crosses between effectively isolated species, where hybrids suffer severe breakdown. Many natural populations must fall into intermediate regimes, with multiple types of gene interaction, but these are more difficult to study. Here, we develop a simple fitness landscape model, and show that it naturally interpolates between previous modeling approaches, involving mildly deleterious recessives, or discrete hybrid incompatibilities. The model yields several new predictions, which we test with genomic data from Mytilus mussels, and published data from plants (Zea, Populus and Senecio) and animals (Mus, Teleogryllus and Drosophila). The predictions are generally supported, and the model explains surprising empirical patterns that have been observed in both extreme regimes. Our approach enables novel and complementary uses of genome-wide datasets, which do not depend on identifying outlier loci, or \"speciation genes\" with anomalous effects. Given its simplicity and flexibility, and its predictive successes with a wide range of data, the approach should be readily extendable to other outstanding questions in the study of hybridization.

evolutionary biology

The origin and remolding of genomic islands of differentiation in the European sea bass

Speciation is a complex process that leads to the progressive establishment of reproductive isolation barriers between diverging populations. Genome-wide comparisons between closely related species have revealed the existence of heterogeneous divergence patterns, dominated by genomic islands of increased divergence supposed to contain reproductive isolation loci. However, this divergence landscape only provides a static picture of the dynamic process of speciation, during which confounding mechanisms unlinked to speciation can interfere. Here, we used haplotype-resolved whole-genome sequences to identify the mechanisms responsible for the formation of genomic islands between Atlantic and Mediterranean sea bass lineages. We show that genomic islands first emerged in allopatry through the effect of linked selection acting on a heterogeneous recombination landscape. Upon secondary contact, preexisting islands were strongly remolded by differential introgression, revealing variable fitness effects among regions involved in reproductive isolation. Interestingly, we found that divergent regions containing ancient polymorphisms conferred the strongest resistance to introgression.

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

Parallel use of a shared genomic island of speciation in clinal and mosaic hybrid zones between cryptic seahorse lineages

Diverging semi-isolated lineages either meet in narrow clinal hybrid zones, or have a mosaic distribution associated with environmental variation. Intrinsic reproductive isolation is often emphasized in the former and local adaptation in the latter, although both can contribute to isolation. Rarely these two patterns of spatial distribution are reported in the same study system. Here we report that the long-snouted seahorse Hippocampus guttulatus is subdivided into discrete panmictic entities by both types of hybrid zones. Along the European Atlantic coasts, a northern and a southern lineage meet in the southwest of France where they coexist in sympatry with little hybridization. In the Mediterranean Sea, two lineages have a mosaic distribution, associated with lagoon-like and marine habitats. A fifth lineage was identified in the Black Sea. Genetic homogeneity over large spatial scales contrasts with isolation maintained in sympatry or close parapatry at a fine scale. A high variation in locus-specific introgression rates provides additional evidence that partial reproductive isolation must be maintaining the divergence. Surprisingly, fixed differences between lagoon and marine populations in the Mediterranean Sea belong to the most differentiated SNPs between the two Atlantic lineages, against the genome-wide pattern of structure. These parallel outlier SNPs cluster on a single chromosome-wide island of differentiation. Since Atlantic lineages do not match the lagoon-sea habitat variation, genetic parallelism at the genomic island suggests a shared genetic barrier contributes to reproductive isolation in contrasting contexts -i.e. spatial vs. ecological. We discuss how a genomic hotspot of parallel differentiation could have evolved and become associated either with space or with a patchy environment in a single study system.

evolutionary biology