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Nouhaud, P.

Publications and source records attributed to Nouhaud, P..

15 recordsLinked to original sources

Genomic signatures of selection and putative adaptive introgression during the African expansion of the house mouse

How species adapt to novel environments following biological invasion remains a central question in evolutionary biology. The recent human-mediated expansion of the western house mouse (Mus musculus domesticus) across Africa provides an opportunity to investigate the genomic basis of these rapid evolutionary responses. Using whole-genome data from 218 wild mice sampled across Europe and Africa, we combined complementary genome-wide differentiation, genotype-environment association, haplotype-based selection, and localized introgression analyses to investigate genomic signatures of selection and assess the contribution of interspecific gene flow from the native congener Mus spretus to these patterns. Genome-wide differentiation analyses identified candidate regions enriched for immune and epithelial-barrier functions, chemosensory perception, and neural or developmental pathways. Genotype-environment association analyses recovered fewer candidates linked mainly to precipitation, whereas haplotype-based scans highlighted recent selective signals involving sensory, immune, and neural functions. Across analyses, candidate regions were dominated by non-coding variation, supporting a predominantly regulatory and likely polygenic genomic architecture. Although excess allele sharing with M. spretus varied among populations, overlap between introgression and selection candidates was limited but greater than expected by chance. Several overlapping regions were also present in European populations, indicating that introgressed variants likely predated African colonization. Overall, our results suggest that the genomic signatures accompanying the African expansion of house mice were driven mainly by selection on M. m. domesticus variation, whereas introgressed M. spretus alleles contributed to a smaller subset of candidate loci and may have played a role in adaptation in African populations.

evolutionary biology↗

An annotated chromosome-level genome assembly ofthe Adzuki bean borer Ostrinia scapulalis (Lepidoptera: Crambidae)

The genus Ostrinia (Lepidoptera: Crambidae) comprises two of the most important maize pests worldwide, the Asian and the European corn borers. Here, we present an annotated, chromosome-level genome assembly for the most closely related species, the Adzuki bean borer Ostrinia scapulalis, which feeds on various dicotyledon plants. The previous reference genome assembly for this species was generated from short-read sequencing data, resulting in high fragmentation and low completeness. Combining PacBio long read and Hi-C sequencing, we generated a 476 Mb genome with 48 contigs organised into 31 chromosomes (30 autosomes and one Z sex chromosome), with a contig N50 of 16.1 Mbp and BUSCO completeness exceeding 98%. We further combined published and novel RNA-seq data encompassing multiple life stages, tissues, and sexes to annotate 14,261 gene models, reaching a proteome BUSCO completeness of 95%. This highly contiguous reference genome assembly provides a much-improved resource for carrying comparative genomic approaches and better understanding speciation and host plant adaptation in the Ostrinia genus.

evolutionary biology↗

A major selective sweep likely linked to insecticide resistance identified along altitudinal gradients in the pine processionary moth

Understanding how natural populations adapt to complex environmental gradients is crucial for predicting evolutionary responses to global change. The pine processionary moth (Thaumetopoea pityocampa), a major forest pest expanding northward and upward in Europe, provides an ideal model to explore genomic adaptation along altitudinal and/or latitudinal gradients. We combined pooled and individual whole- genome resequencing of four pairs of low- and high-elevation populations from Spain, Italy and France (mainland and Corsica) to detect signatures of local adaptation. Population structure analyses revealed strong differentiation among distant populations but limited divergence within altitude pairs. Genome scans identified a few candidate regions under selection, and we notably uncovered a large (~1 Mbp) region showing reduced nucleotide diversity, negative Tajima's D, and fixed allele differences between high- and low-altitude populations, consistent with a recent selective sweep. This region includes a cluster of cytochrome P450 genes and the voltage-gated sodium channel gene para, both involved in detoxification and insecticide resistance. Although signatures of selection were observed at this locus in two distant population pairs, no definitive evidence of recent introgression was found between these distant populations, suggesting independent evolution. Altogether, our results do not show clear evidence for altitudinal adaptation in T. pityocampa, but suggest that xenobiotic exposure could exert a strong selective pressure locally. Our study highlights candidate genes and regions for further investigation of resistance evolution in an insect species in the wild.

evolutionary biology↗

A Chromosome-Level Assembly of the Pine Processionary Moth (Thaumetopoea pityocampa) genome

We present a chromosome-level genome assembly and annotation of the pine processionary moth, Thaumetopoea pityocampa (Lepidoptera: Notodontidae), a key forest pest that is a public health concern. The nuclear genome spans 615.9 Mb, scaffolded into 50 chromosome scale and 115 smaller scaffolds, with high completeness (BUSCO score: 98.9%) that provides a decisive improvement over the previous assembly (537 Mb; 68,292 contigs; BUSCO 83.6%). Coverage differences in resequenced males and females allowed identification of the Z chromosome and several W-linked contigs. As ex-pected from previous studies, we found that synteny was largely conserved with related Lepidoptera, although chromosomal fissions may explain the higher chromosome number of 49 autosomes com-pared to typical lepidopteran karyotypes. We also integrated into the assembly linkage map, allowing estimation of a genome-wide male recombination rate of 5.06 cM/Mb, varying from 11.6 cM/Mb to 1.98 cM/Mb from the smallest to the largest chromosomes. Repetitive elements represented 49.1% of this new assembly, dominated by LINEs (45.1% of classified repeats). Finally, gene prediction identified 12,898 gene models, among which 17 circadian rhythm genes were manually curated. Ex-pert annotation further allowed to identify 51 genes of the odorant receptor (OR) family as well as a total of 236 detoxification genes, including 78 CYPs, 56 CCEs, 30 GSTs, 23 UGTs and 49 ABCs. Overall, this assembly represents the first chromosome-level genome for a member of the Thaume-topoeinae subfamily, significantly expanding the currently limited set of genomic resources avail-able for Notodontidae. The fully annotated assembly is publicly accessible through the LepidoDB database (https://bipaa.genouest.org/is/lepidodb/) and will serve as a valuable resource for research on population genomics of this species.

genomics↗

Genomic incompatibilities are persistent barriers when speciation happens with gene flow in Formica ants

A current goal of speciation research is to identify the loci underlying reproductive barriers between species. Locating such barrier loci in empirical data is difficult due to the often complex demographic history of diverged taxa and the heterogeneity in evolutionary forces across the genome. Here we take advantage of a natural case of hybridization between two wood ant species (Formica aquilonia and F. polyctena) to identify regions of reduced long-term gene flow using demographically explicit scans of non-admixed genomes. In addition we identify candidate Bateson-Dobzhansky-Muller incompatibilities (BDMIs) through an imbalanced recombinant haplotype frequency analysis of natural F. aquilonia x F. polyctena hybrid genomes. Both approaches find barriers that are scattered across the genome. Furthermore, candidate BDMIs significantly overlap with the long-term barriers identified by gIMble, indicating that incompatibilities have persisted despite divergence with gene flow between the wood ant species. Intriguingly, BDMIs interact in a network and the number of pairwise interactions a BDMI has correlates with its long-term barrier strength: hub-like BDMIs with many pairwise interactions reduce gene flow more effectively. Finally in regards to function, long-term barriers identified by gIMble arise outside regions of both gene coding sequences (CDS) and transposable elements. In contrast, regions where long-term barriers and BDMIs co-locate are significantly associated with introns, implying a potential role of alternative splicing or gene regulation in incompatibilities, rather than CDS divergence. Overall, our results highlight the underappreciated impact of multilocus BDMIs and the need to consider network connectivity of BDMIs in future work. SignificanceDetecting barrier loci that reduce gene flow between closely related species is a common goal of speciation research. However, reliable detection of barrier loci is difficult due to confounding signals in genomic data. Here we take advantage of two different, recently developed approaches and find that barrier loci between wood ant species are scattered across the genome, and despite on-going gene flow, maintain two distinct species. We reveal that genomic regions that are incompatible between the two species can act as persistent barriers, despite theoretical predictions for their collapse under gene flow. Connectivity between incompatibilities also seems to play an important role in barrier persistence. These results highlight the need to consider connectivity between barrier loci in future speciation research.

evolutionary biology↗

The loss of a supergene in obligately polygynous Formica wood ant species

Some of the most striking examples of phenotypic variation within species are controlled by supergenes. However, most research on supergenes has focused on their emergence and long-term maintenance, leaving the later stages of their life cycle largely unexplored. Specifically, what happens to a derived supergene haplotype when the trait it controls reaches fixation? Here we answer this question using the ancient supergene system of Formica ants, where (monogynous) single-queen colonies carry only the ancestral haplotype M while the derived haplotype P is exclusive to (polygynous) colonies with multiple queens. Through comparative genomics of all seven European wood ant species, we found that the P haplotype was present in only one of the three obligate polygynous species (F. polyctena). In the two others (F. aquilonia and F. paralugubris) the P haplotype was completely missing except for duplicated P-specific paralogs of two genes, Zasp52 and TTLL2, with Zasp52 being directly involved in wing muscle development. We hypothesize that these genes play a direct role in polygyny and contribute to differences in body size and/or dispersal behaviour between monogynous and polygynous queens. A complete lack of P/P genotypes among the 136 workers suggest strong selection against such genotypes. While our analyses did not reveal evidence of increased mutation load on the P, it is possible that this skew in genotype distributions is driven by a few loci with strong fitness effects. We propose that selection to escape P-associated fitness costs underlies the loss of this haplotype in obligate polygynous wood ants.

genomics↗

Extensive hybridisation between multiple differently adapted species may aid persistence in a changing climate

Hybridisation and gene flow can have both deleterious and adaptive consequences for natural populations and species. To better understand the extent and consequences of hybridisation in nature, information on naturally hybridising non-model organisms is required, including characterising the structure and extent of natural hybrid zones. Here we study natural populations of five keystone mound-building wood ant (Formica rufa group) species across Finland. No genomic studies across the species group exist and the extent of hybridisation and genomic differentiation in sympatry is unknown. Combining genome-wide and morphological data, we show that Formica rufa, F. aquilonia, F. lugubris, and F. pratensis form distinct gene pools in Finland. We demonstrate more extensive hybridisation than previously thought between all five species and reveal a mosaic hybrid zone between F. aquilonia, F. rufa and F. polyctena. We show that hybrids between these climatically differently adapted species occupy warmer habitats than the cold-adapted parent F. aquilonia. This suggests hybrids occupy a different microclimatic niche compared to the locally abundant parent. We propose that wood ant hybridisation may increase with a warming climate, and warm winters, in particular, may provide a competitive advantage for the hybrids over F. aquilonia in the future. In summary, our results demonstrate how extensive hybridisation may help persistence in a changing climate. Additionally, they provide an example on how mosaic hybrid zones can have significant ecological and evolutionary consequences because of their large extent and independent hybrid populations that face both ecological and intrinsic selection pressures.

evolutionary biology↗

A quarter-million-year-old polymorphism drives reproductive mode variation in the pea aphid

Although asexual linages evolved from sexual lineages in many different taxa, the genetics of sex loss remains poorly understood. We addressed this issue in the pea aphid Acyrthosiphon pisum, whose natural populations encompass lineages performing cyclical parthenogenesis (CP) and producing one sexual generation per year, as well as obligate parthenogenetic (OP) lineages that can no longer produce sexual females but can still produce males. A SNP-based, whole-genome scan of CP and OP populations sequenced in pools (103 individuals from six populations) showed that a single X-linked region controls the variation in reproductive mode. This 840-kb region is highly divergent between CP and OP populations (FST = 34.9%), with >2000 SNPs or short Indels showing a high degree of association with the phenotypic trait. Comparison of de novo genome assemblies built from long reads did not reveal large structural rearrangements between CP and OP lineages within the candidate region. This reproductive polymorphism still appears relatively ancient, as we estimated its age at ~0.25 million years from the divergence between cp and op alleles. The low genetic differentiation between CP and OP populations at the rest of the genome (FST = 2.4%) suggests gene flow between them. Males from OP lineages thus likely transmit their op allele to new genomic backgrounds. This "contagious asexuality", combined with environment-induced selection (each reproductive mode being favored under different climates) probably contributes to the long-term persistence of the cp and op alleles. SignificanceAsexual taxa occur in all major clades of Eukaryotes and derive from related sexual species. Yet, the genetic basis for these transitions is poorly known because crosses cannot generally be performed to genetically map the ability to propagate asexually. As a result, only one gene responsible for sex loss has been identified in one animal species. Here, using pooled genome sequencing, we identified an 840kb region (carrying 32 genes) that controls the transition to permanent asexuality in the pea aphid. We also revealed that sexual and asexual alleles diverged 0.25 million years ago and that asexual lineages likely persist through contagious asexuality, providing new insights into the mechanisms of coexistence of sexual and asexual lineages.

evolutionary biology↗

Rapid and repeatable genome evolution across three hybrid ant populations

Hybridization is frequent in the wild but it is unclear whether admixture events lead to predictable outcomes and if so, at what timescale. We show that selection led to correlated sorting of genetic variation in less than 50 generations in three hybrid Formica aquilonia x F. polyctena ant populations. Removal of ancestry from the species with the lowest effective population size happened repeatedly in all populations, consistent with purging of deleterious load. This process was modulated by recombination rate variation and the density of functional sites. Moreover, haplotypes with signatures of positive selection in either species were more likely to fix in hybrids. These mechanisms led to mosaic genomes with comparable ancestry proportions. Our work demonstrates predictable evolution over short timescales after admixture in nature.

evolutionary biology↗

Whole-genome analysis of multiple wood ant population pairs supports similar speciation histories, but different degrees of gene flow, across their European range

The application of demographic history modeling and inference to the study of divergence between species is becoming a cornerstone of speciation genomics. The demographic history is usually reconstructed by analysing a single population from each species, assuming that the divergence history inferred between these populations represents the actual speciation history. However, this assumption is rarely explicitly tested, and it may not be met when species diverge with gene flow. For instance, secondary contact between two species after a range expansion may be confined into a specific geographic region. In this study, we tested to what extent the divergence history inferred from two heterospecific populations would vary depending on their geographic locations, using mound-building red wood ants. The wood ant species Formica polyctena and F. aquilonia have contrasting distributions in Europe and naturally hybridize in Finland. We first performed whole-genome resequencing of 20 individuals sampled in multiple populations across both species ranges. We then reconstructed the divergence histories of distinct heterospecific population pairs using a coalescent-based approach. We found that the analysis of these different population pairs always supported a scenario of divergence with gene flow, suggesting that species divergence started in the Pleistocene (ca. 500 kya) and occurred with continuous asymmetrical gene flow from F. aquilonia to F. polyctena until a recent time, when migration stopped (2-19 kya, depending on the population pair considered). However, we found support for contemporary gene flow in the sympatric population pair from Finland, where hybrids have been described. Overall, our results suggest that divergence histories reconstructed from a few individuals may be reliable and applicable at the species level. Nonetheless, the geographical context of populations chosen to represent their species should be taken into account, as it may affect estimates of migration rates between species when gene flow is heterogeneous across their geographical ranges.

evolutionary biology↗

Cost-effective long-read assembly of a hybrid Formica aquilonia x Formica polyctena wood ant genome from a single haploid individual

Formica red wood ants are a keystone species of boreal forest ecosystems and an emerging model system in the study of speciation and hybridization. Here we performed a standard DNA extraction from a single, field-collected Formica aquilonia x Formica polyctena haploid male and assembled its genome using [~]60x of PacBio long reads. After polishing and contaminant removal, the final assembly was 272 Mb (4,687 contigs, N50 = 1.16 Mb). Our reference genome contains 98.5% of the core Hymenoptera BUSCOs and was scaffolded using the pseudo-chromosomal assembly of a related species, F. selysi (28 scaffolds, N50 = 8.49 Mb). Around one third of the genome consists of repeats, and 17,426 gene models were annotated using both protein and RNAseq data (97.4% BUSCO completeness). This resource is of comparable quality to the few other single individual insect genomes assembled to date and paves the way to genomic studies of admixture in natural populations and comparative genomic approaches in Formica wood ants.

genomics↗

Secondary evolve and re-sequencing: an experimental confirmation of putative selection targets without phenotyping

Evolve and re-sequencing (E&R) studies investigate the genomic responses of adaptation during experimental evolution. Because replicate populations evolve in the same controlled environment, consistent responses to selection across replicates are frequently used to identify reliable candidate regions that underlie adaptation to a new environment. However, recent work demonstrated that selection signatures can be restricted to one or a few replicate(s) only. These selection signatures frequently have a weak statistical support, and given the difficulties of functional validation, additional evidence is needed before considering them as candidates for functional analysis. Here, we introduce an experimental procedure to validate candidate loci with weak or replicate-specific selection signature(s). Crossing an evolved population from a primary E&R experiment to the ancestral founder population reduces the frequency of candidate alleles that have reached a high frequency. We hypothesize that genuine selection targets will experience a repeatable frequency increase after the mixing with the ancestral founders if they are exposed to the same environment (secondary E&R experiment). Using this approach, we successfully validate two overlapping selection targets, which showed a mutually exclusive selection signature in a primary E&R experiment of Drosophila simulans adapting to a novel temperature regime. We conclude that secondary E&R experiments provide a reliable confirmation of selection signatures that are either not replicated or show only a low statistical significance in a primary E&R experiment. Such experiments are particularly helpful to prioritize candidate loci for time-consuming functional follow-up investigations.

molecular biology↗

Hybridizing wood ants allow testing for natural selection at candidate barrier loci underlying speciation

While speciation underlies novel biodiversity, it is poorly understood how natural selection shapes genomes during speciation. Selection is assumed to act against gene flow at barrier loci, promoting reproductive isolation and speciation. However, evidence for gene flow and selection is often indirect. Here we utilize haplodiploidy to identify candidate barrier loci in hybrids between two wood ant species and integrate survival analysis to directly measure if natural selection is acting at candidate barrier loci. We find multiple candidate barrier loci but surprisingly, proportion of them show leakage between samples collected ten years apart, natural selection favoring leakage in the latest sample. Barrier leakage and natural selection for introgressed alleles could be due to environment-dependent selection, emphasizing the need to consider temporal variation in natural selection in future speciation work. Integrating data on survival allows us to move beyond genome scans, demonstrating natural selection acting on hybrid genomes in real-time.

evolutionary biology↗

Long-read based assembly and annotation of a Drosophila simulans genome

Long-read sequencing technologies enable high-quality, contiguous genome assemblies. Here we used SMRT sequencing to assemble the genome of a Drosophila simulans strain originating from Madagascar, the ancestral range of the species. We generated 8 Gb of raw data (~50x coverage) with a mean read length of 6,410 bp, a NR50 of 9,125 bp and the longest subread at 49 kb. We benchmarked six different assemblers and merged the best two assemblies from Canu and Falcon. Our final assembly was 127.41 Mb with a N50 of 5.38 Mb and 305 contigs. We anchored more than 4 Mb of novel sequence to the major chromosome arms, and significantly improved the assembly of peri-centromeric and telomeric regions. Finally, we performed full-length transcript sequencing and used this data in conjunction with short-read RNAseq data to annotate 13,422 genes in the genome, improving the annotation in regions with complex, nested gene structures.

genomics↗

Disentangling The Causes For Faster-X Evolution In Aphids

Faster evolution of X chromosomes has been documented in several species and results from the increased efficiency of selection on recessive alleles in hemizygous males and/or from increased drift due to the smaller effective population size of X chromosomes. Aphids are excellent models for evaluating the importance of selection in faster-X evolution, because their peculiar life-cycle and unusual inheritance of sex-chromosomes lead to equal effective population sizes for X and autosomes. Because we lack a high-density genetic map for the pea aphid whose complete genome has been sequenced, we assigned its entire genome to the X and autosomes based on ratios of sequencing depth in males and females. Unexpectedly, we found frequent scaffold misassembly, but we could unambiguously locate 13,726 genes on the X and 19,263 on autosomes. We found higher non-synonymous to synonymous substitutions ratios (dN/dS) for X-linked than for autosomal genes. Our analyses of substitution rates together with polymorphism and expression data showed that relaxed selection is likely to contribute predominantly to faster-X as a large fraction of X-linked genes are expressed at low rates and thus escape selection. Yet, a minor role for positive selection is also suggested by the difference between substitution rates for X and autosomes for male-biased genes (but not for asexual female-biased genes) and by lower Tajimas D for X-linked than for autosomal genes with highly male-biased expression patterns. This study highlights the relevance of organisms displaying alternative inheritance of chromosomes to the understanding of forces shaping genome evolution.

evolutionary biology↗