Assembly of a Hybrid Formica aquilonia × F. polyctena Ant Genome From a Haploid Male

Publisher Copyright: © 2022 The American Genetic Association..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 × Formica polyctena haploid male and assembled its genome using ~60× of PacBio long reads. After polishing and contaminant removal, the final assembly was 272 Mb (4687 contigs, N50 = 1.16 Mb). Our reference genome contains 98.5% of the core Hymenopteran BUSCOs and was pseudo-scaffolded using the 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.Peer reviewe

Differences in Thermal Tolerance between Parental Species Could Fuel Thermal Adaptation in Hybrid Wood Ants

Genetic variability is essential for adaptation and could be acquired via hybridization with a closely related lineage. We use ants to investigate thermal adaptation and the link between temperature and genetic variation arising from hybridization. We test for differences in cold and heat tolerance between Finnish Formica polyctena and Formica aquilonia wood ants and their naturally occurring hybrids. Using workers, we find that the parental individuals differ in both cold and heat tolerances and express thermal limits that reflect their global distributions. Hybrids, however, cannot combine thermal tolerance of parental species as they have the same heat tolerance as F. polyctena but not the same cold tolerance as F. aquilonia. We then focus on a single hybrid population to investigate the relationship between temperature variation and genetic variation across 16 years using reproductive individuals. On the basis of the thermal tolerance results, we expected the frequency of putative F. polyctena alleles to increase in warm years and F. aquilonia alleles to increase in cold years. We find support for this in hybrid males but not in hybrid females. These results contribute to understanding the outcomes of hybridization, which may be sex specific or depend on the environment. Furthermore, genetic variability resulting from hybridization could help hybrid wood ants cope with changing thermal conditions.Peer reviewe

Secondary Evolve and Resequencing : An Experimental Confirmation of Putative Selection Targets without Phenotyping

Evolve and resequencing (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 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 either are not replicated or show only a low statistical significance in a primary E&R experiment unless epistatic interactions predominate. Such experiments are particularly helpful to prioritize candidate loci for time-consuming functional follow-up investigations.Peer reviewe

Rapid and predictable genome evolution across three hybrid ant populations

Funding Information: This work was supported by Academy of Finland (www.aka.fi) no. 328961 and HiLIFE (www2.helsinki.fi/en/helsinki-institute-of-lifescience) grants to JK. SHM was supported by a Royal Society University Research Fellowship URF \R1\180682 (www.royalsociety.org). VCS was supported by Fundação Ciência e Tecnologia CEECINST/00032/2018/CP1523/CT0008 and UIDB/00329/2020 grants (www.fct.pt). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank G. Barroso for assistance with iSMC, the SpecIAnt group for feedback, and CSC–IT Center for Science, Finland, for computational resources. This work was performed under the Global Ant Genomics Alliance. Publisher Copyright: Copyright: © 2022 Nouhaud et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.Hybridization is frequent in the wild but it is unclear when admixture events lead to predictable outcomes and if so, at what timescale. We show that selection led to correlated sorting of genetic variation rapidly after admixture in 3 hybrid Formica aquilonia × F. polyctena ant populations. Removal of ancestry from the species with the lowest effective population size happened 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.Peer reviewe

Rapid and predictable genome evolution across three hybrid ant populations

Hybridization is frequent in the wild but it is unclear when admixture events lead to predictable outcomes and if so, at what timescale. We show that selection led to correlated sorting of genetic variation rapidly after admixture in 3 hybrid Formica aquilonia × F. polyctena ant populations. Removal of ancestry from the species with the lowest effective population size happened 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.info:eu-repo/semantics/publishedVersio

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

The application of demographic history modelling and inference to the study of divergence between species has become a cornerstone of speciation genomics. Speciation histories are usually reconstructed by analysing single populations from each species, assuming that the inferred population history represents the actual speciation history. However, this assumption may not be met when species diverge with gene flow, for example, when secondary contact may be confined to specific geographic regions. Here, we tested whether divergence histories inferred from heterospecific populations may vary depending on their geographic locations, using the two wood ant species Formica polyctena and F. aquilonia. We performed whole-genome resequencing of 20 individuals sampled in multiple locations across the European ranges of both species. Then, we reconstructed the histories of distinct heterospecific population pairs using a coalescent-based approach. Our analyses always supported a scenario of divergence with gene flow, suggesting that divergence started in the Pleistocene (c. 500 kya) and occurred with continuous asymmetrical gene flow from F. aquilonia to F. polyctena until a recent time, when migration became negligible (2–19 kya). However, we found support for contemporary gene flow in a sympatric pair from Finland, where the species hybridise, but no signature of recent bidirectional gene flow elsewhere. Overall, our results suggest that divergence histories reconstructed from a few individuals may be 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 spatially heterogeneous.info:eu-repo/semantics/publishedVersio

Instability of natural selection at candidate barrier loci underlying speciation in wood ants

doi: 10.1111/mec.15606Speciation underlies the generation of novel biodiversity. Yet, there is much to learn about how natural selection shapes genomes during speciation. Selection is assumed to act against gene flow at barrier loci, promoting reproductive isolation. However, evidence for gene flow and selection is often indirect and we know very little about the temporal stability of barrier loci. Here we utilize haplodiploidy to identify candidate male barrier loci in hybrids between two wood ant species. As ant males are haploid, they are expected to reveal recessive barrier loci, which can be masked in diploid females if heterozygous. We then test for barrier stability in a sample collected 10 years later and use survival analysis to provide a direct measure of natural selection acting on candidate male barrier loci. We find multiple candidate male barrier loci scattered throughout the genome. Surprisingly, a proportion of them are not stable after 10 years, natural selection apparently switching from acting against to favouring introgression in the later sample. Instability of the barrier effect and natural selection for introgressed alleles could be due to environment-dependent selection, emphasizing the need to consider temporal variation in the strength of natural selection and the stability of the barrier effect at putative barrier loci in future speciation work.Peer reviewe

Utilisation des polymorphismes : QTL, GWAS et scans génomiques

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Understanding Admixture : Haplodiploidy to the Rescue

Hybridization has broad evolutionary consequences, from fueling or counteracting speciation to facilitating adaptation to novel environments. Hybridization and subsequent introgression appear widespread along the tree of life. However, our understanding of how distinct evolutionary forces shape admixed genomes and the fate of introgressed genetic variants remains scarce. Most admixture research in animals has focused on diploid organisms. Wepropose that haplodiploid organisms can help resolve open questions about the genomic consequences of hybridization in natural populations. The ploidy difference between haploid males and diploid females, the availability of genome-wide male haplotypes, and ongoing cases of admixture make haplodiploid organisms promising models to improve our knowledge with regards to the evolution of hybrid genomes.Peer reviewe