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

Portinha, Beatriz; Avril, Amaury; Bernasconi, Christian; Helanterä, Heikki; Monaghan, Josie; Seifert, Bernhard; Sousa, Vitor C.; Kulmuni, Jonna; Nouhaud, Pierre

doi:10.1111/mec.16481

Cited by 9 publications

(26 citation statements)

References 83 publications

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“…The recent sequencing of the first RWA genome by Nouhaud et al [ 50 ] opened up the prospect of using multiple next generation sequencing (NGS) approaches based on SNPs detection for population and phylogenetic studies of this ant group. For example, Portinha et al [ 51 ] performed whole-genome resequencing of several workers to infer divergence histories among heterospecific populations of F. polyctena and F. aquilonia . As far as our populations are concerned, a double-digest restriction-site-associated DNA sequencing (ddRADseq) approach could be a powerful tool to compare the genetic variation, structure and mating system across populations [ 52 , 53 ] along with genome-wide association studies (GWAS) focused on the identification of the genes that are actively selected by the environmental factors and integrating phenotypic information [ 54 ].…”

Section: Discussionmentioning

confidence: 99%

Assessing Molecular Diversity in Native and Introduced Populations of Red Wood Ant Formica paralugubris

Masoni

Coppi

Balzani

et al. 2022

Animals

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The Formica rufa group comprises several ant species which are collectively referred to as “red wood ants” and play key roles in boreal forest ecosystems, where they are ecologically dominant and greatly influence habitat dynamics. Owing to their intense predatory activity, some of these species are used as biocontrol agents against several forest insect pests and for this aim in Italy, nearly 6000 ant nests were introduced from their native areas in the Alps to several Appeninic sites during the last century. In this work, we assessed and compared the genetic variability and structure of native and introduced populations of F. paralugubris, thus evaluating the extent of genetic drift that may have occurred since the time of introduction, using amplified fragment length polymorphism (AFLP) markers. PCR amplification with a fam_EcoRI-TAC/MseI-ATG primers combination produced a total of 147 scorable bands, with 17 identified as outlier loci. The genetic variation was higher in the introduced population compared to the native ones that, on the other hand, showed a higher diversity between nests. AMOVA results clearly pointed out that the overall genetic structure was dominated by among-worker variation, considering all populations, the Alpine vs. Apennine groups and the comparison among native and related introduced populations (all ranging between 77.84% and 79.84%). Genetic analyses unveiled the existence of six main different groups that do not entirely mirror their geographic subdivision, pointing towards a wide admixture between populations, but, at the same time, rapid diversification of some Apennine populations. Future studies based on high-throughput genomic methods are needed to obtain a thorough understanding of the effects of environmental pressure on the genetic structure and mating system of these populations.

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Section: Discussionmentioning

confidence: 99%

Assessing Molecular Diversity in Native and Introduced Populations of Red Wood Ant Formica paralugubris

Masoni

Coppi

Balzani

et al. 2022

Animals

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“…We collected unmated queens from Bunkkeri ( n = 10) and Långholmen ( n W = 10, n R = 9) in Spring 2018 and workers from Pikkala ( n = 10) in Spring 2015 ( S1 Table ). Data generated by Portinha and colleagues [ 40 ] were used as F . aquilonia and F .…”

Section: Methodsmentioning

confidence: 99%

Rapid and predictable genome evolution across three hybrid ant populations

et al. 2022

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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.

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“…This is expected since F. selysi diverged 5 Mya from the F. rufa species group, whereas species from the F. rufa species group (from which F. aquilonia and F. polyctena belong to) all diverged within the last 500 kya ( Goropashnaya et al 2012 ). This makes our assembly suitable for resequencing-based studies conducted on any of the 13 species of the F. rufa species group (e.g., Portinha et al 2022 ).…”

Section: Resultsmentioning

confidence: 99%

“…This work provides a crucial resource to study speciation and contemporary hybridization, as well as the evolution of extreme sociality in the F. rufa species group, that contains 13 keystone species of forest ecosystems ( Seifert 2021 ). The genome and its annotation are both of sufficient quality for studies aiming to reconstruct speciation histories (e.g., Portinha et al 2022 ) and identify barrier loci or regions of adaptive introgression (e.g., Heliconius Genome Consortium 2012 ). It will also enable new approaches on the genomics of hybridization in this fascinating system ( Nouhaud et al 2020 , 2022 ).…”

Section: Discussionmentioning

confidence: 99%

“…We compared our assembly and the F. selysi assembly ( Brelsford et al 2020 , only chromosome-level assembly available for the Formica genus) by aligning short-read data from F. aquilonia and F. polyctena individuals sampled across Europe ( n = 10 per species). These data were generated by Portinha et al (2022) and we followed their trimming and mapping pipeline to align reads against the F. selysi assembly. Mapping statistics were then collected from BAM files using SAMtools.…”

Section: Methodsmentioning

confidence: 99%

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

Nouhaud

Kulmuni

2022

Journal of Heredity

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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 (4,687 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.

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

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 9 publications

References 83 publications

Assessing Molecular Diversity in Native and Introduced Populations of Red Wood Ant Formica paralugubris

Assessing Molecular Diversity in Native and Introduced Populations of Red Wood Ant Formica paralugubris

Rapid and predictable genome evolution across three hybrid ant populations

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

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