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

Kulmuni, Jonna; Nouhaud, Pierre; Pluckrose, Lucy; Satokangas, Ina; Dhaygude, Kishor; Butlin, Roger K.

doi:10.1111/mec.15606

Cited by 15 publications

(24 citation statements)

References 30 publications

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“…They proposed that recessive incompatibilities between the genomes of the two species are exposed to selection in haploid males. Subsequent research on this system has revealed instability in the direction of selection on introgressed alleles in males across a ten-year time interval, with introgression recently favored on average in loci where introgression was previously selected against (61). In the tawny crazy ant Nylanderia fulva, males invariably carry the same allele at two out of 12 microsatellite loci, while females are almost always heterozygous at these loci (20).…”

Section: Discussionmentioning

confidence: 99%

Linked supergenes underlie split sex ratio and social organization in an ant

Lagunas-Robles

Purcell

Brelsford

2021

Preprint

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Sexually reproducing organisms usually invest equally in male and female offspring. Deviations from this pattern have led researchers to new discoveries in the study of parent-offspring conflict, genomic conflict, and cooperation. Some social insect species exhibit the unusual population-level pattern of split sex ratio, wherein some colonies specialize in the production of future queens and others specialize in the production of males. Theoretical work focused on the relatedness asymmetries emerging from haplodiploid inheritance, whereby queens are equally related to daughters and sons, but their daughter workers are more closely related to sisters than to brothers, led to a series of testable predictions and spawned many empirical studies of this phenomenon. However, not all empirical systems follow predicted patterns, so questions remain about how split sex ratio emerges. Here, we sequence the genomes of 138 Formica glacialis workers from 34 male-producing and 34 gyne-producing colonies to determine whether split sex ratio is under genetic control. We identify a supergene spanning 5.5 Mbp that is closely associated with sex allocation in this system. Strikingly, this supergene is adjacent to another supergene spanning 5 Mbp that is associated with variation in colony queen number. We identify a similar pattern in a second related species, Formica podzolica. The discovery that split sex ratio is determined, at least in part, by a supergene in two species opens a new line of research on the evolutionary drivers of split sex ratio.Significance StatementSome social insects exhibit split sex ratio, wherein some colonies produce future queens and others produce males. This phenomenon spawned many influential theoretical studies and empirical tests, both of which have advanced our understanding of parent-offspring conflicts and cooperation. However, some empirical systems did not follow theoretical predictions, indicating that researchers lack a comprehensive understanding of the drivers of split sex ratio. Here, we show that split sex ratio is associated with a large genomic region in two ant species. The discovery of a genetic basis for sex allocation in ants provides a novel explanation for this phenomenon, particularly in systems where empirical observations deviate from theoretical predictions.

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Section: Discussionmentioning

confidence: 99%

Linked supergenes underlie split sex ratio and social organization in an ant

Lagunas-Robles

Purcell

Brelsford

2021

Preprint

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“…This population has been characterized as a hybrid between F. aquilonia and F. polyctena using both genetic markers and morphological data (Kulmuni et al, 2010; Seifert, Kulmuni, & Pamilo, 2010). The Långholmen population is a supercolony consisting of two genetic lineages of hybrid origin (R and W; (Kulmuni & Pamilo, 2014; Kulmuni et al, 2010), which show moderate genetic differentiation ( F ST ≈ 0.105, Kulmuni et al, 2020).…”

Section: Methodsmentioning

confidence: 99%

“…subgenus. Kulmuni et al (2020) assembled a draft genome using poolseq data from a hybrid F. aquilonia × F. polyctena population, but the assembly is highly fragmented (> 300k contigs, N50 < 2 kbp). At a broader phylogenetic scale, among palaearctic Formica species, two genomes are available for the Coptoformica and Serviformica subgenera, respectively F. exsecta (Dhaygude, Nair, Johansson, Wurm, & Sundström, 2019) and F. selysi (Brelsford et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

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

Nouhaud

Kulmuni

2021

Preprint

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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 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.

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“…However, intrinsic barriers, such as chromosomal rearrangements and genetic incompatibilities can also lead to heterogeneous genomic differentiation (Faria & Navarro, 2010;Navarro, Betran, Barbadilla, & Ruiz, 1997;Kulmuni et al, 2020;Rieseberg, 2001). Intrinsic barriers inhibits allele exchange in such regions and in linked surrounding regions eventually leads to elevated genetic differentiation.…”

Section: Heterogeneous Differentiation Across the Genomementioning

confidence: 99%

Natural selection and intrinsic barriers play important roles in speciation of two closely related Populus (Salicaceae) species

Tian

Ingvarsson

Zhao

et al. 2021

Preprint

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Despite the growing number of recent studies on genome-wide divergence during speciation, the genetic basis and mechanisms of genomic divergence are still incompletely understood. In most species, natural selection plays a key role in heterogeneous genomic divergence. Additionally, intrinsic barriers, such as chromosomal rearrangements or gene incompatibilities, can also cause genomic heterogeneity. Based on whole genome re-sequencing data from 27 Populus alba and 28 P. adenopoda individuals, we explored the reasons for heterogeneous genomic divergence of these two closely related species. The results showed that the two species diverged ~5-10 million years ago (Mya), when the Qinghai-Tibet Plateau reached a certain height and the inland climate of the Asian continent became arid, which is associated with the fact that the two species begin to diverge and eventually led to speciation. In highly differentiated regions, the absolute divergence (dxy) was significantly higher than genomic background, and relative and absolute divergence were highly correlated, which indicates that intrinsic barriers played an important role in maintaining genomic heterogeneous divergence. Additionally, θπ and shared polymorphisms decreased while fixed differences increased in highly differentiated regions, which are characteristics of natural selection. The above description indicates that the combination of intrinsic barriers and natural selection result in heterogeneous genomic divergence and reproductive isolation. We further found some genes that are related to reproduction may be involved in explaining the reproductive isolation of the two species.

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

Cited by 15 publications

References 30 publications

Linked supergenes underlie split sex ratio and social organization in an ant

Linked supergenes underlie split sex ratio and social organization in an ant

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

Natural selection and intrinsic barriers play important roles in speciation of two closely related Populus (Salicaceae) species

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