Rapid and predictable genome evolution across three hybrid ant populations

Nouhaud, Pierre; Martin, Simon H.; Portinha, Beatriz; Sousa, Vitor C.; Kulmuni, Jonna

doi:10.1371/journal.pbio.3001914

Cited by 8 publications

(13 citation statements)

References 65 publications

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“…Third, variation in F. aquilonia ancestry and ancestry heterozygosity, combined with the limited dispersal capabilities of supercolonial wood ants, suggest that hybrid populations may have emerged from independent admixture events. This finding is consistent with previous research on three closely located populations (Nouhaud, Martin, et al, 2022). The mosaic of ancestry proportions across the hybrid zone contrasts with the spatial gradients typical of clinal hybrid zones (Barton & Hewitt, 1985).…”

Section: Discussionsupporting

confidence: 94%

“…We carried out state‐of‐the‐art morphological species identification with NUMOBAT (Seifert, 2021) using three to six individuals from each nest sampled for genomic data. Since both the genomic analysis and morphological identification required the use of whole individuals, we used different individuals from each nest for these separate purposes, which is justified by the fact that wood ant nests are genetically homogeneous (Kulmuni et al, 2020; Nouhaud, Martin, et al, 2022; Pamilo, 1982). We measured altogether 17 morphological characteristics (See Table S2 for a description of the characteristics, and Table S3 for primary morphological data), producing species assignment probabilities at the nest level.…”

Section: Methodsmentioning

confidence: 99%

“…Since many species pairs within the group hybridise, this raises the possibility of previously undetected multispecies hybridisation. However, outside F. aquilonia and F. polyctena (Nouhaud, Martin, et al, 2022; Portinha et al, 2022), no genomic studies on the F. rufa group exist, and consequently also no information on the congruence between morphological and genomic data is available.…”

Section: Introductionmentioning

confidence: 99%

“…Since mosaic zones can be large, and selection can act independently in different hybrid populations, they may result in more heterogeneous patterns and geographically widespread effects than those in clinal hybrid zones. Furthermore, independently evolving hybrid populations allow predictability in the outcomes of hybridisation to be studied (Nouhaud, Martin, et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

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Semipermeable species boundaries create opportunities for gene flow and adaptive potential

et al. 2023

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Hybridisation and gene flow can have both deleterious and adaptive consequences for natural populations and species. To better understand the extent of hybridisation in nature and the balance between its beneficial and deleterious outcomes in a changing environment, information on naturally hybridising nonmodel organisms is needed. This requires the characterisation of the structure and extent of natural hybrid zones. Here, we study natural populations of five keystone mound‐building wood ant species in the Formica rufa group 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 demonstrate more extensive hybridisation than was previously detected between all five species in Finland. Specifically, we reveal a mosaic hybrid zone between Formica aquilonia, F. rufa and F. polyctena, comprising further generation hybrid populations. Despite this, we find that F. rufa, F. aquilonia, F. lugubris and F. pratensis form distinct gene pools in Finland. We also find that hybrids occupy warmer microhabitats than the nonadmixed populations of cold‐adapted F. aquilonia, and suggest that warm winters and springs, in particular, may benefit hybrids over F. aquilonia, the most abundant F. rufa group species in Finland. In summary, our results indicate that extensive hybridisation may create adaptive potential that could promote wood ant persistence in a changing climate. Additionally, they highlight the potentially significant ecological and evolutionary consequences of extensive mosaic hybrid zones, within which independent hybrid populations face an array of ecological and intrinsic selection pressures.

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Section: Discussionsupporting

confidence: 94%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Semipermeable species boundaries create opportunities for gene flow and adaptive potential

et al. 2023

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“…2019, Calfee et al . 2020), but few have explicitly ruled out genetic drift as a mechanism, and selection is regularly implicated even when hybrid zones do not show concordant patterns (but see Nouhaud et al . 2022).…”

Section: Discussionmentioning

confidence: 99%

Selection leads to remarkable variability in the outcomes of hybridization across replicate hybrid zones

McFarlane

Jahner

Lindtke

et al. 2022

Preprint

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Hybrid zones have been held up as an opportunity to see speciation in action, as windows into the evolutionary process. Cases of repeated hybridization provide opportunities for comparative analysis. Within this context, there is an assumption that if the same genetic incompatibilities are maintaining reproductive isolation across all instances of secondary contact, those incompatibilities should be identifiable by consistent patterns across hybrid zones. This is in contrast with changes in allele frequencies due to genetic drift, which will be idiosyncratic for each hybrid zone. To test this assumption, we simulated 20 replicates of each of 24 hybrid zone scenarios with varied genetic incompatibilities, rates of migration, and selection. We found remarkable variability in the outcomes of hybridization in replicate hybrid zones, particularly with Dobzhansky-Muller incompatibilities and strong selection. Specifically, we found substantial differences among replicates in the overall genomic composition of individuals, including admixture proportions, inter-specific ancestry complement in the diploid genome, and number of ancestry junctions. Additionally, we found substantial variation among replicates at focal loci, including a locus that contributed to incompatibility, a locus linked to a locus under selection, and a locus not under selection. From this, we conclude that processes other than selection are responsible for some consistent outcomes of hybridization, whereas selection on incompatibilities can lead to genomically widespread and highly variable outcomes among replicates. We use these results to highlight the challenge of mapping between pattern and process in hybrid zones and call attention to how selection against incompatibilities will commonly lead to unpredictable, variable outcomes. Our hope is that this study informs future research on replicate hybrid zones and encourages further development of statistical techniques, theoretical models, and exploration of additional axes of variation to understand the maintenance of reproductive isolation, while recognizing the difficulties of confidently mapping process to pattern.

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Complex Evolutionary History With Extensive Ancestral Gene Flow in an African Primate Radiation

Jensen,

Swift,

de Vries

et al. 2023

Molecular Biology and Evolution

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Understanding the drivers of speciation is fundamental in evolutionary biology, and recent studies highlight hybridization as an important evolutionary force. Using whole-genome sequencing data from 22 species of guenons (tribe Cercopithecini), one of the world's largest primate radiations, we show that rampant gene flow characterizes their evolutionary history and identify ancient hybridization across deeply divergent lineages that differ in ecology, morphology, and karyotypes. Some hybridization events resulted in mitochondrial introgression between distant lineages, likely facilitated by cointrogression of coadapted nuclear variants. Although the genomic landscapes of introgression were largely lineage specific, we found that genes with immune functions were overrepresented in introgressing regions, in line with adaptive introgression, whereas genes involved in pigmentation and morphology may contribute to reproductive isolation. In line with reports from other systems that hybridization might facilitate diversification, we find that some of the most species-rich guenon clades are of admixed origin. This study provides important insights into the prevalence, role, and outcomes of ancestral hybridization in a large mammalian radiation.

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Rapid and predictable genome evolution across three hybrid ant populations

Cited by 8 publications

References 65 publications

Semipermeable species boundaries create opportunities for gene flow and adaptive potential

Semipermeable species boundaries create opportunities for gene flow and adaptive potential

Selection leads to remarkable variability in the outcomes of hybridization across replicate hybrid zones

Complex Evolutionary History With Extensive Ancestral Gene Flow in an African Primate Radiation

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