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Rapid and predictable genome evolution across three hybrid ant populations [1]

['Pierre Nouhaud', 'Organismal', 'Evolutionary Biology Research Programme', 'University Of Helsinki', 'Helsinki', 'Simon H. Martin', 'Institute Of Evolutionary Biology', 'University Of Edinburgh', 'Edinburgh', 'United Kingdom']

Date: 2023-01

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.

Funding: This work was supported by Academy of Finland ( www.aka.fi ) no. 328961 and HiLIFE ( www2.helsinki.fi/en/helsinki-institute-of-life-science ) 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.

Data Availability: All FASTQ files are available on ENA under project PRJEB55288 (hybrid samples) and PRJEB51899 (F. aquilonia & F. polyctena samples). VCF files, FASTSIMCOAL2 files and scripts, and statistics computed over genomic windows are available from figshare: https://doi.org/10.6084/m9.figshare.c.6140793.v3 . Bioinformatic and MSPRIME scripts are available from https://github.com/pi3rrr3/antmixture .

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.

Here, we took advantage of multiple hybrid populations between the 2 wood ant species Formica aquilonia and F. polyctena to measure how rapid and predictable the evolution of admixed genomes is in the wild and identify the key factors that determine this predictability. These 2 species are polygynous, with up to several hundreds of queens per nest. A population is a supercolony, with dozens of interconnected nests and low relatedness between individuals [ 20 ]. Although differentiation between nests within a population is low in polygynous and supercolonial species, differentiation between populations is high, likely reflecting budding as the main dispersal mode (i.e., dispersing by foot and building a new nest in the vicinity of an already established nest, reviewed in [ 21 ]). Long-distance dispersal happens via temporary social parasitism, where a single mated queen (or possibly few) enters the nest of an unrelated species, executes the local queen, and uses the local workforce to raise her first brood [ 21 ]. Several hybrid F. aquilonia × polyctena populations with distinct mitochondrial sequences have been previously characterized in Southern Finland [ 22 ], providing a test case for the outcomes of admixture in nature.

Hybridization is widespread and has shaped the genomes of many extant species, representing a major source of evolutionary novelties [ 1 – 3 ]. Understanding the evolution of hybrid genomes is important because it can shed light on how species barriers become established, on the fitness costs (e.g., incompatibilities) and benefits (e.g., heterosis) of hybridization, and help us better understand the function of genes and their interactions [ 4 ]. Variation in local ancestry patterns along hybrid genomes has been found across many taxa, including sunflowers [ 5 ], monkeyflowers [ 6 ], humans [ 7 ], swordtail fish [ 8 , 9 ], sparrows [ 10 ], butterflies [ 11 , 12 ], and maize [ 13 ]. Such variation in local ancestry reflects the interaction of recombination with neutral (e.g., drift, migration) and selective processes. Selection may lead to the fixation (adaptive introgression [ 1 ]) or purging of one ancestry component (incompatibilities; genetic load in one hybridizing species [ 14 , 15 ]). Recombination rate variation can modulate the effects of selection, for example, by enabling faster purging of deleterious alleles in low-recombining regions [ 14 ]. Admixture landscapes are also impacted by past demography and stochastic events, such as bottlenecks or initial admixture proportions [ 16 ]. These mechanisms can lead to the fixation or near-fixation of one ancestry component at a given locus within a hybrid population, a process we refer to as sorting of genetic variation (genome stabilization [ 5 , 12 , 17 ]). A few previous studies have investigated the interplay of different neutral and selective factors across multiple admixture events, revealing predictable sorting of ancestral variation in replicated hybrid populations [ 9 , 10 , 12 ]. However, while theory predicts that the efficiency of selection on introgressed variation will quickly decrease [ 7 , 15 , 18 ], the timescale of sorting after admixture in the wild is still unclear (but see [ 19 ]).

Results and discussion

We generated whole-genome sequence data from 3 hybrid populations (Fig 1A, n = 39) and used genomes from both species collected within and outside their overlapping range (n = 10 per species [23]; mean coverage: 20.6×, S1 Table). Analyzing ca. 1.6 million single-nucleotide polymorphisms (SNPs) genome-wide, we confirmed that the hybrid populations were genetically intermediate between F. aquilonia and F. polyctena (Figs 1B and 1C and S1 and S1 Table). Both Bunkkeri and Pikkala individuals carried distinct F. aquilonia-like mitotypes (Fig 1D). F. polyctena-like mitotypes were observed in the Långholmen population (Fig 1D), where 2 hybrid lineages termed W and R coexist (S1 Fig, [23]). These lineages basically share a single mitotype and are possibly maintained through environment-dependent genetic incompatibilities and assortative mating [24,25]. The 3 hybrid populations have highly differentiated mitotypes (108 mutational steps between both F. aquilonia-like and F. polyctena-like clusters, Fig 1D) and nuclear DNA (mean pairwise F ST estimates between hybrid populations ranging from 0.18 to 0.23) but low diversity of mitotypes within a population (≤2). These results are consistent with population bottlenecks during colony establishment coupled with little long-distance dispersal, as described above.

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TIFF original image Download: Fig 1. Young, independently evolving hybrid wood ant populations between F. aquilonia and F. polyctena in Southern Finland. (A) Sampling sites across Europe (eCH: East Switzerland, wCH: West Switzerland, map base layer from Natural Earth: https://www.naturalearthdata.com/downloads/110m-physical-vectors). (B) Principal component analysis of 46,886 nuclear SNPs (5 kbp-thinned, MAC ≥ 2). PC1 discriminates between both species and PC2 between hybrid populations. Colors and symbols as in panel A. (C) sNMF estimation of individual ancestry coefficients for K = 2 and K = 6 populations (cross-entropy criterion gives K = 6 as the best K, see S1 Table for detailed admixture proportions computed using sNMF K = 2 , LOTER and naive chromosome painting outputs). (D) Haplotype network derived from 199 mitochondrial SNPs. Circles represent haplotypes, with sizes proportional to their. Dashes indicate the number of mutational steps, with numbers ≥5 provided. The black arrow indicates 2 Finnish F. polyctena individuals carrying F. aquilonia-like mitotypes. (E) Admixture history between F. aquilonia and F. polyctena inferred through an SFS-based approach. The question marks represent the uncertainty associated with the admixture model: parameter estimates are comparable under both single origin and independent origins scenarios, but single origin models support separation of hybrid populations after brief periods of shared ancestry. N e : average effective population size in number of haploids, m: migration rate. (F) Results of the model choice analysis performed with FASTSIMCOAL2 for each population pair. SO: single origin scenario; IO: independent origins scenario; IOm: independent origins scenario with migration between hybrid populations after admixture. The data underlying this figure can be found in https://doi.org/10.6084/m9.figshare.c.6140793.v3. MAC, minor allele count; SFS, site-frequency spectrum; SNP, single-nucleotide polymorphism. https://doi.org/10.1371/journal.pbio.3001914.g001

To elucidate the ancestry of the hybrid populations and date admixture events, we reconstructed the demographic histories of pairs of hybrid populations using a coalescent approach based on the site-frequency spectrum (SFS) of nuclear SNPs (FASTSIMCOAL2 [26]). Coalescent analyses support balanced admixture proportions between species (i.e., no apparent minor ancestry; Fig 1E and S2–S11 Tables), with comparable parameter estimates under scenarios assuming a single origin (SO, 1 admixture event) or independent origins (IO, multiple admixture events, S7–S11 Tables). Consistent with field observations, assuming hybridization events occurred over the last 50 generations led to higher likelihoods (compared to older admixture events), with admixture time estimates ranging from 14 to 47 generations ago (S2–S11 Tables). Model choice provided more support towards an IO scenario for the Bunkkeri—LångholmenW pair (median relative likelihoods: L IO = 0.99, L SO = 0.01; Fig 1F) and Bunkkeri—Pikkala (L IO = 0.88, L SO = 0.10; Fig 1F) and towards an SO scenario for the LångholmenW—LångholmenR pair (L IO = 0, L SO = 1.00; Fig 1F). Results were inconclusive for the remaining pair (Pikkala—LångholmenW: L IO = 0.43, L SO = 0.37; Fig 1F). Parameter estimates from models that assume SO indicate that even if the hybrid populations originate from a single admixture event, they mostly evolved independently (on average 9.5 generations of shared ancestry since admixture, S7–S11 Tables). Following the admixture events, no significant gene flow was inferred either between hybrid populations or between hybrids and both species (L IOm < 0.12 in all comparisons, S7–S11 Tables and Fig 1F). These demographic reconstruction results and patterns of mitochondrial variation are consistent with 2 alternative scenarios for the origin of these hybrid populations. Either they arose through independent hybridization events or an ancestral hybrid population combining several matrilines from both species was established and split into 3 locations, spanning 60 km within <50 generations. Considering wood ant reproductive and dispersal biology, we suggest independent admixture events (IO) as a more likely scenario, in line with model choice supporting IO for 2 population comparisons. However, we acknowledge that reconstructing very recent events accurately is challenging, and we next evaluate our results in the light of both IO and SO scenarios.

To investigate how evolution has shaped hybrid genomes after admixture, we mapped ancestry components along chromosomes independently for each hybrid population. To do this, we inferred local ancestry at 1.5 million phased SNPs using LOTER (Fig 2A [27]) and quantified tree topology weights in 100-SNP windows with TWISST (Fig 2B [28]). Hybrid populations have strongly correlated admixture landscapes along the genome (i.e., local ancestry in 1 population predicts the local ancestry in another population, Figs 2D and S3, Spearman’s rank correlation coefficients computed from TWISST weights ranging from 0.51 to 0.62, P < 10−15 for all population pairs). To test whether such predictability would be expected under neutrality, we used MSPRIME [29] to simulate neutral admixture events following both SO and IO scenarios for each hybrid population pair, using demographic parameters inferred with FASTSIMCOAL2 for the same pair. In all instances (4 population pairs × 2 admixture scenarios), neutral simulations led to balanced contributions of both ancestry components along the genome, but did not capture the clear deviations towards either ancestry component observed locally in the genome (i.e., sorting) with our empirical data (Fig 2C–2E, two-sample Kolmogorov–Smirnov tests, P < 10−15 for all populations, S3 and S4 Figs and S12 and S13 Tables). Thus, the extent of correlated sorting among hybrid populations cannot be explained solely by neutral processes, including the admixture scenario (SO versus IO) and/or demographic history. Moreover, both SFS-based demographic modeling (Fig 1F) and the lack of mitochondrial haplotype sharing between hybrid populations (Fig 1D) argue against gene flow as a potential source for the parallelism observed. As such, other mechanisms must be invoked to explain the rapid evolution of sorted and correlated admixture landscapes in the different hybrid populations.

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TIFF original image Download: Fig 2. Sorting of genetic variation is more correlated than expected under neutrality across 3 hybrid wood ant populations. Examples of (A) local ancestry and (B) topology weighting patterns (green: hybrids locally related to F. aquilonia, yellow: hybrids locally related to F. polyctena) inferred independently in each population along 1 pseudo-chromosome (Scaffold 13). (C) Excess of extreme topology weightings in observed compared to simulated data (IO, SO) in all populations. Empirical and simulated distributions compared with two-sample Kolmogorov–Smirnov tests (D, test statistic and P, P-value). (D) Genome-wide comparison of topology weighting differences between each population pair (Δ WEIGHT. : F. aquilonia weighting minus F. polyctena weighting, computed per population over 14,890 100-SNP windows, gray circles). The regression line is indicated in white. ρ, Spearman’s correlation coefficient and P, P-value of the Spearman’s correlation test. (E) A larger fraction of the genome is sorted in observed compared to simulated data in all populations (sorting measured as the absolute F. aquilonia or F. polyctena weighting, see S3 Fig for detailed results per pairwise comparison). The data underlying this figure can be found in https://doi.org/10.6084/m9.figshare.c.6140793.v3. IO, independent origins; SO, single origin. https://doi.org/10.1371/journal.pbio.3001914.g002

We hypothesized that correlated sorting of genetic variation in hybrid populations is caused by selection against deleterious alleles that have accumulated in the hybridizing species with the lowest effective population size (N e [7,8,30,31]). This effect is expected to be stronger in gene-dense regions [8,32] but also in low-recombining regions [14], where tighter linkage between deleterious alleles, and between neutral and deleterious alleles, leads to removal of larger tracts of ancestry. The 2 Formica species were estimated to have contrasting effective population sizes, with a ca. 30% lower N e in F. polyctena compared to F. aquilonia in the last 200,000 generations ([23], Fig 1E). In hybrid populations, sorting (hereafter ≥90% of either ancestry component inferred from LOTER at a given locus) was faster in low-recombining regions of the genome, as well as in gene-rich regions (Figs 3A and S5). Moreover, in low-recombining regions, the F. aquilonia ancestry was preferentially fixed in all populations (Fig 3A). Focusing on coding SNPs, we found a significant enrichment for F. aquilonia ancestry genome-wide in all populations, consistent with the hypothesis that hybrid populations have purged the deleterious load accumulated in F. polyctena due to its smaller N e (genomic permutations, P < 0.002 in all populations, Fig 3B). These results support the contributions of both recombination rate variation and genetic load in promoting sorting of ancestral variation in hybrids, as previously characterized in other study systems (reviewed in [33]). Our study also reveals that consistent sorting of ancestral variation can happen in less than 50 generations in small populations (Fig 1E).

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TIFF original image Download: Fig 3. Sorting of ancestral polymorphism in hybrids is driven by recombination rate variation and genetic load. (A) Heatmap showing the fraction of sorted 20 kbp windows and the direction of sorting (ancestry component fixed) as a function of recombination rate and gene density quantiles in each hybrid population. (B) Coding regions are significantly enriched for the F. aquilonia ancestry component in all hybrid populations (P < 0.002). For each population (panel, same as A) is plotted local ancestry (y-axis, 0: F. aquilonia allele fixed, 1: F. polyctena allele fixed) as a function of the fraction of SNPs within CDS (x-axis). Confidence intervals (in gray) were obtained using 500 genomic permutations (white line: median of the permutation approach). The data underlying this figure can be found in https://doi.org/10.6084/m9.figshare.c.6140793.v3. CDS, coding sequence; SNP, single-nucleotide polymorphism. https://doi.org/10.1371/journal.pbio.3001914.g003

Positive selection could contribute to the correlated sorting of genetic variation across hybrid populations: advantageous alleles from either species could repeatedly sweep in distinct hybrid populations after admixture. Under this scenario, a genomic region fixed for the F. aquilonia ancestry component in hybrids would display signatures of selection in F. aquilonia individuals. To test this hypothesis, we looked for selective sweep signatures in both hybridizing species with RAiSD [34], which quantifies changes in the SFS, levels of linkage disequilibrium and genetic diversity along the genome through the composite sweep statistic μ (Fig 4). Consistently sorted genomic windows (i.e., windows fixed for either species ancestry across all hybrid populations, 1.92% of the windows overall) displayed significantly higher sweep statistics only in the species from which the ancestry component was fixed in hybrids (genomic permutations, P < 0.001, Fig 4B). While recombination rate estimates were significantly lower than the rest of the genome in these consistently sorted windows (Wilcoxon test, W = 1,740,660, P < 10−15), purging of load in low-recombining regions cannot explain the observation that hybrids have fixed ancestry from the species where a sweep may have occurred prior to hybridization (Fig 4B).

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TIFF original image Download: Fig 4. Signatures of selective sweeps in hybridizing species predict the direction of sorting in admixed genomes. (A) Distribution of selective sweep statistics (μ) computed over 20 kbp windows in F. aquilonia (left) and F. polyctena (right). Genome-wide μ distribution (gray) and observed values in windows fixed for either F. aquilonia (n = 104 windows, green) or F. polyctena ancestry components (n = 98, yellow) in all hybrid populations. (B) Windows fixed for either F. aquilonia (left) or F. polyctena (right) ancestry components in all hybrid populations are significantly enriched for high μ values in F. aquilonia or F. polyctena individuals, respectively. This suggests that a haplotype with a signature of positive selection in either species is more likely to fix in hybrids. Simulated μ values were obtained through 1,000 genomic permutations (as in [64]). Each circle represents medians computed over all consistently sorted windows (solid: observed, open: simulated). The data underlying this figure can be found in https://doi.org/10.6084/m9.figshare.c.6140793.v3. https://doi.org/10.1371/journal.pbio.3001914.g004

Hybrid genomes provide powerful insights into evolution because they are exposed to strong, and often opposing, selective forces [33]. In this study, we coupled reconstruction of admixture histories, local ancestry inference, and coalescent simulations to show that the sorting of ancestral variation is predictable and, in some instances, likely independent across several natural hybrid ant populations. Some predictability has been previously characterized in other systems (e.g., [9]), and introgression is for example limited on sex chromosomes compared to autosomes in replicated hybrid populations of both Italian sparrows [10] and Lycaeides butterflies [12]. We also documented that the known interplay between negative selection and recombination rate variation contributes to remarkable correlation of ancestry components along the genome between hybrid wood ant populations (Spearman’s rank correlation coefficients using TWISST ranging from 0.51 to 0.62 in hybrid wood ants, Fig 2D). Since ancestry proportions are balanced in hybrid wood ants, negative selection should not target any minor ancestry component, as assumed under unbalanced ancestry proportions and when species barriers are highly polygenic (e.g., [8]). Instead, our results suggest that negative selection is impacting ancestry from the species with the smaller effective population size, and presumably a higher load of deleterious alleles. Distinguishing signatures of incompatibilities from those of genetic load and their possible interplay remains a challenge for future studies.

We also showed, to our knowledge for the first time, that events of positive selection prior to admixture likely contribute to the predictability of admixture outcomes (see [35] for a theoretical treatment): Genomic regions displaying signatures of selective sweeps in 1 hybridizing species tend to fix the same ancestry component in hybrid populations. These genomic regions could also act as incompatibilities, which we cannot identify on the sole basis of our data, but which impact the landscape of introgression in hybrids [9], as previously documented in our study system [23,36]. In the future, novel methodological developments [37,38] coupled with larger sample sizes may allow identifying candidate incompatibilities in hybrid wood ants.

Finally, in contrast to other recent studies of hybrid genome evolution, the ant hybrids still show balanced ancestry contributions after ca. 50 generations since admixture. Fluctuating, environment-dependent selection could be one mechanism maintaining both ancestry components in hybrids, as microsatellite allele frequencies of the cold-adapted F. aquilonia species have been shown to positively correlate with yearly temperature over a 16-year time period in one of the hybrid populations we studied [25]. As this correlation was stronger in males, haplodiploidy is another mechanism that may contribute to the maintenance of genetic variation in wood ants. To conclude, we have shown that the sorting of ancestral genetic variation in hybrid genomes can occur rapidly and predictably after admixture due to both positive and purifying selection.

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[1] Url: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3001914

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