Natal dispersal, mating patterns and inbreeding in the ant Formica exsecta

Peer reviewe

How do species barriers decay? Concordance and local introgression in mosaic hybrid zones of mussels.

The Mytilus complex of marine mussel species forms a mosaic of hybrid zones, found across temperate regions of the globe. This allows us to study 'replicated' instances of secondary contact between closely related species. Previous work on this complex has shown that local introgression is both widespread and highly heterogeneous, and has identified SNPs that are outliers of differentiation between lineages. Here, we developed an ancestry-informative panel of such SNPs. We then compared their frequencies in newly sampled populations, including samples from within the hybrid zones, and parental populations at different distances from the contact. Results show that close to the hybrid zones, some outlier loci are near to fixation for the heterospecific allele, suggesting enhanced local introgression, or the local sweep of a shared ancestral allele. Conversely, genomic cline analyses, treating local parental populations as the reference, reveal a globally high concordance among loci, albeit with a few signals of asymmetric introgression. Enhanced local introgression at specific loci is consistent with the early transfer of adaptive variants after contact, possibly including asymmetric bi-stable variants (Dobzhansky-Muller incompatibilities), or haplotypes loaded with fewer deleterious mutations. Having escaped one barrier, however, these variants can be trapped or delayed at the next barrier, confining the introgression locally. These results shed light on the decay of species barriers during phases of contact.ANR, France; Russian Science Foundatio

Direct Estimation of the Mitochondrial DNA Mutation Rate in Drosophila melanogaster

Mitochondrial DNA (mtDNA) variants are widely used in evolutionary genetics as markers for population history and to estimate divergence times among taxa. Inferences of species history are generally based on phylogenetic comparisons, which assume that molecular evolution is clock-like. Between-species comparisons have also been used to estimate the mutation rate, using sites that are thought to evolve neutrally. We directly estimated the mtDNA mutation rate by scanning the mitochondrial genome of Drosophila melanogaster lines that had undergone approximately 200 generations of spontaneous mutation accumulation (MA). We detected a total of 28 point mutations and eight insertion-deletion (indel) mutations, yielding an estimate for the single-nucleotide mutation rate of 6.2 × 10−8 per site per fly generation. Most mutations were heteroplasmic within a line, and their frequency distribution suggests that the effective number of mitochondrial genomes transmitted per female per generation is about 30. We observed repeated occurrences of some indel mutations, suggesting that indel mutational hotspots are common. Among the point mutations, there is a large excess of G→A mutations on the major strand (the sense strand for the majority of mitochondrial genes). These mutations tend to occur at nonsynonymous sites of protein-coding genes, and they are expected to be deleterious, so do not become fixed between species. The overall mtDNA mutation rate per base pair per fly generation in Drosophila is estimated to be about 10× higher than the nuclear mutation rate, but the mitochondrial major strand G→A mutation rate is about 70× higher than the nuclear rate. Silent sites are substantially more strongly biased towards A and T than nonsynonymous sites, consistent with the extreme mutation bias towards A+T. Strand-asymmetric mutation bias, coupled with selection to maintain specific nonsynonymous bases, therefore provides an explanation for the extreme base composition of the mitochondrial genome of Drosophila

Uncovering cryptic asexuality in Daphnia magna by RAD sequencing

The breeding systems of many organisms are cryptic and difficult to investigate with observational data, yet they have profound effects on a species’ ecology, evolution, and genome organization. Genomic approaches offer a novel, indirect way to investigate breeding systems, specifically by studying the transmission of genetic information from parents to offspring. Here we exemplify this method through an assessment of self-fertilization vs. automictic parthenogenesis in Daphnia magna. Self-fertilization reduces heterozygosity by 50% compared to the parents, but under automixis, whereby two haploid products from a single meiosis fuse, the expected heterozygosity reduction depends on whether the two meiotic products are separated during meiosis I or II (i.e., central vs. terminal fusion). Reviewing the existing literature and incorporating recombination interference, we derive an interchromosomal and an intrachromosomal prediction of how to distinguish various forms of automixis from self-fertilization using offspring heterozygosity data. We then test these predictions using RAD-sequencing data on presumed automictic diapause offspring of so-called nonmale producing strains and compare them with “self-fertilized” offspring produced by within-clone mating. The results unequivocally show that these offspring were produced by automixis, mostly, but not exclusively, through terminal fusion. However, the results also show that this conclusion was only possible owing to genome-wide heterozygosity data, with phenotypic data as well as data from microsatellite markers yielding inconclusive or even misleading results. Our study thus demonstrates how to use the power of genomic approaches for elucidating breeding systems, and it provides the first demonstration of automictic parthenogenesis in Daphnia

Inbreeding and reproductive investment in the ant Formica exsecta

In social animals, inbreeding depression may manifest by compromising care or resources individuals receive from inbred group members. We studied the effects of worker inbreeding on colony productivity and investment in the ant Formica exsecta. The production of biomass decreased with increasing inbreeding, as did biomass produced per worker. Inbred colonies produced fewer gynes (unmated reproductive females), whereas the numbers of males remained unchanged. As a result, sex ratios showed increased male bias, and the fraction of workers increased among the diploid brood. Males raised in inbred colonies were smaller, whereas the weight of gynes remained unchanged. The results probably reflect a trade-off between number and quality of offspring, which is expected if the reproductive success of gynes is more dependent on their weight or condition than it is for males. As males are haploid (with the exception of abnormal diploid males produced in very low frequencies in this population), and therefore cannot be inbred themselves, the effect on their size must be mediated through the workers of the colony. We suggest the effects are caused by the inbred workers being less proficient in feeding the growing larvae. This represents a new kind of social inbreeding depression that may affect sex ratios as well as caste fate in social insects

Bayesian inference of parental allele inheritance in fetus for noninvasive prenatal diagnosis

International audienceThe field of noninvasive prenatal diagnosis (NIPD) has undergone significant progress over the last decade. Direct haplotyping has been successfully applied for NIPD of a few single-gene disorders. However, technical issues remain for triplet-repeat expansion diseases (a.k.a. trinucleotide repeat disorder). Developping an NIPD approach for couples at risk of transmitting dynamic mutations is thus challenging but crucial. For instance, fetal genotyping using circulating cell-free fetal DNA (cff-DNA) from maternal blood might not be able to detect complex genetic patterns in the fetal DNA that could have been inherited from a parent at risk. In such family, a workaround would be to directly detect which haplotypes among the pair of parental homologous chromosomes have been inherited by the fetus, for an entire targeted region of the genome. In combination with haplotype phasing of the parent(s) at risk, it would allow to determine if the haplotype region carrying the pathogenic variation was transmitted to the fetus or not.We present a Bayesian approach that is able, not only to infer the fetal genotype, but more importantly to directly infer the fetal allele origin from the parental phased haplotypes at each locus in a target chromosome region. In particular, our model aims to identify the parental haplotype of origin for the genetic material inherited by the fetus. To do so, only haplotype data from both parents and genotype data from circulating cell-free DNA (cf-DNA) in maternal plasma (i.e. a mix of maternal and fetal DNA) are used. On contrary to existing fetal genotyping models which consider all loci independently, we infer the allele origin jointly on all loci in the targeted region. Because of combinatorial issues, we cannot directly derive the joint posterior but we rather use a Markov chain Monte Carlo (MCMC) procedure (specifically a Gibbs sampler) to estimate the full posterior over the entire region, and a maximum a posteriori (MAP) estimation to determine the allele inheritance patterns over the entire region.We performed analyses using blood samples from families with Huntington’s disease or myotonic dystrophy type 1. We were able to perform the Bayesian inference of parental haplotype transmissions for five fetuses. The predicted variant status of four of these fetuses was in agreement with the invasive prenatal diagnosis findings. Conversely, no conclusive result was obtained for the NIPD of fragile X syndrome. Although improvements should be made to achieve clinically acceptable accuracy, our study shows that linked-read sequencing and parental haplotype phasing can be successfully used for NIPD of triplet-repeat expansion diseases

Distinguishing contemporary hybridization from past introgression with post-genomic ancestry-informative SNPs in strongly differentiated Ciona species

International audienceBiological introductions bring into contact species that can still hybridize. The evolutionary outcomes of such secondary contacts may be diverse (e.g. adaptive introgression from or into the introduced species) but are not yet well examined in the wild. The recent secondary contact between the non-native sea squirt Ciona robusta (formerly known as C. intestinalis type A) and its native congener C. intestinalis (formerly known as C. intestinalis type B), in the Western English Channel, provides an excellent case study to examine. To examine contemporary hybridization between the two species, we developed a panel of 310 ancestry-informative SNPs from a population transcriptomic study. Hybridization rates were examined on 449 individuals sampled in eight sites from the sympatric range and five sites from allopatric ranges. The results clearly showed an almost complete absence of contemporary hybridization between the two species in syntopic localities, with only one-first-generation hybrid and no other genotype compatible with recent backcrosses. Despite the almost lack of contemporary hybridization, shared polymorphisms were observed in sympatric and allopatric populations of both species. Furthermore, one allopatric population from SE Pacific exhibited a higher rate of shared polymorphisms compared to all other C. robusta populations. Altogether, these results indicate that the observed level of shared polymorphism is more probably the outcome of ancient gene flow spread afterwards at a worldwide scale. They also emphasize efficient reproductive barriers preventing hybridization between introduced and native species, which suggests hybridization should not impede too much the expansion and the establishment of the non-native species in its introduction range

Data from: Natal dispersal, mating patterns, and inbreeding in the ant Formica exsecta

Sex-biased dispersal and multiple mating may prevent or alleviate inbreeding and its outcome, inbreeding depression, but studies demonstrating this in the wild are scarce. Perennial ant colonies offer a unique system to investigate the relationships between natal dispersal behaviour and inbreeding. Due to the sedentary life of ant colonies and life-time sperm storage by queens, measures of dispersal distance and mating strategy are easier to obtain than in most taxa. We used a suite of molecular markers to infer the natal colonies of queens and males in a wild population of the ant Formica exsecta. Dispersal was male-biased, with median male dispersal distances (ca. 140m) twice those of queens (ca. 60m). The results show the population to be inbred, and that inbreeding avoidance behaviours - sex-biased dispersal, queen dispersal distance and multiple mating - were all ineffective in reducing homozygosity among colony workers. Queen homozygosity did not affect dispersal behaviour, but more homozygous queens had lower colony founding success and were more incestuously mated themselves, with potentially accumulating effects on colony fitness. We also provide independent evidence that dispersal is sex-biased, and show that our estimate corresponds well to dispersal estimates derived from population genetic estimates

Full dataset 310 SNPs

Full dataset of the 310 SNPs using to investigate contemporary hybridization and introgression patterns between two Ciona species (Ciona robusta and Ciona intestinalis). The file contains the genotype of the 451 individuals studied (213 of C. robusta, 236 of C. intestinalis and 2 F1 hybrids from experimental crosses; note that the natural F1 hybrid found in our study is included in the 236 individuals of C. intestinalis). The file contains also informations on the 310 SNPs (chromosome number, exact nucleotide position along chromosomes and category of polymorphism)