Breeding system and reproductive skew in a highly polygynous ant population

Abstract.: Factors affecting relatedness among nest members in ant colonies with high queen number are still poorly understood. In order to identify the major determinants of nest kin structure, we conducted a detailed analysis of the breeding system of the ant Formica exsecta. We estimated the number of mature queens by mark-release-recapture in 29 nests and dissected a sub-sample of queens to assess their reproductive status. We also used microsatellites to estimate relatedness within and between all classes of nestmates (queens, their mates, worker brood, queen brood and male brood). Queen number was very high, with an arithmetic mean of 253 per nest. Most queens (90%) were reproductively active, consistent with the genetic analyses revealing that there was only a minimal reproductive skew among nestmate queens. Despite the high queen number and low reproductive skew, almost all classes of individuals were significantly related to each other. Interestingly, the number of resident queens was a poor predictor of kin structure at the nest level, consistent with the observation that new queens are produced in bursts leading to highly fluctuating queen number across years. Queen number also varied tremendously across nests, with estimates ranging from five to several hundred queens. Accordingly, the harmonic mean queen number (40.5) was six times lower than the arithmetic mean. The variation in queen number was the most important factor of the breeding system contributing to a significant relatedness between almost all classes of nestmates despite a high average number of queens per nes

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

Mutation Patterns in the Human Genome: More Variable Than Expected

Why are some genomic positions more mutable than others? The identification of cryptic mutation hotspots in the human genome indicates that the determinants of mutation rates are more complex than anticipated

Maternal age effect and severe germ-line bottleneck in the inheritance of human mitochondrial DNA

The manifestation of mitochondrial DNA (mtDNA) diseases depends on the frequency of heteroplasmy (the presence of several alleles in an individual), yet its transmission across generations cannot be readily predicted owing to a lack of data on the size of the mtDNA bottleneck during oogenesis. For deleterious heteroplasmies, a severe bottleneck may abruptly transform a benign (low) frequency in a mother into a disease-causing (high) frequency in her child. Here we present a high-resolution study of heteroplasmy transmission conducted on blood and buccal mtDNA of 39 healthy mother–child pairs of European ancestry (a total of 156 samples, each sequenced at ∼20,000× per site). On average, each individual carried one heteroplasmy, and one in eight individuals carried a disease-associated heteroplasmy, with minor allele frequency ≥1%. We observed frequent drastic heteroplasmy frequency shifts between generations and estimated the effective size of the germ-line mtDNA bottleneck at only ∼30–35 (interquartile range from 9 to 141). Accounting for heteroplasmies, we estimated the mtDNA germ-line mutation rate at 1.3 × 10−8 (interquartile range from 4.2 × 10−9 to 4.1 × 10−8) mutations per site per year, an order of magnitude higher than for nuclear DNA. Notably, we found a positive association between the number of heteroplasmies in a child and maternal age at fertilization, likely attributable to oocyte aging. This study also took advantage of droplet digital PCR (ddPCR) to validate heteroplasmies and confirm a de novo mutation. Our results can be used to predict the transmission of disease-causing mtDNA variants and illuminate evolutionary dynamics of the mitochondrial genome

Estimation of the spontaneous mutation rate in Heliconius melpomene

This is the final published version. It first appeared at mbe.oxfordjournals.org/content/early/2014/11/03/molbev.msu302.abstract.We estimated the spontaneous mutation rate in Heliconius melpomene by genome sequencing of\ud a pair of parents and 30 of their offspring, based on the ratio of number of de novo heterozygotes\ud to the number of callable site-individuals. We detected nine new mutations, each one affecting a\ud single site in a single offspring. This yields an estimated mutation rate of 2.9 x 10-9 (95%\ud confidence interval, 1.3 x 10-9 - 5.5 x 10-9), which is similar to recent estimates in Drosophila\ud melanogaster, the only other insect species in which the mutation rate has been directly estimated.\ud We infer that recent effective population size of H. melpomene is about 2 million, a substantially\ud lower value than its census size, suggesting a role for natural selection reducing diversity. We\ud estimate that H. melpomene diverged from its M?llerian co-mimic H. erato about 6 MYA, a\ud somewhat later date than estimates based on a local molecular clock.CJ was funded by BBSRC [H01439X/1], JWD was funded by the Herchel Smith Fund and PDK and\ud RWN were funded by the BBSRC

FITNESS CONSEQUENCES OF SEX-SPECIFIC SELECTION

Theory suggests that sex-specific selection can facilitate adaptation in sexually reproducing populations. However, sexual conflict theory and recent experiments indicate that sex-specific selection is potentially costly due to sexual antagonism: alleles harmful to one sex can accumulate within a population because they are favored in the other sex. Whether sex-specific selection provides a net fitness benefit or cost depends, in part, on the relative frequency and strength of sexually concordant versus sexually antagonistic selection throughout a species’ genome. Here, we model the net fitness consequences of sex-specific selection while explicitly considering both sexually concordant and sexually antagonistic selection. The model shows that, even when sexual antagonism is rare, the fitness costs that it imposes will generally overwhelm fitness benefits of sexually concordant selection. Furthermore, the cost of sexual antagonism is, at best, only partially resolved by the evolution of sex-limited gene expression. To evaluate the key parameters of the model, we analyze an extensive dataset of sex-specific selection gradients from wild populations, along with data from the experimental evolution literature. The model and data imply that sex-specific selection may likely impose a net cost on sexually reproducing species, although additional research will be required to confirm this conclusion.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/78600/1/j.1558-5646.2009.00934.x.pd

High Rate of Large Deletions in Caenorhabditis briggsae Mitochondrial Genome Mutation Processes

Mitochondrial DNA (mtDNA) mutations underlie a variety of human genetic disorders and are associated with the aging process. mtDNA polymorphisms are widely used in a variety of evolutionary applications. Although mtDNA mutation spectra are known to differ between distantly related model organisms, the extent to which mtDNA mutation processes vary between more closely related species and within species remains enigmatic. We analyzed mtDNA divergence in two sets of 250-generation Caenorhabditis briggsae mutation-accumulation (MA) lines, each derived from a different natural isolate progenitor: strain HK104 from Okayama, Japan, and strain PB800 from Ohio, United States. Both sets of C. briggsae MA lines accumulated numerous large heteroplasmic mtDNA deletions, whereas only one similar event was observed in a previous analysis of Caenorhabditis elegans MA line mtDNA. Homopolymer length change mutations were frequent in both sets of C. briggsae MA lines and occurred in both intergenic and protein-coding gene regions. The spectrum of C. briggsae mtDNA base substitution mutations differed from the spectrum previously observed in C. elegans. In C. briggsae, the HK104 MA lines experienced many different base substitution types, whereas the PB800 lines displayed only C:G → T:A transitions, although the difference was not significant. Over half of the mtDNA base substitutions detected in the C. briggsae MA lines were in a heteroplasmic state, whereas all those previously characterized in C. elegans MA line mtDNA were fixed changes, indicating a narrower mtDNA bottleneck in C. elegans as compared with C. briggsae. Our results show that C. briggsae mtDNA is highly susceptible to large deletions and that the mitochondrial mutation process varies between Caenorhabditis nematode species