Inexpensive short-read sequencing technologies applied to reduced representation genomes is revolutionizing genetic research, especially population genetics analysis, by allowing the genotyping of massive numbers of single-nucleotide polymorphisms (SNP) for large numbers of individuals and populations. Restriction site-associated DNA (RAD) sequencing is a recent technique based on the characterization of genomic regions flanking restriction sites. One of its potential drawbacks is the presence of polymorphism within the restriction site, which makes it impossible to observe the associated SNP allele (i.e. allele dropout, ADO). To investigate the effect of ADO on genetic variation estimated from RAD markers, we first mathematically derived measures of the effect of ADO on allele frequencies as a function of different parameters within a single population. We then used RAD data sets simulated using a coalescence model to investigate the magnitude of biases induced by ADO on the estimation of expected heterozygosity and F ST under a simple demographic model of divergence between two populations. We found that ADO tends to overestimate genetic variation both within and between populations. Assuming a mutation rate per nucleotide between 10 −9 and 10 −8, this bias remained low for most studied combinations of divergence time and effective population size, except for large effective population sizes. Averaging F ST values over multiple SNPs, for example, by sliding window analysis, did not correct ADO biases. We briefly discuss possible solutions to filter the most problematic cases of ADO using read coverage to detect markers with a large excess of null alleles.

Molecular markers produced by next-generation sequencing (NGS) technologies are revolutionizing genetic research. However, the costs of analysing large numbers of individual genomes remain prohibitive for most population genetics studies. Here, we present results based on mathematical derivations showing that, under many realistic experimental designs, NGS of DNA pools from diploid individuals allows to estimate the allele frequencies at single nucleotide polymorphisms (SNPs) with at least the same accuracy as individual-based analyses, for considerably lower library construction and sequencing efforts. These findings remain true when taking into account the possibility of substantially unequal contributions of each individual to the final pool of sequence reads. We propose the intuitive notion of effective pool size to account for unequal pooling and derive a Bayesian hierarchical model to estimate this parameter directly from the data. We provide a user-friendly application assessing the accuracy of allele frequency estimation from both pool- and individual-based NGS population data under various sampling, sequencing depth and experimental error designs. We illustrate our findings with theoretical examples and real data sets corresponding to SNP loci obtained using restriction site-associated DNA (RAD) sequencing in pool- and individual-based experiments carried out on the same population of the pine processionary moth (Thaumetopoea pityocampa). NGS of DNA pools might not be optimal for all types of studies but provides a cost-effective approach for estimating allele frequencies for very large numbers of SNPs. It thus allows comparison of genome-wide patterns of genetic variation for large numbers of individuals in multiple populations.

Sexual reproduction can lead to major conflicts between sexes and within genomes. Here we report an extreme case of such conflicts in the little fire ant Wasmannia auropunctata. We found that sterile workers are produced by normal sexual reproduction, whereas daughter queens are invariably clonally produced. Because males usually develop from unfertilized maternal eggs in ants and other haplodiploid species, they normally achieve direct fitness only through diploid female offspring. Hence, although the clonal production of queens increases the queen's relatedness to reproductive daughters, it potentially reduces male reproductive success to zero. In an apparent response to this conflict between sexes, genetic analyses reveal that males reproduce clonally, most likely by eliminating the maternal half of the genome in diploid eggs. As a result, all sons have nuclear genomes identical to those of their father. The obligate clonal production of males and queens from individuals of the same sex effectively results in a complete separation of the male and female gene pools. These findings show that the haplodiploid sex-determination system provides grounds for the evolution of extraordinary genetic systems and new types of sexual conflict.

Adaptive evolution is currently accepted as playing a significant role in biological invasions. Adaptations relevant to invasions are typically thought to occur either recently within the introduced range, as an evolutionary response to novel selection regimes, or within the native range, because of long-term adaptation to the local environment. We propose that recent adaptation within the native range, in particular adaptations to human-altered habitat, could also contribute to the evolution of invasive populations. Populations adapted to human-altered habitats in the native range are likely to increase in abundance within areas frequented by humans and associated with human transport mechanisms, thus enhancing the likelihood of transport to a novel range. Given that habitats are altered by humans in similar ways worldwide, as evidenced by global environmental homogenization, propagules from populations adapted to human-altered habitats in the native range should perform well within similarly human-altered habitats in the novel range. We label this scenario ‘Anthropogenically Induced Adaptation to Invade’. We illustrate how it differs from other evolutionary processes that may occur during invasions, and how it can help explain accelerating rates of invasions.

Deciphering invasion routes from molecular data is crucial to understanding biological invasions, including identifying bottlenecks in population size and admixture among distinct populations. Here, we unravel the invasion routes of the invasive pest Drosophila suzukii using a multi-locus microsatellite dataset (25 loci on 23 worldwide sampling locations). To do this, we use approximate Bayesian computation (ABC), which has improved the reconstruction of invasion routes, but can be computationally expensive. We use our study to illustrate the use of a new, more efficient, ABC method, ABC random forest (ABC-RF) and compare it to a standard ABC method (ABC-LDA). We find that Japan emerges as the most probable source of the earliest recorded invasion into Hawaii. Southeast China and Hawaii together are the most probable sources of populations in western North America, which then in turn served as sources for those in eastern North America. European populations are genetically more homogeneous than North American populations, and their most probable source is northeast China, with evidence of limited gene flow from the eastern US as well. All introduced populations passed through bottlenecks, and analyses reveal five distinct admixture events. These findings can inform hypotheses concerning how this species evolved between different and independent source and invasive populations. Methodological comparisons indicate that ABC-RF and ABC-LDA show concordant results if ABC-LDA is based on a large number of simulated datasets but that ABC-RF out-performs ABC-LDA when using a comparable and more manageable number of simulated datasets, especially when analyzing complex introduction scenarios.

SummaryMany animal species comprise discrete phenotypic forms. A common example in natural populations of insects is the occurrence of different color patterns, which has motivated a rich body of ecological and genetic research [1, 2, 3, 4, 5, 6]. The occurrence of dark, i.e., melanic, forms displaying discrete color patterns is found across multiple taxa, but the underlying genomic basis remains poorly characterized. In numerous ladybird species (Coccinellidae), the spatial arrangement of black and red patches on adult elytra varies wildly within species, forming strikingly different complex color patterns [7, 8]. In the harlequin ladybird, Harmonia axyridis, more than 200 distinct color forms have been described, which classic genetic studies suggest result from allelic variation at a single, unknown, locus [9, 10]. Here, we combined whole-genome sequencing, population-based genome-wide association studies, gene expression, and functional analyses to establish that the transcription factor Pannier controls melanic pattern polymorphism in H. axyridis. We show that pannier is necessary for the formation of melanic elements on the elytra. Allelic variation in pannier leads to protein expression in distinct domains on the elytra and thus determines the distinct color patterns in H. axyridis. Recombination between pannier alleles may be reduced by a highly divergent sequence of ∼170 kb in the cis-regulatory regions of pannier, with a 50 kb inversion between color forms. This most likely helps maintain the distinct alleles found in natural populations. Thus, we propose that highly variable discrete color forms can arise in natural populations through cis-regulatory allelic variation of a single gene.

A better understanding of the factors affecting host plant use by spotted-wing drosophila (Drosophila suzukii) could aid in the development of efficient management tools and practices to control this pest. Here, proxies of both preference (maternal oviposition behavior) and performance (adult emergence) were evaluated for 12 different fruits in the form of purees. The effect of the chemical composition of the fruits on preference and performance traits was then estimated. We synthesized the literature to interpret our findings in the light of previous studies that measured oviposition preference and larval performance of D. suzukii. We show that fruit identity influences different parts of the life cycle, including oviposition preference under both choice and no-choice conditions, emergence rate, development time, and number of emerging adults. Blackcurrant was always among the most preferred fruit we used, while grape and tomato were the least preferred fruits. Larvae performed better in cranberry, raspberry, strawberry, and cherry than in the other fruits tested. We found that fruit chemical compounds can explain part of the effect of fruit on D. suzukii traits. In particular, oviposition preference under choice conditions was strongly influenced by fruit phosphorus content. In general, the consensus across studies is that raspberry, blackberry, and strawberry are among the best hosts while blackcurrant, grape and rose hips are poor hosts. Our results generally confirm this view but also suggest that oviposition preferences do not necessarily match larval performances. We discuss opportunities to use our results to develop new approaches for pest management.

Next-generation sequencing opened up new possibilities in phylogenetics; however, choosing an appropriate method of sample preparation remains challenging. Here, we demonstrate that restriction-site-associated DNA sequencing (RAD-seq) generates useful data for phylogenomics. Analysis of our RAD library using current bioinformatic and phylogenetic tools produced 400× more sites than our Sanger approach (2,262,825 nt/species), fully resolving relationships between 18 species of ground beetles (divergences up to 17 My). This suggests that RAD-seq is promising to infer phylogeny of eukaryotic species, though potential biases need to be evaluated and new methodologies developed to take full advantage of such data.