Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near-instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky-Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock-on effects on speciation both within and outside regions of hybridization.

Comparative analysis of multiple genomes in a phylogenetic framework dramatically improves the precision and sensitivity of evolutionary inference, producing more robust results than single-genome analyses can provide. The genomes of 12 Drosophila species, ten of which are presented here for the first time (sechellia, simulans, yakuba, erecta, ananassae, persimilis, willistoni, mojavensis, virilis and grimshawi), illustrate how rates and patterns of sequence divergence across taxa can illuminate evolutionary processes on a genomic scale. These genome sequences augment the formidable genetic tools that have made Drosophila melanogaster a pre-eminent model for animal genetics, and will further catalyse fundamental research on mechanisms of development, cell biology, genetics, disease, neurobiology, behaviour, physiology and evolution. Despite remarkable similarities among these Drosophila species, we identified many putatively non-neutral changes in protein-coding genes, non-coding RNA genes, and cis-regulatory regions. These may prove to underlie differences in the ecology and behaviour of these diverse species.

Sexual selection has a reputation as a major cause of speciation, one of the most potent forces driving reproductive isolation. This reputation arises from observations that species differ most in traits involved with mating success and from successful models of sexual selection–driven speciation. But how well proven is the case? Models confirm that the process can occur, but is strongest in conjunction with ecological or niche specialization. Some models also show that strong sexual selection can act against speciation. Studies using the comparative method are equivocal and often inconclusive, but some phylogeographic studies are more convincing. Experimental evolution and genetic or genomic analyses are in their infancy, but look particularly promising for resolving the importance of sexual selection. The case for sexual selection is not as strongly supported as, for example, allopatric speciation. Sexual selection probably contributes most effectively alongside ecological selection or selection for species recognition than as a solitary process.

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Abstract Genetic variation is the fuel of evolution, with standing genetic variation especially important for short-term evolution and local adaptation. To date, studies of spatiotemporal patterns of genetic variation in natural populations have been challenging, as comprehensive sampling is logistically difficult, and sequencing of entire populations costly. Here, we address these issues using a collaborative approach, sequencing 48 pooled population samples from 32 locations, and perform the first continent-wide genomic analysis of genetic variation in European Drosophila melanogaster. Our analyses uncover longitudinal population structure, provide evidence for continent-wide selective sweeps, identify candidate genes for local climate adaptation, and document clines in chromosomal inversion and transposable element frequencies. We also characterize variation among populations in the composition of the fly microbiome, and identify five new DNA viruses in our samples.

Parenting in the burying beetle Nicrophorus vespilloides is complex and, unusually, the sex and number of parents that can be present is flexible. Such flexibility is expected to involve specialized behaviour by the two sexes under biparental conditions. Here, we show that offspring fare equally well regardless of the sex or number of parents present. Comparing transcriptomes, we find a largely overlapping set of differentially expressed genes in both uniparental and biparental females and in uniparental males including vitellogenin, associated with reproduction, and takeout, influencing sex-specific mating and feeding behaviour. Gene expression in biparental males is similar to that in non-caring states. Thus, being ‘biparental’ in N. vespilloides describes the family social organization rather than the number of directly parenting individuals. There was no specialization; instead, in biparental families, direct male parental care appears to be limited with female behaviour unchanged. This should lead to strong sexual conflict.

SummaryBackgroundIn Drosophila, male courtship behavior is regulated in large part by the gene fruitless (fru). fru encodes a set of putative transcription factors that promote male sexual behavior by controlling the development of sexually dimorphic neuronal circuitry. Little is known about how Fru proteins function at the level of transcriptional regulation or the role that isoform diversity plays in the formation of a male-specific nervous system.ResultsTo characterize the roles of sex-specific Fru isoforms in specifying male behavior, we generated novel isoform-specific mutants and used a genomic approach to identify direct Fru isoform targets during development. We demonstrate that all Fru isoforms directly target genes involved in the development of the nervous system, with individual isoforms exhibiting unique binding specificities. We observe that fru behavioral phenotypes are specified by either a single isoform or a combination of isoforms. Finally, we illustrate the utility of these data for the identification of novel sexually dimorphic genomic enhancers and novel downstream regulators of male sexual behavior.ConclusionsThese findings suggest that Fru isoform diversity facilitates both redundancy and specificity in gene expression, and that the regulation of neuronal developmental genes may be the most ancient and conserved role of fru in the specification of a male-specific nervous system.

The earliest stages of convergent evolution are difficult to observe in the wild, limiting our understanding of the incipient genomic architecture underlying convergent phenotypes. To address this, we capitalized on a novel trait, flatwing, that arose and proliferated at the start of the 21st century in a population of field crickets (Teleogryllus oceanicus) on the Hawaiian island of Kauai. Flatwing erases sound-producing structures on male forewings. Mutant males cannot sing to attract females, but they are protected from fatal attack by an acoustically orienting parasitoid fly (Ormia ochracea). Two years later, the silent morph appeared on the neighboring island of Oahu. We tested two hypotheses for the evolutionary origin of flatwings in Hawaii: (1) that the silent morph originated on Kauai and subsequently introgressed into Oahu and (2) that flatwing originated independently on each island. Morphometric analysis of male wings revealed that Kauai flatwings almost completely lack typical derived structures, whereas Oahu flatwings retain noticeably more wild-type wing venation. Using standard genetic crosses, we confirmed that the mutation segregates as a single-locus, sex-linked Mendelian trait on both islands. However, genome-wide scans using RAD-seq recovered almost completely distinct markers linked with flatwing on each island. The patterns of allelic association with flatwing on either island reveal different genomic architectures consistent with the timing of two mutational events on the X chromosome. Divergent wing morphologies linked to different loci thus cause identical behavioral outcomes--silence--illustrating the power of selection to rapidly shape convergent adaptations from distinct genomic starting points.