The transition from ‘well-marked varieties’ of a single species into ‘well-defined species’—especially in the absence of geographic barriers to gene flow (sympatric speciation)—has puzzled evolutionary biologists ever since Darwin^1,2. Gene flow counteracts the buildup of genome-wide differentiation, which is a hallmark of speciation and increases the likelihood of the evolution of irreversible reproductive barriers (incompatibilities) that complete the speciation process³. Theory predicts that the genetic architecture of divergently selected traits can influence whether sympatric speciation occurs⁴, but empirical tests of this theory are scant because comprehensive data are difficult to collect and synthesize across species, owing to their unique biologies and evolutionary histories⁵. Here, within a young species complex of neotropical cichlid fishes (Amphilophusspp.), we analysed genomic divergence among populations and species. By generating a new genome assembly and re-sequencing 453 genomes, we uncovered the genetic architecture of traits that have been suggested to be important for divergence. Species that differ in monogenic or oligogenic traits that affect ecological performance and/or mate choice show remarkably localized genomic differentiation. By contrast, differentiation among species that have diverged in polygenic traits is genomically widespread and much higher overall, consistent with the evolution of effective and stable genome-wide barriers to gene flow. Thus, we conclude that simple trait architectures are not always as conducive to speciation with gene flow as previously suggested, whereas polygenic architectures can promote rapid and stable speciation in sympatry.

Showing their stripes: The adaptive radiation of East African cichlids has led to more than 1200 species across a number of lakes. Across these species, many convergent traits have emerged, including the presence or absence of horizontal stripes. Kratochwil et al. show that the appearance or loss of stripes is related to changes in the agouti-related peptide 2 gene, which acts as a kind of on-off switch for stripe generation (see the Perspective by Gante). This action has enabled rapid and repeated evolution of stripes across this speciose radiation. Science , this issue p. 457 ; see also p. 396

The formation of species in the absence of geographic barriers (i.e. sympatric speciation) remains one of the most controversial topics in evolutionary biology. While theoretical models have shown that this most extreme case of primary divergence-with-gene-flow is possible, only a handful of accepted empirical examples exist. And even for the most convincing examples uncertainties remain; complex histories of isolation and secondary contact can make species falsely appear to have originated by sympatric speciation. This alternative scenario is notoriously difficult to rule out. Midas cichlids inhabiting small and remote crater lakes in Nicaragua are traditionally considered to be one of the best examples of sympatric speciation and lend themselves to test the different evolutionary scenarios that could lead to apparent sympatric speciation since the system is relatively small and the source populations known. Here we reconstruct the evolutionary history of two small-scale radiations of Midas cichlids inhabiting crater lakes Apoyo and Xiloá through a comprehensive genomic data set. We find no signs of differential admixture of any of the sympatric species in the respective radiations. Together with coalescent simulations of different demographic models our results support a scenario of speciation that was initiated in sympatry and does not result from secondary contact of already partly diverged populations. Furthermore, several species seem to have diverged simultaneously, making Midas cichlids an empirical example of multispecies outcomes of sympatric speciation. Importantly, however, the demographic models strongly support an admixture event from the source population into both crater lakes shortly before the onset of the radiations within the lakes. This opens the possibility that the formation of reproductive barriers involved in sympatric speciation was facilitated by genetic variants that evolved in a period of isolation between the initial founding population and the secondary migrants that came from the same source population. Thus, the exact mechanisms by which these species arose might be different from what had been thought before. Speciation is the main driver of biological diversity and how species arise is a central question in evolutionary biology. For speciation to occur in sexually reproducing organisms the exchange of genetic material (gene flow) between populations has to be reduced. Ultimately this has to be due to genetically determined reproductive incompatibilities between species. Yet, whether (an initial period of) geographic isolation is necessary for these incompatibilities to evolve has been subject to one of the most persistent debates in evolutionary biology. Sympatric speciation is the most extreme case of primary divergence-with-gene-flow and lies at the heart of this question. However, only few empirical examples of sympatric speciation are generally accepted and in most of these cases some ambiguities and doubts remain. This study provides evidence that the Nicaraguan crater lake cichlids can indeed be considered a valid example of sympatric speciation in the sense that the species themselves probably started to diverge in the absence of geographic barriers. However, the data also suggests that this divergence in sympatry may have been facilitated by genetic variants that evolved during a time of isolation between an initial founding population and a secondary wave of colonizers stemming from the same source population. This highlights the limitations in the definitions of sympatric speciation when the mosaic nature of genomes is taken into account: some of the genetic regions driving divergence may have evolved in allopatry while the populations themselves diverged in sympatry.

Microsatellite genotyping is a common DNA characterization technique in population, ecological and evolutionary genetics research. Since different alleles are sized relative to internal size-standards, different laboratories must calibrate and standardize allelic designations when exchanging data. This interchange of microsatellite data can often prove problematic. Here, 16 microsatellite loci were calibrated and standardized for the Atlantic salmon, Salmo salar, across 12 laboratories. Although inconsistencies were observed, particularly due to differences between migration of DNA fragments and actual allelic size (‘size shifts’), inter-laboratory calibration was successful. Standardization also allowed an assessment of the degree and partitioning of genotyping error. Notably, the global allelic error rate was reduced from 0.05 ± 0.01 prior to calibration to 0.01 ± 0.002 post-calibration. Most errors were found to occur during analysis (i.e. when size-calling alleles; the mean proportion of all errors that were analytical errors across loci was 0.58 after calibration). No evidence was found of an association between the degree of error and allelic size range of a locus, number of alleles, nor repeat type, nor was there evidence that genotyping errors were more prevalent when a laboratory analyzed samples outside of the usual geographic area they encounter. The microsatellite calibration between laboratories presented here will be especially important for genetic assignment of marine-caught Atlantic salmon, enabling analysis of marine mortality, a major factor in the observed declines of this highly valued species.