Rapid hybrid speciation in Darwin's finches: Galapagos finches have driven hypotheses of how speciation occurs. Most commonly, it is assumed that natural selection separates species originating from a single population on the basis of variation in traits that confer advantages for survival and reproduction. Lamichhaney et al. document a case where cross-species hybridization established a reproductively isolated lineage, which demonstrates a process known as homoploid hybrid speciation in action (see the Perspective by Wagner). The authors used genetic markers and phenotypic analyses to create a pedigree that revealed how a cross-island migrant bred with a native species to form a self-perpetuating hybrid population that was reproductively isolated from both parental species. Science , this issue p. 224 ; see also p. 157

Ecological adaptation is of major relevance to speciation and sustainable population management, but the underlying genetic factors are typically hard to study in natural populations due to genetic differentiation caused by natural selection being confounded with genetic drift in subdivided populations. Here, we use whole genome population sequencing of Atlantic and Baltic herring to reveal the underlying genetic architecture at an unprecedented detailed resolution for both adaptation to a new niche environment and timing of reproduction. We identify almost 500 independent loci associated with a recent niche expansion from marine (Atlantic Ocean) to brackish waters (Baltic Sea), and more than 100 independent loci showing genetic differentiation between spring- and autumn-spawning populations irrespective of geographic origin. Our results show that both coding and non-coding changes contribute to adaptation. Haplotype blocks, often spanning multiple genes and maintained by selection, are associated with genetic differentiation.

The Atlantic herring is one of the most abundant vertebrates on earth but its nucleotide diversity is moderate (π = 0.3%), only three-fold higher than in human. Here, we present a pedigree-based estimation of the mutation rate in this species. Based on whole-genome sequencing of four parents and 12 offspring, the estimated mutation rate is 2.0 × 10^-9 per base per generation. We observed a high degree of parental mosaicism indicating that a large fraction of these de novo mutations occurred during early germ cell development. The estimated mutation rate – the lowest among vertebrates analyzed to date – partially explains the discrepancy between the rather low nucleotide diversity in herring and its huge census population size. But a species like the herring will never reach its expected nucleotide diversity because of fluctuations in population size over the millions of years it takes to build up high nucleotide diversity.

Recent adaptive radiations are models for investigating mechanisms contributing to the evolution of biodiversity. An unresolved question is the relative importance of new mutations, ancestral variants, and introgressive hybridization for phenotypic evolution and speciation. Here, we address this issue using Darwin’s finches and investigate the genomic architecture underlying their phenotypic diversity. Admixture mapping for beak and body size in the small, medium, and large ground finches revealed 28 loci showing strong genetic differentiation. These loci represent ancestral haplotype blocks with origins predating speciation events during the Darwin’s finch radiation. Genes expressed in the developing beak are overrepresented in these genomic regions. Ancestral haplotypes constitute genetic modules for selection and act as key determinants of the unusual phenotypic diversity of Darwin’s finches. Such ancestral haplotype blocks can be critical for how species adapt to environmental variability and change.

Evolutionary convergence has been long considered primary evidence of adaptation driven by natural selection and provides opportunities to explore evolutionary repeatability and predictability. In recent years, there has been increased interest in exploring the genetic mechanisms underlying convergent evolution, in part, owing to the advent of genomic techniques. However, the current ‘genomics gold rush’ in studies of convergence has overshadowed the reality that most trait classifications are quite broadly defined, resulting in incomplete or potentially biased interpretations of results. Genomic studies of convergence would be greatly improved by integrating deep ‘vertical’, natural history knowledge with ‘horizontal’ knowledge focusing on the breadth of taxonomic diversity. Natural history collections have and continue to be best positioned for increasing our comprehensive understanding of phenotypic diversity, with modern practices of digitization and databasing of morphological traits providing exciting improvements in our ability to evaluate the degree of morphological convergence. Combining more detailed phenotypic data with the well-established field of genomics will enable scientists to make progress on an important goal in biology: to understand the degree to which genetic or molecular convergence is associated with phenotypic convergence. Although the fields of comparative biology or comparative genomics alone can separately reveal important insights into convergent evolution, here we suggest that the synergistic and complementary roles of natural history collection-derived phenomic data and comparative genomics methods can be particularly powerful in together elucidating the genomic basis of convergent evolution among higher taxa. This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions’.

Significance: The mechanisms by which genomes become smaller in lineages with large genomes, such as many frogs, are poorly understood. Here, we present the sequence of a very small genome from a frog—that of the ornate burrowing frog, Platyplectrum ornatum , whose genome is smaller than that of many birds, a group well known for small genomes. Our data show that this frog evolved molecular mechanisms to keep in check a major process characterizing large genomes: namely, proliferation of transposable elements. We also present basic data on gene expression and sex determination in this emerging model for genome miniaturization.