Speciation genomic studies aim to interpret patterns of genome-wide variation in light of the processes that give rise to new species. However, interpreting the genomic “landscape” of speciation is difficult, because many evolutionary processes can impact levels of variation. Facilitated by the first chromosome-level assembly for the group, we use whole-genome sequencing and simulations to shed light on the processes that have shaped the genomic landscape during a radiation of monkeyflowers. After inferring the phylogenetic relationships among the 9 taxa in this radiation, we show that highly similar diversity (π) and differentiation ( F ST ) landscapes have emerged across the group. Variation in these landscapes was strongly predicted by the local density of functional elements and the recombination rate, suggesting that the landscapes have been shaped by widespread natural selection. Using the varying divergence times between pairs of taxa, we show that the correlations between F ST and genome features arose almost immediately after a population split and have become stronger over time. Simulations of genomic landscape evolution suggest that background selection (BGS; i.e., selection against deleterious mutations) alone is too subtle to generate the observed patterns, but scenarios that involve positive selection and genetic incompatibilities are plausible alternative explanations. Finally, tests for introgression among these taxa reveal widespread evidence of heterogeneous selection against gene flow during this radiation. Combined with previous evidence for adaptation in this system, we conclude that the correlation in F ST among these taxa informs us about the processes contributing to adaptation and speciation during a rapid radiation.

BackgroundEvolutionary origins of derived morphologies ultimately stem from changes in protein structure, gene regulation, and gene content. A well-assembled, annotated reference genome is a central resource for pursuing these molecular phenomena underlying phenotypic evolution. We explored the genome of the Gulf pipefish (Syngnathus scovelli), which belongs to family Syngnathidae (pipefishes, seahorses, and seadragons). These fishes have dramatically derived bodies and a remarkable novelty among vertebrates, the male brood pouch.ResultsWe produce a reference genome, condensed into chromosomes, for the Gulf pipefish. Gene losses and other changes have occurred in pipefish hox and dlx clusters and in the tbx and pitx gene families, candidate mechanisms for the evolution of syngnathid traits, including an elongated axis and the loss of ribs, pelvic fins, and teeth. We measure gene expression changes in pregnant versus non-pregnant brood pouch tissue and characterize the genomic organization of duplicated metalloprotease genes (patristacins) recruited into the function of this novel structure. Phylogenetic inference using ultraconserved sequences provides an alternative hypothesis for the relationship between orders Syngnathiformes and Scombriformes. Comparisons of chromosome structure among percomorphs show that chromosome number in a pipefish ancestor became reduced via chromosomal fusions.ConclusionsThe collected findings from this first syngnathid reference genome open a window into the genomic underpinnings of highly derived morphologies, demonstrating that de novo production of high quality and useful reference genomes is within reach of even small research groups.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-1126-6) contains supplementary material, which is available to authorized users.

Speciation genomic studies aim to interpret patterns of genome-wide variation in light of the processes that give rise to new species. However, interpreting the genomic ‘landscape’ of speciation is difficult, because many evolutionary processes can impact levels of variation. Facilitated by the first chromosome-level assembly for the group, we use whole-genome sequencing and simulations to shed light on the processes that have shaped the genomic landscape during a recent radiation of monkeyflowers. After inferring the phylogenetic relationships among the nine taxa in this radiation, we show that highly similar diversity (π) and differentiation (FST) landscapes have emerged across the group. Variation in these landscapes was strongly predicted by the local density of functional elements and the recombination rate, suggesting that the landscapes have been shaped by widespread natural selection. Using the varying divergence times between pairs of taxa, we show that the correlations between FST and genome features arose almost immediately after a population split and have become stronger over time. Simulations of genomic landscape evolution suggest that background selection (i.e., selection against deleterious mutations) alone is too subtle to generate the observed patterns, but scenarios that involve positive selection and genetic incompatibilities are plausible alternative explanations. Finally, tests for introgression among these taxa reveal widespread evidence of heterogeneous selection against gene flow during this radiation. Thus, combined with existing evidence for adaptation in this system, we conclude that the correlation in FST among these taxa informs us about the genomic basis of adaptation and speciation in this system.Author summaryWhat can patterns of genome-wide variation tell us about the speciation process? The answer to this question depends upon our ability to infer the evolutionary processes underlying these patterns. This, however, is difficult, because many processes can leave similar footprints, but some have nothing to do with speciation per se. For example, many studies have found highly heterogeneous levels of genetic differentiation when comparing the genomes of emerging species. These patterns are often referred to as differentiation ‘landscapes’ because they appear as a rugged topography of ‘peaks’ and ‘valleys’ as one scans across the genome. It has often been argued that selection against deleterious mutations, a process referred to as background selection, is primarily responsible for shaping differentiation landscapes early in speciation. If this hypothesis is correct, then it is unlikely that patterns of differentiation will reveal much about the genomic basis of speciation. However, using genome sequences from nine emerging species of monkeyflower coupled with simulations of genomic divergence, we show that it is unlikely that background selection is the primary architect of these landscapes. Rather, differentiation landscapes have probably been shaped by adaptation and gene flow, which are processes that are central to our understanding of speciation. Therefore, our work has important implications for our understanding of what patterns of differentiation can tell us about the genetic basis of adaptation and speciation.

The structure of the caudal skeleton of extant teleost fishes has been interpreted in two different ways. In a diural interpretation, a caudal skeleton is composed of two centra articulated with one to six hypurals. Most subsequent authors have followed this interpretation. In contrast, a polyural interpretation considers the teleost fin to be derived from a fully metameristic ancestral bauplan originally composed of a one-to-one relationship between neural arches, centra (when present), and hypurals. Three different interpretations of the identity and homology of skeletal components of the caudal skeleton of the teleost fish Danio rerio have been proposed, two from a diural perspective and one from a polyural perspective. We examine each caudal skeletal component of Danio rerio from both a developmental and phylogenetic perspective. We propose that a polyural interpretation of structures is consistent with the current interpretation of the basal neopterygian caudal fin for this model organism rather than the older diural interpretation that does not take into account the metamerism observed in caudal structures during development. The polyural interpretation suggests several shared evolutionary innovations of major clades that would remain undiscovered under the older diural naming paradigm and makes the terminology of the parts of the caudal fin of Danio rerio strictly comparable to more basal fishes.