The temporal and genomic scale of selection following hybridization.

Genomic evidence supports an important role for selection in shaping patterns of introgression along the genome, but frameworks for understanding the evolutionary dynamics within hybrid populations that underlie these patterns have been lacking. Due to the clock-like effect of recombination in hybrids breaking up parental haplotypes, drift and selection produce predictable patterns of ancestry variation at varying spatial genomic scales through time. Here, we develop methods based on the Discrete Wavelet Transform to study the genomic scale of local ancestry variation and its association with recombination rates and show that these methods capture temporal dynamics of drift and genome-wide selection after hybridization. We apply these methods to published datasets from hybrid populations of swordtail fish (Xiphophorus) and baboons (Papio) and to inferred Neanderthal introgression in modern humans. Across systems, upward of 20% of variation in local ancestry at the broadest genomic scales can be attributed to systematic selection against introgressed alleles, consistent with strong selection acting on early-generation hybrids. Signatures of selection at fine genomic scales suggest selection over longer time scales; however, we suggest that our ability to confidently infer selection at fine scales is likely limited by inherent biases in current methods for estimating local ancestry from contiguous segments of genomic similarity. Wavelet approaches will become widely applicable as genomic data from systems with introgression become increasingly available and can help shed light on generalities of the genomic consequences of interspecific hybridization.

Distinct ancient structural polymorphisms control heterodichogamy in walnuts and hickories.

The maintenance of stable mating type polymorphisms is a classic example of balancing selection, underlying the nearly ubiquitous 50/50 sex ratio in species with separate sexes. One lesser known but intriguing example of a balanced mating polymorphism in angiosperms is heterodichogamy - polymorphism for opposing directions of dichogamy (temporal separation of male and female function in hermaphrodites) within a flowering season. This mating system is common throughout Juglandaceae, the family that includes globally important and iconic nut and timber crops - walnuts (Juglans), as well as pecan and other hickories (Carya). In both genera, heterodichogamy is controlled by a single dominant allele. We fine-map the locus in each genus, and find two ancient (>50 Mya) structural variants involving different genes that both segregate as genus-wide trans-species polymorphisms. The Juglans locus maps to a ca. 20 kb structural variant adjacent to a probable trehalose phosphate phosphatase (TPPD-1), homologs of which regulate floral development in model systems. TPPD-1 is differentially expressed between morphs in developing male flowers, with increased allele-specific expression of the dominant haplotype copy. Across species, the dominant haplotype contains a tandem array of duplicated sequence motifs, part of which is an inverted copy of the TPPD-1 3' UTR. These repeats generate various distinct small RNAs matching sequences within the 3' UTR and further downstream. In contrast to the single-gene Juglans locus, the Carya heterodichogamy locus maps to a ca. 200-450 kb cluster of tightly linked polymorphisms across 20 genes, some of which have known roles in flowering and are differentially expressed between morphs in developing flowers. The dominant haplotype in pecan, which is nearly always heterozygous and appears to rarely recombine, shows markedly reduced genetic diversity and is over twice as long as its recessive counterpart due to accumulation of various types of transposable elements. We did not detect either genetic system in other heterodichogamous genera within Juglandaceae, suggesting that additional genetic systems for heterodichogamy may yet remain undiscovered.

Uncovering the genetic architecture of parallel evolution.

Identifying the genetic architecture underlying adaptive traits is exceptionally challenging in natural populations. This is because associations between traits not only mask the targets of selection but also create correlated patterns of genomic divergence that hinder our ability to isolate causal genetic effects. Here, we examine the repeated evolution of components of the auxin pathway that have contributed to the replicated loss of gravitropism (i.e. the ability of a plant to bend in response to gravity) in multiple populations of the Senecio lautus species complex in Australia. We use a powerful approach which combines parallel population genomics with association mapping in a Multiparent Advanced Generation Inter-Cross (MAGIC) population to break down genetic and trait correlations to reveal how adaptive traits evolve during replicated evolution. We sequenced auxin and shoot gravitropism-related gene regions in 80 individuals from six natural populations (three parallel divergence events) and 133 individuals from a MAGIC population derived from two of the recently diverged natural populations. We show that artificial tail selection on gravitropism in the MAGIC population recreates patterns of parallel divergence in the auxin pathway in the natural populations. We reveal a set of 55 auxin gene regions that have evolved repeatedly during the evolution of the species, of which 50 are directly associated with gravitropism divergence in the MAGIC population. Our work creates a strong link between patterns of genomic divergence and trait variation contributing to replicated evolution by natural selection, paving the way to understand the origin and maintenance of adaptations in natural populations.

Species divergence under competition and shared predation.

Species competing for resources also commonly share predators. While competition often drives divergence between species, the effects of shared predation are less understood. Theoretically, competing prey species could either diverge or evolve in the same direction under shared predation depending on the strength and symmetry of their interactions. We took an empirical approach to this question, comparing antipredator and trophic phenotypes between sympatric and allopatric populations of threespine stickleback and prickly sculpin fish that all live in the presence of a trout predator. We found divergence in antipredator traits between the species: in sympatry, antipredator adaptations were relatively increased in stickleback but decreased in sculpin. Shifts in feeding morphology, diet and habitat use were also divergent but driven primarily by stickleback evolution. Our results suggest that asymmetric ecological character displacement indirectly made stickleback more and sculpin less vulnerable to shared predation, driving divergence of antipredator traits between sympatric species.

Genome evolution is surprisingly predictable after initial hybridization.

Over the past two decades, evolutionary biologists have come to appreciate that hybridization, or genetic exchange between distinct lineages, is remarkably common - not just in particular lineages but in taxonomic groups across the tree of life. As a result, the genomes of many modern species harbor regions inherited from related species. This observation has raised fundamental questions about the degree to which the genomic outcomes of hybridization are repeatable and the degree to which natural selection drives such repeatability. However, a lack of appropriate systems to answer these questions has limited empirical progress in this area. Here, we leverage independently formed hybrid populations between the swordtail fish Xiphophorus birchmanni and X. cortezi to address this fundamental question. We find that local ancestry in one hybrid population is remarkably predictive of local ancestry in another, demographically independent hybrid population. Applying newly developed methods, we can attribute much of this repeatability to strong selection in the earliest generations after initial hybridization. We complement these analyses with time-series data that demonstrates that ancestry at regions under selection has remained stable over the past ~40 generations of evolution. Finally, we compare our results to the well-studied X. birchmanni×X. malinche hybrid populations and conclude that deeper evolutionary divergence has resulted in stronger selection and higher repeatability in patterns of local ancestry in hybrids between X. birchmanni and X. cortezi.

Highly Replicated Evolution of Parapatric Ecotypes.

Parallel evolution of ecotypes occurs when selection independently drives the evolution of similar traits across similar environments. The multiple origins of ecotypes are often inferred based on a phylogeny that clusters populations according to geographic location and not by the environment they occupy. However, the use of phylogenies to infer parallel evolution in closely related populations is problematic because gene flow and incomplete lineage sorting can uncouple the genetic structure at neutral markers from the colonization history of populations. Here, we demonstrate multiple origins within ecotypes of an Australian wildflower, Senecio lautus. We observed strong genetic structure as well as phylogenetic clustering by geography and show that this is unlikely due to gene flow between parapatric ecotypes, which was surprisingly low. We further confirm this analytically by demonstrating that phylogenetic distortion due to gene flow often requires higher levels of migration than those observed in S. lautus. Our results imply that selection can repeatedly create similar phenotypes despite the perceived homogenizing effects of gene flow.

On the origin of orphan hybrids between Aquilegia formosa and Aquilegia flavescens.

We report the investigation of an Aquilegia flavescens × A. formosa population in British Columbia that is disjunct from its parents-the latter species is present locally but ecologically separated, while the former is entirely absent. To confirm hybridity, we used multivariate analysis of floral characters of field-sampled populations to ordinate phenotypes of putative hybrids in relation to those of the parental species. Microsatellite genotypes at 11 loci from 72 parental-type and putative hybrid individuals were analysed to assess evidence for admixture. Maternally inherited plastid sequences were analysed to infer the direction of hybridization and test hypotheses on the origin of the orphan hybrid population. Plants from the orphan hybrid population are on average intermediate between typical A. formosa and A. flavescens for most phenotypes examined and show evidence of genetic admixture. This population lies beyond the range of A. flavescens, but within the range of A. formosa. No pure A. flavescens individuals were observed in the vicinity, nor is this species known to occur within 200 km of the site. The hybrids share a plastid haplotype with local A. formosa populations. Alternative explanations for this pattern are evaluated. While we cannot rule out long-distance pollen dispersal followed by proliferation of hybrid genotypes, we consider the spread of an A. formosa plastid during genetic swamping of a historical A. flavescens population to be more parsimonious.