Gregory L. Owens

Hybridization and extinction

Hybridization may drive rare taxa to extinction through genetic swamping, where the rare form is replaced by hybrids, or by demographic swamping, where population growth rates are reduced due to the wasteful production of maladaptive hybrids. Conversely, hybridization may rescue the viability of small, inbred populations. Understanding the factors that contribute to destructive versus constructive outcomes of hybridization is key to managing conservation concerns. Here, we survey the literature for studies of hybridization and extinction to identify the ecological, evolutionary, and genetic factors that critically affect extinction risk through hybridization. We find that while extinction risk is highly situation dependent, genetic swamping is much more frequent than demographic swamping. In addition, human involvement is associated with increased risk and high reproductive isolation with reduced risk. Although climate change is predicted to increase the risk of hybridization‐induced extinction, we find little empirical support for this prediction. Similarly, theoretical and experimental studies imply that genetic rescue through hybridization may be equally or more probable than demographic swamping, but our literature survey failed to support this claim. We conclude that halting the introduction of hybridization‐prone exotics and restoring mature and diverse habitats that are resistant to hybrid establishment should be management priorities.

Shared selective pressure and local genomic landscape lead to repeatable patterns of genomic divergence in sunflowers

The repeated evolution of traits in organisms facing similar environmental conditions is considered to be fundamental evidence for the role of natural selection in moulding phenotypes. Yet, aside from case studies of parallel evolution and its genetic basis, the repeatability of evolution at the level of the whole genome remains poorly characterized. Here, through the use of transcriptome sequencing, we examined genomic divergence for three pairs of sister species of sunflowers. Two of the pairs (Helianthus petiolaris – H. debilis and H. annuus – H. argophyllus) have diverged along a similar latitudinal gradient and presumably experienced similar selective pressure. In contrast, a third species pair (H. exilis – H. bolanderi) diverged along a longitudinal gradient. Analyses of divergence, as measured in terms of FST, indicated little repeatability across the three pairs of species for individual genetic markers (SNPs), modest repeatability at the level of individual genes and the highest repeatability when large regions of the genome were compared. As expected, higher repeatability was observed for the two species pairs that have diverged along a similar latitudinal gradient, with genes involved in flowering time among the most divergent genes. Genes showing extreme low or high differentiation were more similar than genes showing medium levels of divergence, implying that both purifying and divergent selection contributed to repeatable patterns of divergence. The location of a gene along the chromosome also predicted divergence levels, presumably because of shared heterogeneity in both recombination and mutation rates. In conclusion, repeated genome evolution appeared to result from both similar selective pressures and shared local genomic landscapes.

Parallel Ecological Speciation in Plants

Populations that have independently evolved reproductive isolation from their ancestors while remaining reproductively cohesive have undergone parallel speciation. A specific type of parallel speciation, known as parallel ecological speciation, is one of several forms of evidence for ecologys role in speciation. In this paper we search the literature for candidate examples of parallel ecological speciation in plants. We use four explicit criteria (independence, isolation, compatibility, and selection) to judge the strength of evidence for each potential case. We find that evidence for parallel ecological speciation in plants is unexpectedly scarce, especially relative to the many well-characterized systems in animals. This does not imply that ecological speciation is uncommon in plants. It only implies that evidence from parallel ecological speciation is rare. Potential explanations for the lack of convincing examples include a lack of rigorous testing and the possibility that plants are less prone to parallel ecological speciation than animals.

Recurrent selection explains parallel evolution of genomic regions of high relative but low absolute differentiation in a ring species

Recent technological developments allow investigation of the repeatability of evolution at the genomic level. Such investigation is particularly powerful when applied to a ring species, in which spatial variation represents changes during the evolution of two species from one. We examined genomic variation among three subspecies of the greenish warbler ring species, using genotypes at 13 013 950 nucleotide sites along a new greenish warbler consensus genome assembly. Genomic regions of low within‐group variation are remarkably consistent between the three populations. These regions show high relative differentiation but low absolute differentiation between populations. Comparisons with outgroup species show the locations of these peaks of relative differentiation are not well explained by phylogenetically conserved variation in recombination rates or selection. These patterns are consistent with a model in which selection in an ancestral form has reduced variation at some parts of the genome, and those same regions experience recurrent selection that subsequently reduces variation within each subspecies. The degree of heterogeneity in nucleotide diversity is greater than explained by models of background selection, but is consistent with selective sweeps. Given the evidence that greenish warblers have had both population differentiation for a long period of time and periods of gene flow between those populations, we propose that some genomic regions underwent selective sweeps over a broad geographic area followed by within‐population selection‐induced reductions in variation. An important implication of this ‘sweep‐before‐differentiation’ model is that genomic regions of high relative differentiation may have moved among populations more recently than other genomic regions.

Gene flow and selection interact to promote adaptive divergence in regions of low recombination

Adaptation to new environments often occurs in the face of gene flow. Under these conditions, gene flow and recombination can impede adaptation by breaking down linkage disequilibrium between locally adapted alleles. Theory predicts that this decay can be halted or slowed if adaptive alleles are tightly linked in regions of low recombination, potentially favouring divergence and adaptive evolution in these regions over others. Here, we compiled a global genomic data set of over 1,300 individual threespine stickleback from 52 populations and compared the tendency for adaptive alleles to occur in regions of low recombination between populations that diverged with or without gene flow. In support of theory, we found that putatively adaptive alleles (FST and dXY outliers) tend to occur more often in regions of low recombination in populations where divergent selection and gene flow have jointly occurred. This result remained significant when we employed different genomic window sizes, controlled for the effects of mutation rate and gene density, controlled for overall genetic differentiation, varied the genetic map used to estimate recombination and used a continuous (rather than discrete) measure of geographic distance as proxy for gene flow/shared ancestry. We argue that our study provides the first statistical evidence that the interaction of gene flow and selection biases divergence toward regions of low recombination.

Rapid adaptive evolution of colour vision in the threespine stickleback radiation.

Vision is a sensory modality of fundamental importance for many animals, aiding in foraging, detection of predators and mate choice. Adaptation to local ambient light conditions is thought to be commonplace, and a match between spectral sensitivity and light spectrum is predicted. We use opsin gene expression to test for local adaptation and matching of spectral sensitivity in multiple independent lake populations of threespine stickleback populations derived since the last ice age from an ancestral marine form. We show that sensitivity across the visual spectrum is shifted repeatedly towards longer wavelengths in freshwater compared with the ancestral marine form. Laboratory rearing suggests that this shift is largely genetically based. Using a new metric, we found that the magnitude of shift in spectral sensitivity in each population corresponds strongly to the transition in the availability of different wavelengths of light between the marine and lake environments. We also found evidence of local adaptation by sympatric benthic and limnetic ecotypes to different light environments within lakes. Our findings indicate rapid parallel evolution of the visual system to altered light conditions. The changes have not, however, yielded a close matching of spectrum-wide sensitivity to wavelength availability, for reasons we discuss.

Revisiting a classic case of introgression: hybridization and gene flow in Californian sunflowers.

During invasion, colonizing species can hybridize with native species, potentially swamping out native genomes. However, theory predicts that introgression will often be biased into the invading species. Thus, empirical estimates of gene flow between native and invasive species are important to quantify the actual threat of hybridization with invasive species. One classic example of introgression occurs in California, where Helianthus bolanderi was thought to be a hybrid between the serpentine endemic Helianthus exilis and the congeneric invader Helianthus annuus. We used genotyping by sequencing to look for signals of introgression and population structure. We find that H. bolanderi and H. exilis form one genetic clade, with weak population structure that is associated with geographic location rather than soil composition and likely represent a single species, not two. Additionally, while our results confirmed early molecular analysis and failed to support the hybrid origin of H. bolanderi, we did find evidence for introgression mainly into the invader H. annuus, as predicted by theory.

HYBRID INCOMPATIBILITY IS ACQUIRED FASTER IN ANNUAL THAN IN PERENNIAL SPECIES OF SUNFLOWER AND TARWEED

Hybrid sterility is an important species barrier, especially in plants where hybrids can often form between divergent taxa. Here we explore how life history affects the acquisition of hybrid sterility in two groups in the sunflower family. We analyzed genetic distance and F1 pollen sterility for interspecific crosses in annual and perennial groups. We find that reproductive isolation is acquired in a steady manner and that annual species acquire hybrid sterility barriers faster than perennial species. Potential causes of the observed sterility pattern are discussed.

Genome-wide genotyping-by-sequencing data provide a high-resolution view of wild Helianthus diversity, genetic structure, and interspecies gene flow

PREMISE Wild sunflowers harbor considerable genetic diversity and are a major resource for improvement of the cultivated sunflower, Helianthus annuus. The Helianthus genus is also well known for its propensity for gene flow between taxa. METHODS We surveyed genomic diversity of 292 samples of wild Helianthus from 22 taxa that are cross-compatible with the cultivar using genotyping by sequencing. With these data, we derived a high-resolution phylogeny of the taxa, interrogated genome-wide levels of diversity, explored H. annuus population structure, and identified localized gene flow between H. annuus and its close relatives. KEY RESULTS Our phylogenomic analyses confirmed a number of previously established interspecific relationships and indicated for the first time that a newly described annual sunflower, H. winteri, is nested within H. annuus. Principal component analyses showed that H. annuus has geographic population structure with most notable subpopulations occurring in California and Texas. While gene flow was identified between H. annuus and H. bolanderi in California and between H. annuus and H. argophyllus in Texas, this genetic exchange does not appear to drive observed patterns of H. annuus population structure. CONCLUSIONS Wild H. annuus remains an excellent resource for cultivated sunflower breeding effort because of its diversity and the ease with which it can be crossed with cultivated H. annuus. Cases of interspecific gene flow such as those documented here also indicate wild H. annuus can act as a bridge to capture alleles from other wild taxa; continued breeding efforts with it may therefore reap the largest rewards.

A novel post hoc method for detecting index switching finds no evidence for increased switching on the Illumina HiSeq X

High‐throughput sequencing using the Illumina HiSeq platform is a pervasive and critical molecular ecology resource, and has provided the data underlying many recent advances. A recent study has suggested that “index switching,” where reads are misattributed to the wrong sample, may be higher in new versions of the HiSeq platform. This has the potential to invalidate both published and in‐progress work across the field. Here, we test for evidence of index switching in an exemplar whole‐genome shotgun data set sequenced on both the Illumina HiSeq 2500, which should not have the problem, and the Illumina HiSeq X, which may. We leverage unbalanced heterozygotes, which may be produced by index switching, and ask whether the undersequenced allele is more likely to be found in other samples in the same lane than expected based on the allele frequency. Although we validate the sensitivity of this method using simulations, we find that neither the HiSeq 2500 nor the HiSeq X has evidence of index switching. This suggests that, thankfully, index switching may not be a ubiquitous problem in HiSeq X sequence data. Lastly, we provide scripts for applying our method so that index switching can be tested for in other data sets.