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Hopkins, R.

Publications and source records attributed to Hopkins, R..

At least 19 recordsLinked to original sources

Estimating self-fertilization rates from the diploid genotype spectrum

The distribution of self-fertilization across the tree of life remains poorly characterized. Here we present the diploid genotype spectrum (DGS) as a useful genomic data summary for characterizing populations undergoing partial self-fertilization (selfing). This statistic provides a straightforward baseline for estimating selfing rates from population genomic data. At every segregating site across a genome, the diploid genotype configuration records the numbers of homozygous ancestral, heterozygous, and homozygous derived individuals, and the DGS compiles the counts of these configurations across sites. We show that the expected relative frequencies of DGS configurations among segregating sites can be computed under the standard coalescent approximation for partial selfing. We present two methods for doing this, one that is an intuitive recursion through possible states of the model, and one that is a more efficient combinatorial version. We give a worked example, validate the analytical expectations using forward simulations, and introduce a software package that estimates population selfing rates from diploid SNP data. The computations here mechanistically link selfing to observed patterns of diploid genotype configurations.

genomics↗

Unmasking the large and highly repetitive genome of Phlox reveals a complex evolutionary history of speciation with gene flow

The large size and high repetitive content of many plant genomes have hindered elucidation of how the fundamental processes of evolution give rise to speciation. Here we present chromosome-level assemblies of 6 gigabase genomes for four closely related Phlox wildflower species. We generate extensive population genetic data for the three well-studied annual species P. drummondii, P. cuspidata, and P. roemeriana, including structural variation from whole-genome long-read resequencing data. The whole-genome assemblies reveal extensive differences in amount and distribution of genetic variation within and between species, reflective of differences in life-history strategies, mating systems, and edaphic specialization. The population genetic data exposes a history of widespread and consistent gene flow between all three annual Phlox species throughout their divergence and speciation. Our unmasking of structural variants and repetitive elements exposes rich and dynamic forms of genetic variation that show strong phylogenetic signal and pervasive patterns of gene flow. Our results lay a foundation for untangling the highly complex genomes of plants to make advancements in our understanding of the processes of speciation and divergence.

evolutionary biology↗

A lectin receptor-like kinase controls self-pollen recognition in Phlox (Polemoniaceae)

Self-incompatibility (SI) describes a widespread collection of genetic mechanisms in flowering plants used to specifically recognize and reject self-pollen. These mechanisms are fundamental to plant sexual reproduction and offer valuable insight into the molecular basis of cell-cell communication and self-recognition more broadly. Here, we leverage an independent evolution of SI in the lineage containing Phlox (Polemoniaceae) to characterize a novel gene causing self-pollen recognition which we name Phlox drummondii Pistil Identity Receptor Kinase (PdPIRK). Recognition of self-pollen associates with a single genomic region containing the Phlox S-locus. We generate predictions regarding how S-loci must function and evolve to identify a single candidate gene within this S-associated region. This gene, PdPIRK, is highly and specifically expressed in the pistil and has exceptionally high polymorphism maintained by negative frequency dependent selection, two hallmarks of self-pollen recognition genes. Functional validation with gene silencing confirms that PdPIRK is necessary for self-incompatibility, and we further demonstrate allele specific activity, confirming its role in self-pollen recognition per se. PdPIRK encodes a G-type lectin receptor-like kinase, which is a member of the same gene family as SRK, the gene controlling self-pollen recognition in the distantly related Brassicaceae. Our findings suggest the presence of genetic constraints or paths of least resistance governing how S-loci evolve and add to our understanding of the diverse molecular mechanisms through which organisms achieve self-recognition.

plant biology↗

Variation in response to water availability across Phlox species

Plants adapt to environmental variation both by evolving divergent trait means and by plastically adjusting trait expression in response to local conditions. While these dual strategies are essential for persistence in diverse environments, how they interact and vary across closely related species is understudied. For plants, water availability is a particularly important selective force that shapes species distributions, selects for growth habit and life history strategy, and can dictate individuals plastic expressions of trait values and reproductive success. Here, we use ecological niche modeling, field soil collections, and a controlled drought experiment to test how biogeography and evolutionary history influence responses to limited water availability in three closely related Texas annual Phlox species and their F1 hybrids. We infer that the species occupy distinct niches that diverge along a primary axis of water availably and soil moisture. Each species has a distinct vegetative growth habit that does not match broad predictions of divergence in response to water availability. Nevertheless, we find that all the species show a significant morphological response to controlled soil dry down with reduced biomass, smaller leaves, and fewer flowers, as would be predicted in a response to drought. We find that Phlox drummondii, which occupies intermediate habitats, exhibits the strongest plastic response to water limitation, despite it not having the broadest environmental niche. Additionally, most hybrids involving P. drummondii display intermediate phenotypes in both wet and dry treatments, while hybrids between P. cuspidata and P. roemeriana show phenotypes consistent with hybrid vigor. These results challenge the hypothesis that species from broader environments evolve greater plasticity. Instead, the most plastic species did not have the broadest niche, suggesting plasticity and niche breadth may evolve independently.

evolutionary biology↗

The genetic architecture of quantitative variation in the self-incompatibility response within Phlox drummondii (Polemoniaceae)

Flowering plants display extensive variation in selfing rate, a trait with significant ecological and evolutionary consequences. Many species use genetic mechanisms to recognize and reject self-pollen (termed self-incompatibility or SI), and the loss of SI is one of the most common evolutionary transitions among flowering plants. Despite the ubiquity of transitions to self-compatibility (SC), little is known about the genetic architecture through which SC evolves. Specifically, it is important to determine if SC has a polygenic or simple genetic basis and if variation in compatibility localizes to the genomic locus causing self-pollen recognition (the "S-locus"). Phlox drummondii (Polemoniaceae) has been a model system for exploring mating system evolution and expresses extensive range-wide variation in the SI response. Here we investigate the genetic architecture of SC variants segregating within this otherwise SI species. Using multiple independent crosses, we uncover numerous QTLs associated with intraspecific variation in SI, consistent with a polygenic genetic architecture. While some QTLs overlap across mapping experiments, other QTLs are unique, suggesting that multiple genetic routes to SC exist. Through these crossing experiments, we demonstrate that P. drummondii has a sporophytic SI system, suggesting that an independent evolution of SI occurred in the lineage containing Phlox. We map this novel S-locus and find that the genomic region containing the S-locus is associated with intraspecific variation in SI in one of the three mapping populations. Although further work is necessary to clarify the conditions under which quantitative variation in SI represents a transitional pathway to complete SC, our study reveals the underlying genetic architecture upon which selection could act to drive this frequent and evolutionarily significant transition.

plant biology↗

High-throughput iNaturalist image analysis reveals flower color divergence in Monarda fistulosa

Characterizing patterns of trait variation across widespread species is a fundamental goal of natural history. Here we create a pipeline to analyze a large community science dataset and test hypothesized flower color divergence across the range of a widespread wildflower. Monarda fistulosa is a North American perennial that produces showy lavender inflorescences. Although previous literature suggests that the flowers of western M. fistulosa might display a deeper purple color than the eastern varieties, this divergence has not been assessed at scale. We process over 40,000 community science photographs of M. fistulosa to identify flowers and extract color. We demonstrate that the flowers of the montane western variety have lower lightness and higher chroma, corresponding to a deeper violet color, than those of eastern M. fistulosa. Our approach and validation provides a scalable framework for phenotyping community science images and enables analysis of geographic color variation in other widespread species.

evolutionary biology↗

A Shared Neural Network for Highly Liked and Disliked Music

Music research has increasingly focused on neural responses to naturalistic stimuli. The neural correlates of music-induced peak moments of pleasure (e.g., chills) have been well-studied; data on other types of aesthetic responses, such as judgments of beauty, goodness, or liking are sparse. Among these, liking is of particular interest given its complex nature and its ubiquity in everyday--and musical--experiences. In this functional magnetic resonance imaging (fMRI) study, 26 participants listened to musical excerpts while continuously rating how much they liked the music. In addition, subjects provided an overall liking judgment at the end of each musical piece. Participants musical preferences manifested remarkably early and were sustained over time, with the value of the continuous rating at the end of each piece showing the strongest correlation with the overall ratings. At the neural level, highly liked and disliked musical pieces activated a shared neural network previously associated with the processing of both positive and negative emotional stimuli. This network encompassed the anterior cingulate cortex, limbic system, basal ganglia, and precuneus. These activations reflected individual differences, such that participants with greater trait-level responsiveness to artistic stimuli showed stronger engagement of this network while listening to music. Finally, the default-mode network was associated with the slope of the continuous ratings, suggesting that the faster participants liked a musical excerpt, the more disengaged this network became. In linking behavior and brain function to better characterize the way humans make aesthetic judgments of music the data support a model in which preferences and aesthetic choices are modulated by brain circuits associated with emotion and reward.

neuroscience↗

A massive community-science flower color dataset reveals convergent evolution of delayed flowering phenology in North American red-flowering plants

The radiation of angiosperms is marked by a phenomenal diversity of floral size, shape, color, scent, and reward. Through hundreds of years of documentation and quantification, scientists have sought to make sense of this variation by defining pollination syndromes. These syndromes are the convergent evolution of common suits of floral traits across distantly related species that have evolved by selection to optimize pollination strategies. The availability of community-science datasets provides an opportunity to develop new tools and to examine new traits that may help further characterize broad patterns of flowering plant diversity. Here we test the hypothesis that flowering phenology can also be a pollination syndrome trait. We generate a novel flower color dataset by using GPT-4 with Vision (GPT-4V) to assign flower color to 11,729 North American species. We map these colors to 1,674,908 community-scientist observations of flowering plants to investigate patterns of phenology. We demonstrate constrained flowering time in the eastern United States for plants with red or orange flowers relative to plants with flowers of other colors. Red-and orange-colored flowers are often characteristic of the "hummingbird" pollination syndrome; importantly, the onset of red and orange flowers corresponds to the arrival of migratory hummingbirds. Our results suggest that the hummingbird pollination syndrome can include flowering phenology and reveal an opportunity to expand the suite of traits included in pollination syndromes. Our methods demonstrate an effective pipeline for leveraging enormous amounts of community science data by using artificial intelligence to extract information about patterns of trait variation.

evolutionary biology↗

Mismatch between pollen and pistil size causes asymmetric mechanical reproductive isolation across Phlox species

In flowering plants, pollen-pistil interactions can serve as an important barrier to reproduction between species. As the last barrier to reproduction before fertilization, interactions between these reproductive organs are both complex and important for determining a suitable mate. Here, we test whether differences in style length generate a post-mating prezygotic mechanical barrier between five species of perennial Phlox wildflowers with geographically overlapping distributions. We perform controlled pairwise reciprocal crosses between three species with long styles and two species with short styles to assess crossing success (seed set). We find that heterospecific seed set is broadly reduced compared to conspecific cross success and reveal a striking asymmetry in heterospecific crosses between species with different style lengths. To determine the mechanism underlying this asymmetric reproductive isolating barrier we assess pollen tube growth in vitro and in vivo. We demonstrate that pollen tubes of short-styled species do not grow long enough to reach the ovaries of long-styled species. We find that short-styled species also have smaller pollen and that both within and between species pollen diameter is highly correlated with pollen tube length. Our results support the hypothesis that the small pollen of short-styled species lacks resources to grow pollen tubes long enough to access the ovaries of the long-styled species, resulting in an asymmetrical, mechanical barrier to reproduction. Such mechanisms, combined with additional pollen-pistil incompatibilities, may be particularly important for closely related species in geographic proximity that share pollinators.

evolutionary biology↗

A cis-regulatory point mutation at a R2R3-Myb transcription factor contributes to speciation by reinforcement in Phlox drummondii

The process of reinforcement, whereby selection favors the evolution of increased reproductive trait divergence to reduce costly hybridization between species, has been well documented in nature, yet we know very little about how this process evolves at the molecular level. In this study, we combine functional characterization and genetic association tests to identify the mutational basis of reinforcement in the Texas wildflower Phlox drummondii. P. drummondii evolved from light to dark flower color intensity by selection to stop hybridization with the closely related species P. cuspidata, and previous research suggests differential expression of a R2R3-Myb transcription factor underlies this phenotypic transition. Using gene-silencing experiments, we demonstrate expression of this transcription factor does control variation in flower color intensity. We then apply association mapping across a large genomic region flanking the R2R3-Myb gene and identified a point mutation within the genes promoter that is highly associated with flower color intensity in nature. Alleles at this mutation site match the expected patterns of dominance, create variation in predicted cis-regulatory motifs within the R2R3-Myb proximal promoter, and occur in the direction of evolution predicted for flower color variation in this system. By identifying the mutational basis of reinforcement in this system we demonstrate that, as predicted by theory, reproductive isolation can evolve despite gene flow through a very simple genetic basis.

evolutionary biology↗

A multi-dimensional selective landscape drives adaptive divergence between and within closely related Phlox species

Natural selection shapes diversity across micro and macro-evolutionary scales. Selection causes local adaptation across populations within species and is simultaneously responsible for much of the divergence between species. However, it is unclear if either the force of or the response to selection is the same or different across these scales. Here we show that natural selection drives adaptive divergence between closely related species in a pattern that is distinct from local adaptation within a species. We use reciprocal common-garden transplant experiments across three species of Phlox wildflowers to show widespread adaptive divergence causing species to have highest fitness in their native habitats. Using provenance trials, we also find that one of these Phlox species has strong local adaptation between populations. We compare the axes of divergence and selection between these two scales of diversity and discover that one suite of traits predicts fitness differences between species and that an independent suite of traits predicts fitness variation within species across individuals. Our work reveals how forces of selection can both drive key divergence between species, allowing for and causing speciation, while simultaneously causing extensive diversity that is maintained across populations within a species. The selection landscape is complex and multidimensional

evolutionary biology↗

Genomics highlight an underestimation of the urban heat island effect on red oak phenology

The phenological timing of leaf-out in temperate forests is a critical transition point each year, altering the global climate system via changes to carbon and hydrologic cycles and land-surface albedo. In turn, climate is impacting phenology by advancing leaf-out an average of 2.8 +/-0.35 days per decade as the planet warms. Thus, understanding the relationship between warming and leaf-out is critical for understanding future global change. Rural-to-urban gradients in temperature, which result in clines over which urban areas are up to 4{degrees}C warmer than their surrounding countryside (dubbed the urban heat island - UHI - effect), may be used as a space-for-time substitution in studies of response to climate change. However, studies have recently highlighted that using the UHI effect over space rather than measurements at the same site through time results in consistently weaker relationships between temperature and leaf-out date in spring (i.e., urban-to-rural gradients underpredict the impact of warming on leaf-out). While such studies suggest many potential environmental explanations, the effect of genetic diversity is often neglected. While sensitive to environmental warming, leaf-out phenology is also highly heritable. Given that rural areas are largely natural sites, they likely have higher intraspecific genetic diversity than urban sites, where plants are selected by land managers for a narrow set of resilience traits. Here we measured the environment, genomic background, and phenological timing of northern red oak (Q. rubra) over several years between an urban and rural site to demonstrate how genetic background explains why the UHI effect leads to an underprediction of plant response to warming. Using a space-for-time substitution, we found that the date of leaf-out at our sites is predicted to advance approximately 20 days over the next 80 years. However, if we further account for the genomic background at the two sites, leaf-out, phenology is predicted to advance 22 days; a 10% difference between the two models. We demonstrate that this stronger relationship is because urban trees are largely a monoculture and, moreover, are most closely related to individuals at the rural site that leaf out latest. We highlight the critical need to consider genetic background, particularly in studies examining highly heritable traits, because both environment and genetics are changing across rural-to-urban gradients.

plant biology↗

Phylogenomic patterns of divergence and gene flow detail the evolution of reinforcement and hybrid speciation in Phlox wildflowers

SO_SCPLOWUMMARYC_SCPLOWO_LIThe tree of life is riddled with reticulate evolutionary histories, and some clades, such as the eastern standing Phlox, appear to be hotspots of hybridization. In this group there are two cases of reinforcement and nine hypothesized hybrid species. Given the historical importance of this group for our understanding of plant speciation, the relationships of these taxa and the role of hybridization and gene flow in their diversification require genomic validation. C_LIO_LIUsing phylogenomic analyses, we resolve the evolutionary relationships of the eastern standing Phlox and test hypotheses about if and how hybridization and gene flow were creative forces in their diversification. C_LIO_LIOur results provide novel resolution of the phylogenetic relationships in this group, including well-supported paraphyly across some species. We identify gene flow during one of two cases of reinforcement and find support for one of the five hypothesized homoploid hybrid speciation events. Additionally, we infer the ancestries of four allotetraploid hybrid species. C_LIO_LIHybridization has contributed to diverse evolutionary outcomes within this Phlox group; although, not as extensively as previously hypothesized. This study demonstrates the importance of phylogenomics in confirming hypothesized histories of non-model systems and adds to the growing evidence of interspecific genetic exchange in the generation of biodiversity. C_LI

evolutionary biology↗

Hybridization and introgression are prevalent in Southern European Erysimum (Brassicaceae) species

Background and AimsHybridization is a common and important force in plant evolution. One of its outcomes is introgression - the transfer of small genomic regions from one taxon to another by hybridization and repeated backcrossing. This process is believed to be common in glacial refugia, where range expansions and contractions can lead to cycles of sympatry and isolation, creating conditions for extensive hybridization and introgression. Polyploidization is another genome-wide process with a major influence on plant evolution. Both hybridization and polyploidization can have complex effects on plant evolution. However, these effects are often difficult to understand in recently evolved species complexes. MethodsWe combined flow cytometry, transcriptomic and genomic analyses, and pollen-tube growth assays to investigate the consequences of polyploidization, hybridization, and introgression on the recent evolution of several Erysimum (Brassicaceae) species from the South of the Iberian Peninsula, a well-known glacial refugium. This species complex differentiated in the last 2Myr, and its evolution has been hypothesized to be determined mainly by polyploidization, interspecific hybridization, and introgression. Key ResultsOur results support a scenario of widespread hybridization involving both extant and "ghost" taxa. Several taxa studied here, most notably those with purple corollas, are polyploids, likely of allopolyploid origin. Moreover, hybridization in this group might be an ongoing phenomenon, as prezygotic barriers appeared weak in many cases. ConclusionsThe evolution of Erysimum spp. has been determined by hybridization to a large extent. The adaptive value of such genomic exchanges remains unclear, but our results indicate the importance of hybridization for plant diversification across evolutionary scales.

evolutionary biology↗

Targeted sequencing of candidate genes of dyslipidemia in Punjabi Sikhs: Population-specific rare variants in GCKR promote ectopic fat deposition

Dyslipidemia is a well-established risk factor for cardiovascular diseases. Although, advances in genome-wide technologies have enabled the discovery of hundreds of genes associated with blood lipid phenotypes, most of the heritability remains unexplained. Here we performed targeted resequencing of 13 bona fide candidate genes of dyslipidemia to identify the underlying biological functions. We sequenced 940 Sikh subjects with extreme serum levels of hypertriglyceridemia (HTG) and 2,355 subjects were used for replication studies; all 3,295 participants were part of the Asian Indians Diabetic Heart Study. Gene-centric analysis revealed a burden of variants for increasing HTG risk in GCKR (p=2.1x10-5), LPL (p=1.6x10-3) and MLXIPL (p=1.6x10-2) genes. Of these, three missense and damaging variants within GCKR were further examined for functional consequences in vivo using a transgenic zebrafish model. All three mutations were South Asian population-specific and were largely absent in other multiethnic populations of the Exome Aggregation Consortium. We built different transgenic models of human GCKR with and without mutations and analyzed the effects of dietary changes in vivo. Despite the short-term feeding, profound phenotypic changes were apparent in hepatocyte histology and fat deposition associated with increased expression of GCKR in response to a high fat diet (HFD). Liver histology of the GCKRmut showed severe fatty metamorphosis which correlated with ~7 fold increase in the mRNA expression in the GCKRmut fish even in the absence of a high fat diet. These findings suggest that functionally disruptive GCKR variants not only increase the risk of HTG but may enhance ectopic lipid/fat storage defects in the absence of obesity and HFD. To our knowledge, this is the first transgenic zebrafish model of a putative human disease gene built to accurately assess the influence of rare genetic changes and their phenotypic consequences in vivo.

genetics↗

DPP9 is an endogenous and direct inhibitor of the NLRP1 inflammasome that guards against human auto-inflammatory diseases

The inflammasome is a critical immune complex that activates IL-1 driven inflammation in response to pathogen- and danger-associated signals. Nod-like receptor protein-1 (NLRP1) is a widely expressed inflammasome sensor. Inherited gain-of-function mutations in NLRP1 cause a spectrum of human Mendelian diseases, including systemic autoimmunity and skin cancer susceptibility. However, its endogenous regulation and its cognate ligands are still unknown. Here we apply a proteomics screen to identify dipeptidyl dipeptidase, DPP9 as a novel interacting partner and a specific endogenous inhibitor of NLRP1 inflammasome in diverse primary cell types from human and mice. DPP9 inhibition via small molecule drugs, targeted mutations in its catalytic site and CRISPR/Cas9-mediated genetic deletion potently and specifically activate the NLRP1 inflammasome leading to pyroptosis and IL-1 processing via ASC and caspase-1. Mechanistically, DPP9 maintains NLRP1 in its monomeric, inactive state by binding to the auto-cleaving FIIND domain. NLRP1-FIIND is a self-sufficient DPP9 binding module and its disruption by a single missense mutation abrogates DPP9 binding and explains the aberrant inflammasome activation in NAIAD patients with arthritis and dyskeratosis. These findings uncover a unique peptidase enzyme-based mechanism of inflammasome regulation, and suggest that the DPP9-NLRP1 complex could be broadly involved in human inflammatory disorders.

immunology↗

Variation in context dependent foraging behavior across pollinators

Pollinator foraging behavior has direct consequences for plant reproduction and has been implicated in driving floral trait evolution. Exploring the degree to which pollinators exhibit flexibility in foraging behavior will add to a mechanistic understanding of how pollinators can impact selection on plant traits. Although plants have evolved suites of floral traits to attract pollinators, flower color is a particularly important aspect of the floral display. Some pollinators show strong innate color preference, but many pollinators display flexibility in preference due to learning associations between rewards and color, or due to variable perception of color in different environments or plant communities. This study examines the flexibility in flower color preference of two groups of native butterfly pollinators under natural field conditions. Our study reveals that pipevine swallowtails and skippers, the predominate pollinators of the two native Texas Phlox species, display distinct patterns of color preferences across different contexts. Pipevine swallowtails exhibit highly flexible color preferences and likely utilize other floral traits to make foraging decisions. In contrast, skippers have consistent color preferences and likely use flower color as a primary cue for foraging. As a result of this variation in color preference flexibility, the two pollinator groups impose concordant selection on flower color in some contexts but discordant selection in other contexts. This variability could have profound implications for how flower traits respond to pollinator-mediated selection. Our findings suggest that studying dynamics of behavior in natural field conditions is important for understanding plant-pollinator interactions.

animal behavior and cognition↗

Correlated evolution of self and interspecific incompatibly across the range of a Texas wildflower

Plant species have repeatedly evolved recognition systems between pollen and pistils that identify and reject inappropriate matings. Two of the most important systems recognize self-pollen and interspecific pollen. Outstanding questions are whether and how these two recognition systems are linked and if this association could constrain the evolution of mate choice. Our study characterizes variation in self and interspecific incompatibility in the native range of the Texas wildflower Phlox drummondii. We found quantitative variation in self-incompatibility and demonstrate that this variation is significantly correlated with variation in incompatibility with its close congener P. cuspidata. Furthermore, we find strong evidence that self and interspecific incompatibility involve common mechanisms of pollen adhesion or early pollen-tube germination. Finally, we show that P. drummondii populations that co-occur and hybridize with P. cuspidata have significantly higher interspecific incompatibility and self-incompatibility than isolated P. drummondii populations. This geographic variation suggests that the evolution of self-compatibility is constrained by selection favoring interspecific incompatibility to reduce maladaptive hybridization. To our knowledge this is the strongest evidence that a correlation between variation in self and interspecific incompatibilities could influence the evolution of pollen recognition across the range of a species.

plant biology↗