David Bryant Lowry

Supernumerary B-Chromosomes are extra genetic elements that frequently deviate from Mendelian inheritance to ensure their own survival. Their evolutionary origins and biological impacts within natural plant populations remain largely unexplored. Switchgrass (Panicum virgatum) is a model for studies of local adaptation, but reliance on a single reference genome has limited the detection of lineage-specific genomic content. We generated chromosome-level genome assemblies from the diverged Atlantic switchgrass subpopulation and discovered a previously undetected genomic element: a ~34 Mb supernumerary B-Chromosome, validated by Hi-C contact mapping and long-read depth, which indicates two to four B copies per nucleus. The B-Chromosome has a bipartite architecture including a gene-rich, single-copy proximal region (~8 Mb) and a repeat-rich, gene-poor distal region (~27 Mb) dominated by LTR/Ty3 (Gypsy) elements and punctuated by Mutator TIR peaks. High-resolution mapping reveals a highly rearranged chimera of fragments from multiple autosomes, biased toward the N-subgenome. Intact LTR retrotransposons on the B-Chromosome are younger than those on the A-Chromosomes, especially in its distal region, consistent with a B-Chromosome that arose and expanded within the Atlantic lineage. Population screening and phylogenetic analysis indicate that the B-Chromosome is largely restricted to the Atlantic subpopulation and likely has a single origin. In a typical family, 70% of open-pollinated progeny of B-positive maternal plants were B-positive, with substantial variation among families. Finally, B-Chromosome presence is associated with expression differences in A-Chromosome genes that differ between genetic backgrounds. Together, our results show how accessory chromosomes contribute to the evolutionary and genomic diversity of natural plant populations.

Premise: Rising temperatures can reduce plant reproductive success by disrupting pollen development, yet little is known about how reproductive heat sensitivity varies among natural populations. We evaluated pollen viability responses to elevated temperature in two closely related taxa of yellow monkeyflowers across multiple geographic scales to determine whether heat sensitivity varies among species, between populations and across elevations. Methods: We conducted three common garden growth chamber experiments. First, we compared pollen viability responses to heat stress between Mimulus guttatus and members of the M. tilingii species complex. Second, we tested whether broad elevational categories explained variation in heat responses. Third, we evaluated heat sensitivity among nine eastern Sierra Nevada populations of M. guttatus spanning an elevational gradient. Pollen viability was assessed following exposure to control and heat treatments. Key results: Heat exposure reduced pollen viability in all experiments. In the species comparison experiment, pollen viability decreased more strongly in the high-elevation restricted M. tilingii species complex than the widespread M. guttatus . We found substantial population-level variation in pollen viability within M. guttatus but not members of the M. tilingii complex. Broad elevational categories did not explain this variation in pollen viability responses. However, within eastern Sierra Nevada populations, reductions in pollen viability became stronger with increasing source elevation. Several populations deviated from this trend, indicating reproductive responses to heat cannot be explained by elevation alone. Conclusions: Pollen heat sensitivity varies substantially among species and populations of yellow monkeyflowers. Elevation alone is insufficient to predict pollen viability responses to elevated temperatures, suggesting that local adaptation or genetic variation may contribute to reproductive heat tolerance. Some populations of M. guttatus may contain greater capacity to maintain reproductive function under future warming, highlighting the importance of considering intraspecific variation when predicting plant responses to climate change.

Lipomas are common benign adipocytic neoplasms with well-characterized somatic cytogenetic alterations, but the inherited genetic architecture predisposing to their formation remains poorly understood. Recent phenome-wide evidence identified lipoma as strongly associated with genetic predisposition toward longer telomeres. Here, I examined this relationship from the complementary perspective of lipoma genetics. FinnGen R13 genome-wide association and native fine-mapping data resolved nine independent lipoma susceptibility signals across seven genomic regions. Unbiased annotation of these signals implicated telomere-maintenance and genome-stability genes, including telomerase reverse transcriptase (TERT), regulator of telomere elongation helicase 1 (RTEL1), and STN1 subunit of CST complex (STN1), with proximity-expanded mapping additionally encompassing telomerase RNA component (TERC). Using 198 leukocyte telomere length (LTL)-associated genetic variants from All of Us, multiplicative-random-effects inverse-variance-weighted Mendelian randomization showed a strong positive association between genetically proxied LTL and lipoma susceptibility (beta=0.445, 95% CI 0.355-0.535; P=2.49 x 10^-22). The association replicated using independent UK Biobank LTL effects (beta=0.587, 95% CI 0.459-0.715; P=3.09 x 10^-19), remained positive across alternative estimators and sensitivity analyses, persisted after exclusion of 15 variants assigned to canonical telomere/DNA-damage-response genes, and extended across lipomas of the limbs, trunk, and head/face/neck. Regional analyses showed strong evidence for a shared LTL-lipoma association component at TERC (PP.H4=0.989), strong but unresolved regional overlap at TERT (PP.H4=0.924), and distinct association components at STN1 (formerly OBFC1; PP.H3=0.9995), demonstrating heterogeneous local architectures. The study used a human-supervised agentic research workflow in which ChatGPT contributed to analytical planning, interpretation, quality control, and synthesis, while Codex performed substantial computational execution and reproducibility auditing. Together, these findings connect the independently derived genetic architecture of lipoma susceptibility with a broader trade-off between maintenance of cellular replicative capacity and suppression of neoplastic growth.

Premise: Surviving the effects of oceanic salt spray is critical for plants in coastal ecosystems, yet the mechanisms of coastal plant resilience to salt spray are not well understood. We investigated mechanisms of salt spray adaptation by comparing five latitudinal pairs of yellow monkeyflower accessions locally adapted to coastal and inland habitats. Methods: We measured sodium levels in coastal and inland leaves exposed to experimental salt spray in the laboratory and compared leaf surface traits that may contribute to differences in sodium uptake between ecotypes. We assayed tissue tolerance by allowing sodium to enter leaf discs through the cut edges and recording time to necrosis for coastal and inland accessions. Results: The leaf surface of coastal accessions took up less sodium from the experimental salt spray than the inland accessions, which may contribute to local adaptation to oceanic salt spray in coastal habitats. Higher water content per unit leaf area and less water loss under salt spray further reduced sodium concentrations in salt‐sprayed coastal leaves compared to inland accessions. The coastal ecotype also had greater tissue tolerance to sodium than the inland ecotype. Conclusions: Coastal monkeyflowers employ salt spray exclusion and tissue tolerance mechanisms for salt spray resilience. Our results suggest that plant adaptation to coastal habitats may often involve the evolution of multiple mechanisms to survive stress imposed by oceanic salt spray.

Summary: Temperatures are rising globally and threatening the persistence of natural plant populations. Elevated temperatures disrupt gametogenesis, fertilization, and seed filling, often at lower thresholds than those affecting photosynthesis, growth, or survival. While crop scientists have found that key reproductive stages are particularly vulnerable to heat stress across plant systems, ecological and evolutionary studies have largely focused on other fitness metrics to estimate populations' resilience to warming. We advocate for integrating pollen, ovule, and seed filling developmental metrics into ecological and evolutionary studies to improve predictions of plant population dynamics under future climates. Such studies will offer not only a better understanding of how natural populations will respond to increasing temperature stress but also are likely to reveal novel mechanistic insights that can be utilized to improve crop resilience in a warming world.

Uncovering the genetic architecture of quantitative traits is challenging because polygenic control yields small individual gene effects and because gene–gene and genotype-by-environment interactions add further complexity. To understand the genetic basis of polygenic traits and their plasticity across environments, we integrated genome-wide SNPs and RNA-seq transcript data with interpretable statistical and machine learning models in a switchgrass (Panicum virgatum) diversity panel grown at contrasting field sites in Michigan and Texas. Notably, in addition to single environments, our trait prediction models were able to predict phenotypic differences, across environments i.e., plasticity. By interpreting trait prediction models with explainable artificial intelligence methods, we identified important features—genes that are the most predictive of flowering time and annual biomass production across environments, based on their associated gene expression levels and nearby SNPs. This approach recovered canonical flowering regulators and revealed novel, environment-specific candidate flowering genes. Further, transcriptome models consistently recovered more switchgrass genes homologous to experimentally validated genes in Arabidopsis and rice than SNP-based models. Feature interaction scores from the models also allow the identification of trait- and environment-dependent gene–gene interactions, where flowering time showed stronger and more abundant interactions than biomass. While some of the interactions identified are consistent with the link between flowering time and yield, most are novel predictors that need to be further evaluated. Together, these results demonstrate that interpretable genomic prediction with explainable artificial intelligence approaches can convert trait prediction models into mechanistic hypotheses about putative causal genes and interactions controlling traits within and across environments. These results will help to prioritize target genes for validation and inform germplasm selection for cultivar improvement.

Phenotypic plasticity allows plants to rapidly respond to changing environments without the need for evolutionary change or migration. While selection can create variation in plasticity across natural populations, these responses are not adaptive in all environments. To predict whether plasticity will be adaptive requires evaluation of its fitness effects across a range of environments, including novel ones. Here, we test how traits and their plasticity vary for genotypes collected across a natural hybrid zone between two tree species with contrasting climatic niches. Fast-growing Populus trichocarpa inhabits maritime environments with relatively warm and stable temperatures, while P. balsamifera inhabits continental environments with cold winters and large temperature variance throughout the year. We planted 44 clonally replicated genotypes into thirteen common gardens and measured vegetative phenology, leaf morphology, stomata morphology and conductance, and photochemistry. Overall, genotypes from colder, more continental environments exhibited higher plasticity. P. balsamifera ancestry was associated with increased plasticity in timing of fall phenology, stomatal conductance, and leaf mass per unit area. We assessed the effects of trait plasticity on fitness estimated as yearly growth across common gardens and found that the plasticity-fitness relationship was often garden-specific, indicating that the planting environment did not consistently mediate plasticity-fitness relationships. When the effects of trait plasticity on growth varied by garden temperature, higher plasticity generally had neutral or negative associations with growth in warmer environments. These results suggest that elevated plasticity evolved in a P. balsamifera genomic background as part of a climate generalist strategy to seasonal temperature variability, but that there is a trade-off between plasticity and growth in warmer environments. Consequently, less-plastic but warm-adapted P. trichocarpa genotypes are likely to have a fitness advantage under warming climates. These results demonstrate that plasticity may sometimes be maladaptive and will not be universally beneficial in a warming world.

The generality of the worldwide leaf economics spectrum (LES) has made it a pillar of trait-based ecological research. Yet, few studies have examined the processes shaping the evolution of the LES within species, in part, because most species occupy only a small portion of the LES. To address this gap, we took advantage of the distinct leaf economics strategies present in different ecotypes of the phenotypically diverse perennial grass Panicum virgatum (switchgrass) to generate a genetic mapping population, which we planted in common gardens at three sites spanning 12 degrees of latitude in the central United States. With this genetic mapping population, we evaluated two potentially interacting causes of LES evolution: 1) genetic architecture, where multiple traits are influenced by either the same gene (pleiotropy) or by genes in close physical proximity (genetic linkage), and 2) correlational selection, where selection acts on traits in combination rather than in isolation. We found that shared genetic architecture influenced covariation between photosynthetic rate ( A _MASS ) and leaf nitrogen ( N _MASS ) and between A _MASS and leaf mass per area (LMA). We also found that correlational selection favored the trait combinations predicted by the LES (e.g., high LMA with low N _MASS or low LMA with high N _MASS ) and disfavored other, mismatched trait combinations at two of the three sites. Together, these results demonstrate how the evolution of an integrated LES within species can arise from multiple evolutionary causes.

Summary: Plastic responses of plants to their environment vary as a result of genetic differentiation within and among species. To accurately predict rangewide responses to climate change, it is necessary to characterize genotype‐specific reaction norms across the continuum of historic and future climate conditions comprising a species' range. The North American hybrid zone of Populus trichocarpa and Populus balsamifera represents a natural system that has been shaped by climate, geography, and introgression. We leverage a dataset containing 44 clonal genotypes from this natural hybrid zone, planted across 17 replicated common garden experiments spanning a broad climatic range. Growth and mortality were measured over 2 yr, enabling us to model reaction norms for each genotype across these tested environments. Species ancestry and intraspecific genomic variation significantly influenced growth across environments, with genotypic variation in reaction norms reflecting a trade‐off between cold tolerance and growth. Using modeled reaction norms for each genotype, we predicted that genotypes with more P. trichocarpa ancestry may gain an advantage under warmer climates. Spatial shifts of the hybrid zone could facilitate the spread of beneficial alleles into novel climates. These results highlight that genotypic variation in responses to temperature will have landscape‐level effects.

Premise: Surviving under oceanic salt spray is critical for plants in coastal ecosystems, yet the mechanisms of coastal plant resilience to salt spray are not well understood. We investigated mechanisms of salt spray adaptation by comparing five latitudinal pairs of yellow monkeyflower accessions locally adapted to coastal and inland habitats. Methods: We measured sodium levels in coastal and inland leaves exposed to experimental salt spray in the lab, and compared leaf surface traits that may contribute to differences in sodium uptake between ecotypes. We assayed tissue tolerance by allowing sodium to enter leaves through wounding and recording time to necrosis for coastal and inland accessions. Key Results: Coastal monkeyflowers take up less sodium through the leaf surface under experimental salt spray, which may contribute to local adaptation under oceanic salt spray in coastal habitats. Higher water content per unit leaf area and less water loss under salt spray further reduce sodium concentrations in salt-sprayed coastal leaves compared to inland counterparts. The coastal ecotype also shows greater tissue tolerance to sodium than the inland ecotype. Conclusions: Coastal monkeyflowers employ salt spray exclusion and tissue tolerance mechanisms for salt spray resilience. Our results suggest that plant adaptation to coastal habitats may often involve the evolution of multiple mechanisms to survive stress imposed by oceanic salt spray.