Both intrinsic and extrinsic forces work together to shape connectivity and genetic variation in populations across the landscape. Here we explored how geography, breeding system traits, and environmental factors influence the population genetic patterns of Triodanis perfoliata, a widespread mix‐mating annual plant in the contiguous US. By integrating population genomic data with spatial analyses and modeling the relationship between a breeding system and genetic diversity, we illustrate the complex ways in which these forces shape genetic variation. Specifically, we used 4705 single nucleotide polymorphisms to assess genetic diversity, structure, and evolutionary history among 18 populations. Populations with more obligately selfing flowers harbored less genetic diversity (π: R2 = .63, p = .01, n = 9 populations), and we found significant population structuring (FST = 0.48). Both geographic isolation and environmental factors played significant roles in predicting the observed genetic diversity: we found that corridors of suitable environments appear to facilitate gene flow between populations, and that environmental resistance is correlated with increased genetic distance between populations. Last, we integrated our genetic results with species distribution modeling to assess likely patterns of connectivity among our study populations. Our landscape and evolutionary genetic results suggest that T. perfoliata experienced a complex demographic and evolutionary history, particularly in the center of its distribution. As such, there is no singular mechanism driving this species' evolution. Together, our analyses support the hypothesis that the breeding system, geography, and environmental variables shape the patterns of diversity and connectivity of T. perfoliata in the US.
Premise Understanding species’ responses to climate change is a critical challenge facing biologists today. Though many species are widespread, few studies of climate‐driven shifts in flowering time have examined large continuous spatial scales for individual species. And even fewer studies have examined these shifts at time scales greater than a few decades. Methods We used digitized herbarium specimens and PRISM climate data to produce the spatially and temporally broadest‐scale study of flowering time in a single species to date, spanning the contiguous United States and 153 years (1863–2016) for a widespread weedy annual, Triodanis perfoliata (Campanulaceae). We examined factors driving phenological shifts as well as the roles of geographic and temporal scale in understanding these trends. Results Year was a significant factor in both geospatial and climatic analyses, revealing that flowering time has advanced by ~9 days over the past ~150 years. We found that temperature as well as vapor pressure deficit, an understudied climatic parameter associated with evapotranspiration and water stress, were strongly associated with peak flowering. We also examined how sampling at different spatiotemporal scales influences the power to detect flowering‐time shifts, finding that relatively large spatial and temporal scales are ideal for detecting flowering‐time shifts in this widespread species. Conclusions Our results emphasize the importance of understanding the interplay of geospatial factors at different scales to examine how species respond to climate change.
Local selection can promote phenotypic divergence despite gene flow across habitat mosaics, but adaptation itself may generate substantial barriers to genetic exchange. In plants, life-history, phenology, and mating system divergence have been proposed to promote genetic differentiation in sympatry. In this study, we investigate phenotypic and genetic variation in Mimulus guttatus (yellow monkeyflowers) across a geothermal soil mosaic in Yellowstone National Park (YNP). Plants from thermal annual and nonthermal perennial habitats were heritably differentiated for life-history and mating system traits, consistent with local adaptation to the ephemeral thermal-soil growing season. However, genome-wide genetic variation primarily clustered plants by geographic region, with little variation sorting by habitat. The one exception was an extreme thermal population also isolated by a 200 m geographical gap of no intermediate habitat. Individual inbreeding coefficients (F IS ) were higher (and predicted by trait variation) in annual plants and annual pairs showed greater isolation by distance at local (<1 km) scales. Finally, YNP adaptation does not reuse a widespread inversion that underlies M. guttatus life-history ecotypes range-wide, suggesting a novel genetic mechanism. Overall, this work suggests that life-history and mating system adaptation strong enough to shape individual mating patterns does not necessarily generate incipient speciation without geographical barriers.
The evolution of genomic incompatibilities causing postzygotic barriers to hybridization is a key step in species divergence. Incompatibilities take two general forms structural divergence between chromosomes leading to severe hybrid sterility in F1hybrids and epistatic interactions between genes causing reduced fitness of hybrid gametes or zygotes (Dobzhansky-Muller incompatibilities). Despite substantial recent progress in understanding the molecular mechanisms and evolutionary origins of both types of incompatibility, how each behaves across multiple generations of hybridization remains relatively unexplored. Here, we use genetic mapping in F2and RIL hybrid populations between the phenotypically divergent but naturally hybridizing monkeyflowersMimulus cardinalisandM. parishiito characterize the genetic basis of hybrid incompatibility and examine its changing effects over multiple generations of experimental hybridization. In F2s, we found severe hybrid pollen inviability (< 50% reduction vs. parental genotypes) and pseudolinkage caused by a reciprocal translocation between Chromosomes 6 and 7 in the parental species. RILs retained excess heterozygosity around the translocation breakpoints, which caused substantial pollen inviability when interstitial crossovers had not created compatible heterokaryotypic configurations. Strong transmission ratio distortion and inter-chromosomal linkage disequilibrium in both F2s and RILs identified a novel two-locus genic incompatibility causing sex-independent gametophytic (haploid) lethality. The latter interaction completely eliminated three of the expected nine F2genotypic classes without detectable effects on the pollen number or viability of double heterozygotes. Along with the mapping of numerous milder incompatibilities, these key findings illuminate the complex genetics of plant hybrid breakdown and are an important step toward understanding the genomic consequences of natural hybridization in this model system.
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