Patterns of genetic variation in a prairie wildflower, Silphium integrifolium, suggest a non-prairie origin and locally adaptive variation

PREMISE: Understanding the relationship between genetic structure and geography provides information about a species’ history and can be used for breeding and conservation goals. The North American prairie is interesting because of its recent origin and subsequent fragmentation. Silphium integrifolium, an iconic perennial American prairie wildflower, is targeted for domestication, having undergone a few generations of improvement. We present the first application of population genetic data in this species to address the following goals: (1) improve breeding by characterizing genetic structure and (2) identify the species geographic origin and potential targets and drivers of selection during range expansion. METHODS: We developed a reference transcriptome as a genotyping reference for samples from throughout the species range. Population genetic analyses were used to describe patterns of genetic variation, and demographic modeling was used to characterize potential processes that shaped variation. Outlier scans for selection and associations with environmental variables were used to identify loci linked to putative targets and drivers of selection. RESULTS: Genetic variation partitioned samples into three geographic clusters. Patterns of variation and demographic modeling suggest that the species origin is in the American Southeast. Breeding program accessions are from the region with lowest observed genetic variation. CONCLUSIONS: This prairie species did not originate within the prairie. Breeding may be improved by including accessions from outside of the germplasm founding region. The geographic structuring and the identified targets and drivers of adaptation can guide collecting efforts toward populations with beneficial agronomic traits

Self-incompatibility and Biosystematics in the Wild Chilean Tomato Group (Solanum sect. Lycopersicum)

Understanding the forces that influence the patterns of plant reproduction is a shared con- cern of plant evolutionary biology. Self-incompatibility (SI), the molecular rejection of self- pollen by an otherwise fertile hermaphroditic plant, is a widespread mechanism that promotes outcrossing (de Nettancourt, 1977). SI is found in over 100 plant families (Igic et al., 2008). The descriptions of the patterns of phylogenetic distribution of SI, as well as its strength in natural populations, and geographic distribution, have lead many to proclaim the importance of SI in the development and maintenance of plant species diversity (Whitehouse, 1950; Stebbins, 1957; Bateman, 1952). The transition from SI to self-compatibility (SC) in plant lineages is one of the most common pathways in plant evolution (Stebbins, 1974). The loss of enforced outcrossing leads to a reduction of genetic diversity and increased linkage disequilibrium within species. This has lead many to conclude that habitual self-fertilization is an evolutionary dead- end (Stebbins, 1957; Stebbins, 1974; Takebayashi and Morrell, 2001; Goldberg et al., 2010). Despite longstanding interest in patterns of SI occurrence and its maintenance and loss, rel- atively few empirical details are known about the evolution of SI and its relationship with realized mating patterns in natural populations. This thesis provides results from three research projects that relate to SI. First, the largest collection of reports of the strength of SI across flowering plants and its relationship with outcrossing rate are discussed. Second, variation in the strength of SI is quantified across populations of a wild tomato species. Results from controlled crosses to investigate the genetic basis of variation in SI and the effect of SI variation on outcrossing rate are reported. Lastly, results from an integrative biosystematic study, motivated by observed unique relationships between alleles involved in SI, suggest that species are not properly described in a group of wild tomatoes. The distribution of morphological and genetic variation and patterns of reproductive isolation across populations are provided as evidence of multiple species within a currently described single species. Together, the chapters synthesize novel insights into the evolution of a common plant breeding system

Data from: The expression of self-incompatibility in angiosperms is bimodal

Self-incompatibility is expressed by nearly one half of all angiosperms. A large proportion of the remaining species are self-compatible, and they either outcross using various contrivances or self-fertilize to some extent. Because of the common occurrence of populations and individuals with intermediate levels of self-incompatibility, categorization of the expression of self-incompatibility as an approximately binary trait has become controversial. We collect a widely reported index (ISI) used to asses the strength and variation of self-incompatibility from over 1200 angiosperm taxa. Its distribution is bimodal and positively associated with outcrossing rate, albeit with a weak relationship within self-compatible taxa. A substantial fraction of species have intermediate mean values of ISI. Their occurrence can be caused by segregating ephemeral self-compatible mutations, averaging artifacts, and experimental biases, in addition to the often invoked stabilizing selection acting on the expression of self-incompatibility. Selection may also generally favor taxa with high ISI values through increased lineage birth and death rates, and it may counter lower-level selection advantages within taxa expressing intermediate and low values of ISI. Such a null hypothesis is nearly universally overlooked, despite the fact that it could adequately explain the observed distribution of mating and breeding systems

ISI.dryad

ISI.drya

Contributions of Flowering Time Genes to Sunflower Domestication and Improvement

Determining the identity and distribution of molecular changes leading to the evolution of modern crop species provides major insights into the timing and nature of historical forces involved in rapid phenotypic evolution. In this study, we employed an integrated candidate gene strategy to identify loci involved in the evolution of flowering time during early domestication and modern improvement of the sunflower (Helianthus annuus). Sunflower homologs of many genes with known functions in flowering time were isolated and cataloged. Then, colocalization with previously mapped quantitative trait loci (QTLs), expression, or protein sequence differences between wild and domesticated sunflower, and molecular evolutionary signatures of selective sweeps were applied as step-wise criteria for narrowing down an original pool of 30 candidates. This process led to the discovery that five paralogs in the FLOWERING LOCUS T/TERMINAL FLOWER 1 gene family experienced selective sweeps during the evolution of cultivated sunflower and may be the causal loci underlying flowering time QTLs. Our findings suggest that gene duplication fosters evolutionary innovation and that natural variation in both coding and regulatory sequences of these paralogs responded to a complex history of artificial selection on flowering time during the evolution of cultivated sunflower

Multiple reproductive barriers separate recently diverged sunflower ecotypes

Measuring reproductive barriers between groups of organisms is an effective way to determine the traits and mechanisms that impede gene flow. However, to understand the ecological and evolutionary factors that drive speciation, it is important to distinguish between the barriers that arise early in the speciation process and those that arise after speciation is largely complete. In this article, we comprehensively test for reproductive isolation between recently diverged