Speciation, domestication, conservation biology, and weed evolution.
Fellow, Royal Society of London
Fellow, Royal Society of Canada
Canada Research Chair in Plant Evolutionary Genomics
M.S. University of Tennessee 1984
Ph.D. Washington State University 1987
Assistant Professor, Claremont Graduate School 1987-1993
Associate/Full/Distinguished Professor, Indiana University 1993-
Plant evolutionary genomics; speciation; domestication; invasiveness; Compositae genomics
The Rieseberg lab integrates high-throughput genomic methods, bioinformatics, ecological experiments, and evolutionary theory to study the origin and evolution of species, domesticated plants, and weeds. Some of the problems we are currently working on are described below:
Our primary research interest concerns how new plant species arise (Science 317:910-914) – one of the most fundamental questions in biology. Much of this work focuses on members of the sunflower genus Helianthus, but we also analyze patterns of variation in other plant and animal groups to make more general conclusions about speciation. Problems that have attracted our attention recently include, the nature of species (Nature 440:524-527), the importance of advantageous alleles in holding species together (Molecular Ecology 13:1341-1356), the evolutionary forces underlying phenotypic diversification (PNAS 99:12242-12245), the frequency of polyploid speciation (PNAS 106:13875-13879), the role of hybridization in evolution (ARES 28:359-389), and the contribution of chromosomal rearrangements to speciation (TREE 16:351-358).
In Helianthus, our goals are to identify and order the genetic changes responsible for the origin of species in this group and to understand how the new species survive, evolve, and interact after they are formed. Specific phenomena that appear to be critical for speciation in this group include hybridization, ecological divergence, and chromosomal rearrangements.
1.1. The role of hybridization in evolution.
Hybridization has played a major role in the evolution of wild sunflowers, contributing both to adaptation within species and to the origin of entirely new species. We have employed phylogenetic reconstruction, quantitative trait locus (QTL) analyses, field experiments, computer simulations, and comparative genomic approaches to identify hybrid taxa (Fig. 1), determine how they have become reproductively isolated (Science 272:741-745), estimate the speed with which they arose (Evolution 62:266-275), and assess the contribution of hybrid gene combinations to adaptation (Science 301:1211-1216). Sequence data have also been employed to determine the demographic history of hybridizing sunflower species and to estimate rates of long term gene flow (Evolution 62:1936–1950)
Fig. 1. Hybrid sunflower species, H. anomalus (photo by J. Rick)
Our current work on hybridization has a strong genomics and bioinformatics flavor. For example, we are using next generation sequencing platforms to scan the genomes of hybridizing species to identify islands of genetic differentiation, as well as recent selective sweeps. Similarly, in collaboration with K. Whitney (Rice University), we are developing SNP arrays to track changes in allele frequencies at candidate genes in ongoing field- and greenhouse-based selection experiments. We also have developed highly automated bioinformatics pipelines for detecting hybridization and polyploidy in large sequence data sets (M. Barker et al. unpublished). Our preliminary analyses imply that both phenomena are more frequent and play a larger role in evolution that previously hypothesized.
1.2. The genetics of ecological divergence.
Speciation in Helianthus appears to have been driven by habitat differentiation. Even hybrid species are strongly divergent ecologically from their parental species. We are employing a combination of ecophysiological studies, QTL analyses, field experiments, association mapping, candidate gene analyses, and hitchhiking mapping to identify the traits, genes, and mutations responsible for habitat divergence in this group (Molecular Ecology 12:1225-1235;Genetics 175:1803–1812). We are particularly interested in the molecular and ecological bases of variability in flowering time, salt adaptation, and drought tolerance. For example, we have recently shown that a latitudinal cline in flowering time in common sunflower (Fig. 2) results from changes at multiple hierarchical levels in multiple genetic pathways, including paralog-specific changes in FT homolog expression and tissue-specific changes in SOC1 homolog expression (B. Blackman et al. unpublished).
Fig. 2. Clinal differentiation of flowering and changes in photoperiod response in wild sunflower populations. (A) Locations of the populations sampled. (B) Flowering responses of wild populations under three photoperiod conditions. (C) Sunflower population near Norman, OK at peak flowering photographed on September 19, 2006. (D) Sunflower population near Austin, TX post-shattering and senesced photographed on September 21, 2006. (from Blackman, B. K., Michaels, S. D., and Rieseberg, L. H. 2009. Connecting the Sun to Flowering in Sunflower Adaptation. unpublished).
1.3. The role of chromosomal rearrangements in speciation.
Chromosomal rearrangements contribute to speciation in two main ways. First, some types of rearrangements such as inversions may suppress recombination locally, thereby facilitating the accumulation of hybrid incompatibilities or other species’ differences (ARES 39:21-42). Other kinds of rearrangements such as translocations can cause sterility in hybrids heterozygous for the rearrangement. A major unsolved mystery is why such “under-dominant” rearrangements are much more frequent in plants than in animals.
We are investigating the establishment of chromosomal rearrangements in wild sunflowers and their role in speciation. We have previously shown that (1) sunflowers have the highest rate of karyotypic evolution in either plants or animals (Genetics 167:449-457), (2) many of the rearrangements are strongly under-dominant (Genetics171:291-303), and (3) rates of interspecific gene flow are reduced near chromosomal breakpoints (Molecular Biology and Evolution 26:1341-1355). Current studies employ a combination of genome sequencing and bioinformatic approaches to ask whether the greater redundancy of plant genomes might account for differences in rates and patterns of karyotypic evolution between plants and animals. Genetic redundancy due to whole genome and/or segmental duplication should reduce the initial under-dominance of chromosomal rearrangements, thereby facilitating their establishment.
Fig. 3. Domesticated sunflower (photo by J. Rick)
The dramatic, human-mediated transformations associated with plant domestication provide a model for studying phenotypic evolution. My lab has exploited this situation by studying the domestication of sunflower (Fig. 3). Phylogeographic analyses indicate that sunflower was domesticated in the eastern United States and not in southern Mexico, establishing the eastern U.S. as one of five to seven regions in the world in which agriculture arose independently (Nature 430:201-205). Genetic study showed that sunflower was easily domesticated: there were few major QTLs and many wild QTL alleles had effects in the direction of the cultivar (Genetics 161:1257-1267). More recently, we employed an integrated candidate gene strategy to identify five paralogs in the FT/TFL1 gene family that have experienced selective sweeps during a stage of sunflower domestication and may be the causal loci contributing flowering time QTL (Fig. 4). Genetic and functional studies of one of these paralogs (HaFT1), indicates that a frameshift mutation in the domesticated allele causes a delay in flowering by interfering with the action of another paralog, HaFT4 (Current Biology 20:629-635).
Fig. 4. Flowchart illustrating the criteria applied in this integrated candidate gene approach and the serial refinement of the candidate gene pool. (from B. Blackman et al. 2009. Contributions of flowering time genes to sunflower domestication and improvement. Unpublished).
Current work includes a large-scale search for associations between sequence variation at candidate genes and domestication traits, genome scans using next generation sequencing approaches to search for regions of the genome that have undergone selective sweeps during domestication and improvement, and further analyses of the FT/TFL1 family to identify the causative mutations underlying flowering time QTLs. Other projects focus on the domestication and improvement of Noug and Yacon, which are indigenous Compositae crops from Ethiopia and South America, respectively.
Invasive plants represent a major threat to the economy and environment, with annual economic costs to North America of $35-40 billion. In collaboration with laboratories at UBC (S. Otto, J. Whitton, and K. Adams) and Indiana University (Z. Lao, Jim Bever, and K. Clay), we are using common garden experiments, microarray analyses (Genetics 179:1881-1890), and hitchhiking and association mapping with next generation sequence data to identify specific genetic changes associated with invasiveness. By targeting Compositae weeds for this work – diffuse knapweed, starthistle, Canada thistle, ragweed, and common sunflower – we can exploit the genomic tools and resources developed by the Compositae Genome Project (see below).
Individuals from weedy or invasive populations of many plant species grow larger and faster than individuals from native populations, an observation that we have confirmed for several Compositae weeds. Explanations for this pattern typically involve life history trade-offs, in which investment in costly defense or abiotic tolerance traits is reallocated to growth and reproduction. We are asking whether similar molecular genetic mechanisms underlie these trade-offs in different Compositae weeds.
We also are exploring the role of hybridization in weed evolution. Many plant invasions are associated with hybridization, so it might be that the increased vigor observed in some invasive plants results from residual heterosis rather than life history trade-offs. We have found evidence of past hybridization in invasive starthistle populations (K. Dlugosch et al. unpublished), and will explore this possibility in other Compositae weeds.
Hybridization may also play a role in weed evolution by providing a vehicle for the escape of genetically engineered genes (transgenes) from crop plants into wild or weedy relatives. We have documented very high levels of gene flow between cultivated and weedy sunflower populations (Fig. 5), indicating that transgene escape is likely. We also have collaborated with several other groups to assess the fitness consequences of individual transgenes in a wild type background. Along with collaborators, we have shown that a Bt transgene that kills some species of insects is highly advantageous and likely to escape (Ecological Applications 13:279-286), but that a transgene affecting a fungal pathogen is unlikely to do so (Science 300:1250). Recent work tests the strength of selection against domestication QTLs and asks whether linkage with transgenes could limit the spread of the latter (Molecular Ecology 17:666-67).
Fig. 5. Weedy sunflowers along border of cultivated field (photo by J. Rick).
4. Compositae genomics
In collaboration with groups at UC Davis (R. Michelmore & K. Bradford), U. Georgia (S. Knapp & J. Burke), U. Massachusetts (R. Kesseli), Indiana University (Z. Lai), and Cal Poly Pomona (D. Still), we are developing genomic resources and tools for the Compositae, one of the largest and most ecologically diverse families of flowering plants (http://cgpdb.ucdavis.edu/). These resources include ~1 million Sanger ESTs for crops and weeds in the family, detailed genetic linkage maps, QTL populations, functional maps, and NimbleGen and/or Affymetrix gene chips for key species. These tools and resources underlie many of the projects described above. In addition, the large sequence and expression data sets generated by the Compositae Genome Project (CGP) are being used to answer more general questions about genomic and phenotypic evolution across the family. For example, analyses of the age distribution of duplicate genes in 18 species from across the Compositae family revealed at least three ancient whole genome duplications. These include a paleopolyploidization shared by all analyzed taxa and placed near the origin of the family just prior to the rapid radiation of its tribes, and independent genome duplications near the base of the tribes Mutisieae and Heliantheae (Molecular Biology and Evolution 25:2445-2455). We also showed that contrary to Arabidopsis, genes annotated to structural components or cellular organization GO categories were significantly enriched among paleologs, whereas genes associated with transcription and other regulatory functions were significantly underrepresented (Fig. 6).
Ongoing work includes the sequencing of gene space for lettuce, sunflower, and safflower, transcriptome sequencing of an additional 25 genotypes from across the Compositae, analyses of copy number variation within and among Compositae species, and comparative analyses of domestication traits and the genes that underlie them. In addition, we are collaborating with researchers at INRA (P. Vincourt), U. Georgia (S. Knapp & J. Burke), and UBC (N. Kane & E. Marden) to sequence the sunflower genome and to determine the genetic basis of wood development in drought tolerant, wood-forming, wild sunflower species.
Fig. 6. GO annotations of Compositae whole transcriptome and paleologs. The left-most column displays the pooled Compositae transcriptome of 18 species, whereas the remaining columns represent paleologs retained in each tribe from the basal Compositae genome duplication and the basal Heliantheae genome duplication. Colors represent % of transcriptome a particular GO category composes. Superscripts indicate significantly different groups as determined by Chi-square tests (p < 0.05). GO categories that are significantly enriched or reduced among paleologs relative to non-paleologs in at least three comparisons are indicated with +/- signs. (from Barker et al. 2009; Molecular Biology and Evolution 25:2445-2455).
Biol 525 - Speciation
Blackman, B.K., J.L. Strasburg, S.D. Michaels, and L.H. Rieseberg. 2010. The role of recently derived FT paralogs in sunflower domestication. Current Biology 20:629–635.
Wood, T.E., N. Takebayashi, M.S. Barker, I. Mayrose, P.B. Greenspoon, L.H. Rieseberg. 2009. The frequency of polyploid speciation in vascular plants. Proceedings of the National Academy of Sciences USA 106:13875-13879.
Rieseberg, L.H., and J.H. Willis. Plant speciation. 2007. Science 317:910-914.
Rieseberg, L.H., T.E. Wood, and E. Baack. 2006. The nature of plant species. Nature 440:524-527.
Harter, A.V., K.A. Gardner, D. Falush, D.L. Lentz, R. Bye, L.H. Rieseberg. 2004. Origin of extant domesticated sunflowers in eastern North America. Nature 430:201-205.
Burke, J.M., and L.H. Rieseberg. 2003. The fitness effects of transgenic disease resistance in wild sunflowers. Science 300:1250.
Rieseberg, L.H., O. Raymond, D.M. Rosenthal, Z. Lai, K. Livingstone, T. Nakazato, J.L. Durphy, A.E. Schwarzbach, L.A. Donovan, and C. Lexer. 2003. Major ecological transitions in annual sunflowers facilitated by hybridization. Science 301:1211-1216.
Rieseberg, L. H., A. Widmer, M. A. Arntz, and J. M. Burke. 2002. Directional selection is the primary cause of phenotypic diversification. Proceedings of the National Academy of Sciences USA 99:12242-12245.