Thomas D. Cabot Associate Professor of Organismic and Evolutionary Biology
Office: Biolabs 1105, 16 Divinity Avenue
Lab Website: http://www.oeb.harvard.edu/faculty/bomblies/
The main interest of the lab is to understand the molecular mechanisms of evolutionary adaptation, but we see this broadly to include adaptation to both the internal environment (e.g. adaptation to changes in the genome) and the external environment (habitat adaptation). We work mostly with Arabidopsis arenosa, which we have been developing as a molecular model system. This lovely relative of A. thaliana is widely distributed in Europe, an obligate outcrosser, and tetraploid through most of its range with an extant diploid variant. Populations vary considerably in a number of interesting and potentially adapative traits, as well as in ploidy.
(1) Adaptation to whole genome duplication. Arabidopsis arenosa is autotetraploid through most of its central European range (that is, it duplicated its entire genome via a within-species event that did not involve hybridization). The tetraploids, like their diploid progenitors, are obligately outcrossing and fully fertile. From artificially doubled diploids, we know that the diploid genome is not already competent to sustain stable meiosis in the polyploid state, yet the established polyploids show cytologically diploid-like behavior (this was from our collaborators James Higgins, now at the University of Leicester, UK, and Chris Franklin at the University of Birmingham in the UK). This suggests that the diploid was not pre-adapted to polyploid meiosis and that the established tetraploid adapted to its polyploid genome. What processes were modified and what protein functions changed to condition this, are questions we are seeking to answer using a combination of genomics, transcriptomics, molecular genetics and cytology. In two genome scans we identified a set of genes that were likely important in tetraploid evolution. With genetic follow-up, we have shown that allelic variation in at least one of these genes has a dramatic effect on chromosome segregation in the tetraploids. These genes indicate that likely the function that evolved was the regulation of meiotic crossover number, and more specifically, the strength of crossover interference. We are currently following this up to test this, and to understand the underlying mechanisms. We are also analyzing the molecular evolution of meiosis-related genes in diploid and tetraploid A. arenosa and have found intriguing patterns that are prompting us to explore the evolution of meiosis genes in greater detail.
(2) Biogeography and Habitat adaptation. Arabidopsis arenosa autotetraploids have adapted to a wide range of habitats, ranging from the apparently ancestral shaded limestone outcrop habitat to silicaceous outcrops, serpentine, railways, acid bogs, beaches, and heavy metal contaminated mine tailings. We are interested in understanding the genetic basis of their invasion of human-associated flatland railway habitats from ancestral mountain rock-outcrop habitats. The invasion of the the drier, hotter railway habitat (which also gets sprayed nearly annually with herbicide) is associated with a switch from perennial winter-dependent episodic flowering to an annual, rapid-cycling, perpetually flowering winter-independent habit. We are using population genomic as well as genetic approaches to explore the molecular basis of this adaptation, and are very interested in whether this involves the same genes or distinct ones from related well-characterized A. thaliana. We already have evidence that early flowering arose at least twice and apparently through independent molecular mechanisms in A. arenosa. Currently we are mapping the causal genes. We are also investigating the associated loss of perenniality in this system and using it as an inroad to understanding the molecular mechanisms of perenniality.
(3) Evolutionary dynamics of interacting genes. One striking observation from our genome scans is that signatures of selection are often seen in genes whose protein products are known to interact. This raises a number of questions: Are these genes adaptating to their genomic context? Do they co-evolve as "adaptive modules" or do they all contribute additively to phenotype? Do they all need to be in the correct allelic state for the complex to function? We are currently exploring these questions with a large population resequencing study and follow-up experiments, as well as broader phylogenetic tests for evolutionary rate co-variation. We are particularly focused on several groups of functionally-connected meiosis genes that show evidence of having undergone selective sweeps in tetraploids, as well as in some cases also in diploids.
Current group members:
Kevin Wright - Postdoc / NIH NRSA fellow. Meiotic adaptation in A. arenosa.
Andrew Lloyd - Postdoc. Marie Curie Fellow. Meiotic mechanisms in tetraploid A. arenosa.
Brian Arnold – PhD student. NSF Predoctoral fellow. Population genetics and genomics of A. arenosa.
Pierre Baduel – PhD student. Flowering time adaptation in A. arenosa.
Yherson Franchesco Molina Henao – PhD student. Variation among strains in meiosis and the propensity to form tetraploids.
Linnea Sandel - Meme Masters student (cosponsored by John Wakeley).
Julie Vu - Undergraduate researcher. Polyploid meiosis.
John Pulice - Undergraduate researcher. Inheritance in polyploids.
Publications from the lab
Bomblies, K., Higgins, J.D., Yant, L. (2015) Meiosis Evolves: Adaptation to external and internal environments. Invited Tansley Review. New Phytologist. IN PRESS.
Arnold, B., Kim, S-T., Bomblies, K. (2015) Single geographic origin of a widespread autotetraploid Arabidopsis arenosa lineage followed by interploidy admixture. Mol Biol Evol. IN PRESS (Link).
Wright, K. M., Arnold, B., Xue, K., Šurinová, M., O'Connell, J., Bomblies, K. (2015) Selection on meiosis genes in diploid and tetraploid Arabidopsis arenosa. Mol Biol Evol 32: 944-955 (Link).
Bomblies, K. (2014) Meiotic Drivers: Cheaters divide and conquer. Invited Perspective Article. eLife 2014;3:e03371.
Bomblies, K., Madlung, A. (2014) Polyploidy in the Arabidopsis genus. Invited review. Chromosome Research. 22: 117-134.
Bomblies, K., Loudet, O. (2014) Editorial Overview: Genome studies and molecular genetics: Genomic approaches to understanding evolution, development and the plant phenome. Current Opinion in Plant Biology, 18: v-vi [Preface to volume co-edited with Olivier Loudet].
Higgins, J. D., Wright, K. M., Bomblies, K., Franklin, C. H. F. (2013) Cytological techniques to analyze meiosis in Arabidopsis arenosa for investigating adaptation to polyploidy. Frontiers in Plant Science. 4: 546. (Link).
Yant, L.*, Hollister, J. D.*, Wright, K. M., Arnold, B. J., Higgins, J. D., Franklin, F. C. H., Bomblies, K. (2013) Meiotic adaptation to genome duplication in Arabidopsis arenosa. Current Biology. Vol 23, pp. 2151-2156. * = contributed equally (Link). [Featured in a Dispatch article in Current Biology and a Science editor's choice].
Wright, K. M., Bomblies, K. (2013) Evolutionary genetics: Inheritance of a complex pollination syndrome. Current Biology. Dispatch article. Vol 23, pp. R525-R527 (Link).
Arnold, B.*, Corbett-Detig, R. B.*, Hartl, D., Bomblies, K. (2013) RADseq underestimates diversity and introduces genealogical biases due to nonrandom haplotype sampling. Molecular Ecology. Vol 22, pp. 3179-3190. * = contributed equally. (Link).
Hunter, B.*, Wright, K. M.*, Bomblies, K. (2013) Short read sequencing in studies of natural variation and adaptation. Curr Op Plant Biol. Vol 16, pp. 85-91. * = contributed equally. (Link).
Bomblies, K. (2013) Genes causing postzygotic hybrid incompatibility in plants: A window into co-evolution, in Polyploid and Hybrid Genomics (eds Z. J. Chen and J. A. Birchler), John Wiley & Sons, Inc., Oxford, UK.
Hollister, J., Arnold, B., Svedin, E., Xue, K., Dilkes, B., Bomblies, K. (2012) Genetic adaptation associated with genome-doubling in autotetraploid Arabidopsis arenosa. PLoS Genetics, 8(12): e1003093 (Open Access - Link).
Arnold, B., Bomblies, K., Wakeley, J. (2012) Extending coalescent theory to autotetraploids. Genetics. Vol 192, pp. 195-204. (Open Access- Link)
Hunter, B., Hollister, J. D., Bomblies, K. (2012) Epigenetic inheritance: What news for evolution? Current Biology. Dispatch article. Vol 22, pp. R54-R56. (Link)
Hunter, B., Bomblies, K. (2010) Progress and promise in using Arabidopsis to study adaptation, divergence and speciation. Invited review. In: The Arabidopsis Book. American Society of Plant Biologists. Ames, IA. (Link)
Bomblies, K. (2010). Doomed lovers: mechanisms of isolation and incompatibility in plant speciation. Invited review. Annual review of Plant Biology 61, pp. 109-124. (Link)
Bomblies, K. (2010) Evolution: Redundancy as an opportunity for innovation. Dispatch article. Current Biology. 20, pp. R320-R322. (Link)
Bomblies, K. (2009). Too much of a good thing? Hybrid necrosis as a by-product of plant immune system diversification. Invited review. Botany 87, pp. 1013-1022. (Link)
General Audience Publications
Bomblies, K. Do we understand the dynamics of our emerging global culture? Essay contribution to “What should we be worried about?” ed. John Brockman. 2013, Harper-Collins, New York, NY.
Bomblies, K. Plant Immunity in a changing world. Essay contribution to “Future Science – 19 essays from the Cutting Edge” edited by Max Brockmann (2011).
Bomblies, K. The stunning diversity of plants. 10 Questions Interview. Seed magazine. February 22, 2010.