Pattern Formation and Genome Evolution
My collaboration with Joshua R. Puzey at William & Mary combines mathematical modelling, statistical analysis and evolutionary genomics to investigate biological diversity. Monkeyflowers (Mimulus) connect projects on floral pigmentation, hybridization, genome duplication and gene regulation. Work with Arielle Cooley and other experimental collaborators links observations of developing plants with models that help distinguish possible mechanisms.
How hybrid flowers acquire new patterns
Hybridization can produce floral patterns absent from either parent. We study this process through the interacting genes that regulate anthocyanin pigmentation. Our 2021 collaboration identified MYB5a/NEGAN as a regulator of petal pigmentation and showed how changing its expression affects the wider regulatory network. [1]
In 2023, Emily Simmons, Arielle Cooley, Puzey and I developed a multigenerational Turing model that combines an activator–inhibitor reaction–diffusion system with diploid inheritance. The model produces spotted offspring from parents with unpatterned petals and reproduces variation across subsequent generations. It provides a proof of concept for how inherited differences in a regulatory network can generate new spatial patterns, rather than requiring a new patterning mechanism to appear in the hybrid. [2]
The work raises further experimental questions about how self-organizing gene activity interacts with positional information, including cues associated with petal veins. Genetic mapping, expression experiments, image analysis and spatial statistics provide complementary ways to investigate those relationships.
Gene expression after hybridization and genome duplication
When divergent genomes are brought together, corresponding genes inherited from the parental lineages need not be expressed equally. Our 2017 collaborative study found that subgenome expression dominance can appear in first-generation Mimulus hybrids, with stronger bias in a naturally established allopolyploid lineage carrying chromosome sets from different species. [3]
In 2019, we developed a likelihood ratio test for changes in homeolog expression bias: the relative expression of corresponding gene copies inherited from the parental species. Applied to leaf and petal RNA-sequencing data, the method distinguishes changes in the balance between copies from overall changes in expression. [4]
A related collaboration investigated barriers to hybrid seed development. Our 2021 study connected cross-direction-dependent seed failure with abnormal endosperm development and divergent epigenetic and imprinting states, helping explain why some combinations of parental genomes fail early in development. [5]
Why mobile DNA varies among individuals
Transposable elements can copy or move within genomes. In work with Ronald Smith and Puzey, I investigated why their abundance varies so widely among individuals. Data from monkeyflowers and fruit flies showed overdispersion: the variance in element counts greatly exceeded the mean.
Our 2022 study used a stochastic population-genetic model and moment analysis to examine possible explanations. Copy-and-paste proliferation, particularly when its rate approximately balances excision, provides a plausible source of the observed overdispersion. Purifying selection on total element load was unlikely to account for its magnitude in this model. Puzey and I contributed equally to the study. [6]
Selected joint publications
[1] Zheng X et al. (2021). The regulatory network for petal anthocyanin pigmentation is shaped by the MYB5a/NEGAN transcription factor in Mimulus. Genetics 217(2):iyaa036. doi:10.1093/genetics/iyaa036.
[2] Simmons ESG, Cooley AM, Puzey JR, Conradi Smith GD (2023). A multigenerational Turing model reproduces transgressive petal spot phenotypes in hybrid Mimulus. Bulletin of Mathematical Biology 85:120. doi:10.1007/s11538-023-01223-7.
[3] Edger PP et al. (2017). Subgenome dominance in an interspecific hybrid, synthetic allopolyploid, and a 140-year-old naturally established neo-allopolyploid monkeyflower. The Plant Cell 29(9):2150–2167. doi:10.1105/tpc.17.00010.
[4] Smith RD, Kinser TJ, Conradi Smith GD, Puzey JR (2019). A likelihood ratio test for changes in homeolog expression bias. BMC Bioinformatics 20:149. doi:10.1186/s12859-019-2709-5.
[5] Kinser TJ et al. (2021). Endosperm-based incompatibilities in hybrid monkeyflowers. The Plant Cell 33:2235–2257. doi:10.1093/plcell/koab117.
[6] Smith RD, Puzey JR, Conradi Smith GD (2022). Population genetics of transposable element load: a mechanistic account of observed overdispersion. PLOS ONE 17:e0270839. doi:10.1371/journal.pone.0270839.