Molecular Evolution and Population Genetics of Duplicated Floral Regulatory Genes

Abstract

Duplicated genes are the building blocks for the origin and diversification of gene families and may play a pivotal role in organismal diversity. Many regulatory genes involved in key developmental pathways are derived from gene duplications and divergence processes underlying gene family expansion. Thus, studies of duplicated genes shed light on genome evolution, the origin and diversification of gene families, and the potential adaptive significance of gene duplications. This dissertation research examined the molecular evolution and population genetics of duplicated floral regulatory genes in two plant systems:Arabidopsis and the allopolyploid Hawaiian silversword alliance adaptive radiation.

In the Arabidopsis system, the molecular evolution of the ancestral APETALA3/PISTILLATA gene duplication and the more recent (within Brassicaceae) APETALA1 CAULIFLOWER duplication was analyzed among four taxonomic levels: between sibling Arabidopsis species (A. thaliana and A. lyrata), among several Brassicaceae species, and among distantly related species from two different plant families (Antirrhinum majus from Scrophulariaceae and Silene latifolia from Caryophyllaceae). Examination of all four loci uncovered contrasting dynamics of molecular evolution between these two sets of paralogous regulatory genes. The CAULIFLOWER (CAL) locus is evolving at a significantly faster rate than its paralog APETALA1 (AP1) and significant differences in substitional distributions exist along these genes, reflecting the possible adaptive differentiation of CAL from AP1. The APETALA3/PISTILLATA paralog pair does not have detectable differences in patterns of substitution. Taken together, these results suggest that altered rates and patterns of sequence evolution may lead to divergence in developmental functions of some paralogous regulatory genes.

In the Hawaiian silversword alliance, the molecular population genetics of duplicated APETALA1 and APETALA3/TM6 orthologs was investigated in three species from different Hawaiian sublineages (Argyroxiphium sandwicense, Dubautia ciliolata, and Dubautia arborea). Comparisons of these duplicated orthologs (ASAPETALA1-A, ASAPETALA1-B and ASAPETALA3/TM6-A, ASAPETALA3/TM6-B) in A. sandwicense and D. ciliolata indicate that two regulatory gene homoeologs (ASAP1-A and ASAP1-B) appear to be evolving in a similar fashion while the other two homoeologs (ASAP3/TM6-A and ASAP3/TM6-B) have patterns of nucleotide diversity consistent with divergent evolutionary trajectories. This divergent evolution between two homoeologous regulatory genes suggests that selection may be partitioning the functional trajectories of these two gene copies.

A multilocus study of six genes (ASAP1-A, ASAP1-B, ASAP3/TM6-A, ASAP3/TM6-B, ASCAB9 and ASNAD1) among all three Hawaiian silversword alliance species was also conducted. This study compared morphological divergence between two recently derived sibling species (Dubautia ciliolata and D. arborea) to the genetic divergence across six genes. These two species differ significantly in morphology; yet have a genetic distance similar to levels expected between intraspecific populations. The extent of genetic divergence and historical demographics of diversification was also examined among all three species. Haplotype divergence, likelihood ratio tests of exponential growth rate, and Bayesian coalescent simulations of migration and divergence across these genes suggest demographic patterns associated with the evolution of these adaptively-radiating species.