Genome duplication

Adaptation to the Internal Environment:  Whole Genome Duplication in 3 species complexes

Perhaps the most radical mutation is the duplication of an entire set of chromosomes. Sudden doubling of the genome presents novel dynamics to the confined environment of the nucleus. How is such a jolt to nuclear organization dealt with? How do highly conserved, critical 'housekeeping' processes adapt quickly, and what are the molecular evolutionary consequences?  

To address this, we are scanning the genomes of young polyploid lineages for molecular signatures of selection by applying genome resequencing at the population level. Numerous unrelated instances of recent whole genome duplication exist in nature, presenting many independent origins of autopolyploid species (formed by doubling of the ancestral genome) and allopolyploid species (formed by hybridization of closely related genomes, followed by doubling). 

Arabidopsis arenosa- In our first genome scan of 24 resequenced Arabidopsis arenosa diploids and autopolyploids we see key players in the meiotic synaptonemal complex exhibiting clear signatures of selection (sample loci in figure to the right). These molecules directly interact with one another in early meiosis and are involved in the pairing of homologous chromosomes during the ordered dance of chromosome segregation. Our working hypothesis is that evolution of these proteins mediates a reduction in chiasmata in autotetraploids, thus reducing entanglements between members of the increased chromosomal complement.

Mimulus and Chamerion- Having detected clear signatures of natural selection in physically interacting meiosis genes in one species, I am very curious whether this is a common solution to genomic upheaval. Therefore we are concentrating my work now on focused genome scans in the Mimulus and Chamerion (Fireweed) genera, both long established ecological models. The Mimulus genus offers the added benefit of harboring young allopolyploid lineages whose genomes can be directly compared to autopolyploids with common parent species, allowing us to ask, for example: do autopolyploids and allopolyploids adapt to genome doubling in similar ways or do they come up with distinct solutions to contrasting challenges? The latest Mimulus and Chamerion population resequencing genome scans are providing some clear parallels to the Arenosa study, but also surprising differences, suggesting fruitful inroads for detailed functional analyses of the consequences of genome evolution.

The overall goal is to understand how the cell adapts to the sudden internal upheaval of genome doubling by investigating many independently evolved natural solutions. This first study has surprised us by indicating that even conserved meiotic processes are capable of nimble evolutionary shifts when required.

This work was an editor’s pick in Science

Also featured in a Current Biology dispatch

More context on my favorite collaborator's site here.

Other main collaborators on this work are: 

James Higgins (Leicester, U.K.)

Brian Husband (Guelph, Canada)

Joshua Puzey (William and Mary, U.S.A.)

Selective sweep following WGD

Above: Plots of differentiation as allele frequency differences at single nucleotide polymorphisms (black dots) between diploids and tetraploids in ASY1, ASY3 and ZYP1 on the y axis, and position along the chromosome on the x axis. Gene models are given with blue arrows, except target genes, which are indicated with bold black arrows. ZYP1 is a tandem duplicate in this genus. Middle: Mimulus. We are performing genome scans for adaptation to auto- and allopolyploidy in multiple independently genome-doubled Mimulus species. Bottom Chamerion, which we are scanning for adaptation to genome doubling. Both species have decades of excellent ecological work for us to integrate our population genomic studies in follow-up projects looking at the consequences of adaptation and gene flow across landscapes.