3. Consequences of Plant Asexual Reproduction

Sex is the dominant mode of reproduction among eukaryotic life, but why sex prevails over asexual reproduction is a long-standing and as of yet unresolved problem in biology. This problem exists because an abundance of theory shows that sexual reproduction can be costly and asexual reproduction can be advantageous in many circumstances. Despite substantial theory addressing this problem, there is little empirical research. We have tried to provide some of the first empirical tests of long-standing theory on the evolution of sex using plants as a model.
The plant genus Oenothera exhibits multiple transitions between sexual and functionally asexual reproduction. In a comparative phylogenetics context we have sought to answer the questions below.

How does asexual reproduction affect speciation and extinction dynamics? Despite some advantages, most evolutionary biologists believe that asexual reproduction is an evolutionary dead-end, and that once sex is lost it cannot be regained. Using recently developed phylogenetic methods, we showed that asexual reproduction in Oenothera is in fact associated with higher rates of speciation and no clear difference in extinction rates (see Johnson et al 2011 Evolution).

What are the phenotypic and molecular evolutionary consequences of sexual and asexual reproduction? Many of the theoretical predictions relating to the costs and benefits of sexual and asexual reproduction make explicit predictions about molecular evolution. Specifically, it is expected that asexual lineages will accumulate deleterious mutations while sexual populations will exhibit faster rates of adaptive molecular evolution. In collaboration with a former PDF (Erika Hersch-Green) and lab manager (Henrietta Myburg), we recently provided evidence in support of these predictions (see Hersch-Green et al. 2012 J Evol Biol). We found that sexual Oenothera lineages exhibit positive selection for the defense protein chitinase, whereas asexual lineages never showed any evidence of positive selection. We extended upon this work to examine molecular evolution in multiple enzymes involved in the production of flavonoid-based chemical defenses. This study found no difference between sexual and asexual lineages in positive selection, but asexual lineages exhibited relaxed purifying selection compared to sexual lineages, which is consistent with the accumulation of deleterious mutations.

In collaboration with PDF Jesse Hollister, Prof. Stephen Wright (EEB, UofT), and a Dr. Stephan Greiner (Max Planck for Molecular Plant Physiology, Golm, Germany), we are expanding this work to understand the evolutionary genomic consequences of plant sexual reproduction. We sequenced the leaf transcriptomes of 30 Oenothera species and multiple populations within some species using RNA-Seq on the Illumina Hi-Seq platform. We also sequenced the entire nuclear genome of one species to serve as a genomic reference. Our assemblies of the transcriptomes identified >20,000 unique transcripts for most species.Our next steps are to examine the population genomic consequences of sex, and to model the demographic histories of sexual and asexual species. We will also test for differences in positive and purifying selection between sexual and asexual lineages for all orthologs (~4000) that align across the phylogenetic tree.

Ph.D. student Ryan Godfrey is extending on some of this work to examine how a loss of sex in Oenothera affects quantitative genetic variation in ecologically important plant traits, as well as genome-wide patterns of population genetic variation in multiple sexual and functional asexual species.

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