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Genetics of Adaptation

Wessinger, Carolyn [1], Rausher, Mark D [1].

Parallel gene breakdown in Penstemon.

Parallel evolution suggests phenotypic evolution can be highly repeatable or predictable under some circumstances, and can often involve directionally asymmetric evolutionary transitions, where shifts in one evolutionary direction frequently occur but reversals are rare. Two outstanding questions pertaining to the evolutionary genetics of parallelism are, first, under which circumstances parallel shifts are predictable at the genetic level (biased to involve certain types of mutations), and second, whether the genetic basis of parallel shifts constrains future evolutionary trajectories, in particular evolutionary reversibility. We addressed these questions by examining the genetics of flower color evolution in the wildflower genus Penstemon. In this genus, there have been as many as 21 separate evolutionary transitions from blue bee-pollinated flowers to red hummingbird-pollinated flowers, with no evidence for reversals. We characterized the genetic basis of red flowers in 13 independent origins of hummingbird-pollinated Penstemon species using a combination of enzyme function and gene expression assays on candidate anthocyanin pathway genes. We discovered that the evolution of red flowers in Penstemon is strikingly predictable at the genetic level. In this genus, a transition to red flowers requires the inactivation of two anthocyanin pathway enzymes in floral tissue: Flavonoid 3',5'-hydroxylase (F3'5'h) and Flavonoid 3'-hydroxylase (F3'h). Despite similar mutational target sizes, these enzymes have experienced strikingly different fates in red-flowered species. In at least 12 of the 13 investigated species, red flowers are accompanied by loss-of-function mutations to the coding sequence of F3'5'h; in most cases, multiple redundant inactivating mutations have accumulated. However, F3'h function is preserved in all 13 cases. Instead, F3'h has experienced floral tissue-specific downregulation in all species. This predictably different fate for these two genes is statistically significant and likely due to pleiotropic differences. In particular, F3'h is pleiotropic and stabilizing selection may be preserving its function, while F3'5'h is apparently non-pleiotropic and therefore loss-of-function mutations to this locus may be fixed without detrimental effects. Thusin Penstemon, the genetic basis of blue to red flower color shifts can be predicted by the pleiotropic roles of the genes. Furthermore, our results also provide evidence indicating that evolutionary degeneration of enzymes in the anthocyanin pathway may contribute to the asymmetry of flower color transitionsin Penstemon. In at least nine of the 12 species, redundant inactivating mutations to F3'5'h have occurred, which likely would severely limit evolutionary reversal of this phenotype, and may contribute to the observed evolutionary asymmetry in flower color.


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1 - Duke University, Biology, Box 90338, Durham, NC, 27705, USA

Keywords:
parallel evolution
Pleiotropy
flower color
Penstemon.

Presentation Type: Regular Oral Presentation
Session: 115
Location: Rendezvous A/Snowbird Center
Date: Monday, June 24th, 2013
Time: 11:45 AM
Number: 115006
Abstract ID:369
Candidate for Awards:W.D. Hamilton Award for Outstanding Student Presentation


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