Abstract
Malpighiaceae possess flowers with a unique bilateral symmetry (zygomorphy), which is a hypothesized adaptation associated with specialization on neotropical oil bee pollinators. Gene expression of two representatives of the CYC2 lineage of floral symmetry TCP genes, CYC2A and CYC2B, demarcate the adaxial (dorsal) region of the flower in the characteristic zygomorphic flowers of most Malpighiaceae. Several clades within the family, however, have independently lost their specialized oil bee pollinators and reverted to radial flowers (actinomorphy) like their ancestors. Here, we investigate CYC2 expression associated with four independent reversals to actinomorphy. We demonstrate that these reversals are always associated with alteration of the highly conserved CYC2 expression pattern observed in most New World (NW) Malpighiaceae. In NW Lasiocarpus and Old World (OW) Microsteria, the expression of CYC2-like genes has expanded to include the ventral region of the corolla. Thus, the pattern of gene expression in these species has become radialized, which is comparable to what has been reported in the radial flowered legume clade Cadia. In striking contrast, in NW Psychopterys and OW Sphedamnocarpus, CYC2-like expression is entirely absent or at barely detectable levels. This is more similar to the pattern of CYC2 expression observed in radial flowered Arabidopsis. These results collectively indicate that, regardless of geographic distribution, reversals to similar floral phenotypes in this large tropical angiosperm clade have evolved via different genetic changes from an otherwise highly conserved developmental program.
Highlights
Convergence is an evolutionary process in which similar features reoccur independently across the Tree of Life (Donoghue, 2005; Protas et al, 2006; Conway Morris, 2008; McGhee, 2011; Wake et al, 2011)
The species exhibit a loss of CYC2B function, and a strikingly similar shift in the expression of CYC2A that is coincident with their shift in floral symmetry. These results indicate that similar floral phenotypes of Old World (OW) Malpighiaceae have evolved via parallel genetic changes from an otherwise highly conserved developmental program
Our results indicate that these reversals in floral symmetry are the result of distinct modifications to the conserved New World (NW) CYC2 program, including the loss of CYC2 expression in Malagasy Sphedamnocarpus and NW Psychopterys, and the radialized expansion of expression in OW Microsteira and NW Lasiocarpus
Summary
Convergence is an evolutionary process in which similar features reoccur independently across the Tree of Life (Donoghue, 2005; Protas et al, 2006; Conway Morris, 2008; McGhee, 2011; Wake et al, 2011). These similarities are commonly thought to have arisen as a result of adaptation to similar selective pressures, rather than due to inheritance from a common ancestor. Evolutionary developmental genetics, has facilitated the characterization of several types of convergence operating at the genetic level. Studies have revealed convergence in terms of genetic change (e.g., Sucena et al, 2003; Prud’homme et al, 2006; Rosenblum et al, 2010), but in others, distinct genetic mechanisms were uncovered (e.g., Hoekstra and Nachman, 2003; Wittkopp et al, 2003; Steiner et al, 2009)
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