Convergence, constraint and the role of gene expression during adaptive radiation: floral anthocyanins in Aquilegia

Abstract

Convergent phenotypes are testament to the role of natural selection in evolution. However, little is known about whether convergence in phenotype extends to convergence at the molecular level. We use the independent losses of floral anthocyanins in columbines (Aquilegia) to determine the degree of molecular convergence in gene expression across the anthocyanin biosynthetic pathway (ABP). Using a phylogeny of the North American Aquilegia clade, we inferred six independent losses of floral anthocyanins. Via semiquantitative reverse transcriptase-polymerase chain reaction (RT-PCR), we monitored developmental and tissue-specific variation in expression of the six major structural ABP loci in three Aquilegia species, two that produce anthocyanins (A+) and one that does not (A-). We then compared ABP expression in petals of old-bud and pre-anthesis flowers of 13 Aquilegia species, eight wild species and two horticultural lines representing seven independent A- lineages as well as three wild A+ species. We only found evidence of down-regulation of ABP loci in A- lineages and losses of expression were significantly more prevalent for genes late in the pathway. Independent contrast analysis indicates that changes in expression of dihydroflavonol reductase (DFR) and anthocyanidin synthase (ANS) are strongly phylogenetically correlated consistent with the multilocus targets of trans-regulatory elements in the ABP of other systems. Our findings strongly suggest that pleiotropy constrains the evolution of loss of floral anthocyanins to mutations affecting genes late in the ABP mostly through convergent changes in regulatory genes. These patterns support the hypothesis that rapid evolutionary change occurs largely through regulatory rather than structural mutations.

Adaptive Radiation, Ecological Opportunity, and Evolutionary Determinism

“…As a result, when species from such clades experience the same selective conditions, they may adapt in genetically and developmentally similar ways (Haldane 1932;Gould 2002;Hoekstra 2006). Recent studies have provided many examples in which parallel phenotypic change in closely related species (or populations of the same species) is caused by similar genetic changes in a wide range of organisms and traits (e.g., Sucena et al 2003;Colosimo et al 2005;Hoekstra et al 2006;Protas et al 2006;Shapiro et al 2006;Whittall et al 2006;Baxter et al 2008;Gross et al 2009;Chan et al 2010; of course, this is not always the case: sometimes convergent phenotypic evolution is accomplished by different genetic changes, even in closely related species [e.g., Hoekstra and Nachman 2003;Wittkopp et al 2003;Hoekstra et al 2006;Kingsley et al 2009] Bossuyt and Milinkovitch 2000;Ruedi and Mayer 2001;Stadelmann et al 2007), and the examples that have been suggested require further examination to assess the extent of species-forspecies matching (Losos 2009). Radiations occurring on different continents usually will be accomplished by distantly related clades that are, for reasons just discussed, likely to diversify in different ways (Pianka 1986;Cadle and Greene 1993;Losos 1994).…”

Morning glory as a powerful model in ecological genomics: tracing adaptation through both natural and artificial selection

“…Investigations in Ipomoea, as well as in Petunia, Antirrhinum and Mimulus, have all revealed that genetic changes associated with this transition are also regulatory, involving modification of transcription factors rather than enzyme-coding genes (Quattrocchio et al, 1999;Durbin et al, 2003;Schwinn et al, 2006;Whittall et al, 2006). The pattern of transcription factor mutations contrasts with that of spontaneous mutations, approximately half of which involve functional inactivation of enzyme-coding genes (Streisfeld and Rausher, 2011).…”

Extrapolating from local ecological processes to genus-wide patterns in colour polymorphism in South AfricanProtea

“…Our study is not the first, however, to document distribution of floral colour polymorphism and monomorphism across several plant species. Published estimates range from 22% of species from a clade within Aquilegia (from [58]) and 36% of species in Polemoniaceae [9]. Other studies of cross-species patterns take an approach different from the one used here but still point to divergent selection as favouring pigment polymorphism [e.g.…”

“…Second, evolutionary transitions between pink and white may not occur at equal rates. Based on phylogenetic comparisons in a few well-studied lineages, floral anthocyanins are more likely to be lost within a lineage than to be gained [58,73]. Similarly, monomorphism should be easier to evolve from polymorphism than the inverse [12].…”