Accelerated regulatory gene evolution in an adaptive radiation

Abstract

The disparity between rates of morphological and molecular evolution remains a key paradox in evolutionary genetics. A proposed resolution to this paradox has been the conjecture that morphological evolution proceeds via diversification in regulatory loci, and that phenotypic evolution may correlate better with regulatory gene divergence. This conjecture can be tested by examining rates of regulatory gene evolution in species that display rapid morphological diversification within adaptive radiations. We have isolated homologues to the Arabidopsis APETALA3 (ASAP3͞TM6) and APETALA1 (ASAP1) floral regulatory genes and the CHLOROPHYLL A͞B BINDING PROTEIN9 (ASCAB9) photosynthetic structural gene from species in the Hawaiian silversword alliance, a premier example of plant adaptive radiation. We have compared rates of regulatory and structural gene evolution in the Hawaiian species to those in related species of North American tarweeds. Molecular evolutionary analyses indicate significant increases in nonsynonymous relative to synonymous nucleotide substitution rates in the ASAP3͞TM6 and ASAP1 regulatory genes in the rapidly evolving Hawaiian species. By contrast, no general increase is evident in neutral mutation rates for these loci in the Hawaiian species. An increase in nonsynonymous relative to synonymous nucleotide substitution rate is also evident in the ASCAB9 structural gene in the Hawaiian species, but not to the extent displayed in the regulatory loci. The significantly accelerated rates of regulatory gene evolution in the Hawaiian species may reflect the influence of allopolyploidy or of selection and adaptive divergence. The analyses suggest that accelerated rates of regulatory gene evolution may accompany rapid morphological diversification in adaptive radiations.floral regulatory loci ͉ MADS-box ͉ CAB9 ͉ Hawaiian silversword alliance R ates of morphological evolution are generally not correlated with rates of molecular evolution. This paradoxical observation was highlighted early by Wilson and coworkers (1-3), and subsequent molecular studies in species groups that have undergone recent adaptive radiations, such as African rift lake cichlids (4), columbines (5), and the Hawaiian silversword alliance (6), have documented marked incongruities in rates of morphological and molecular evolution. A proposed resolution to this paradox has been the conjecture that evolutionary changes in regulatory genes, rather than large-scale diversification in structural genes, may be responsible for interspecific variation in organismal morphologies (1)(2)(3)(7)(8)(9). This conjecture is reinforced by molecular developmental studies that indicate that dramatic shifts in organismal structure may arise from mutations at key regulatory loci (7-9). One test of this conjecture is to examine whether there is a significant acceleration in rates of regulatory gene evolution in species that display rapid morphological diversification within adaptive radiations.The Hawaiian silversword alliance (Asteraceae: Heliantheae-Madiinae) is...

Rapid sequence divergence rates in the 5 prime regulatory regions of young Drosophila melanogaster duplicate gene pairs

“…This is analogous to studies considering rates of coding sequence evolution of duplicate genes (e.g. Ohta, 1994;Lynch and Conery, 2000;Barrier et al, 2001;Conery and Lynch, 2001;Thornton and Long, 2002;Kondrashov, 2005;Kondrashov and Kondrashov, 2006). (iii) Gene expression data from microarray experiments was compiled and related to Drosophila duplicate gene divergence (c.f.…”

High Nucleotide Divergence in Developmental Regulatory Genes Contrasts With the Structural Elements of Olfactory Pathways in Caenorhabditis

“…It is therefore possible for regulatory changes to be quite important, but to still be essentially structural in nature Wagner and Lynch 2008). For example, protein evolution of regulatory genes has been associated with species radiations (Barrier et al 2001;Lawton-Rauh et al 2003) and other major morphological changes (Galant and Carroll 2002;Ronshaugen et al 2002). In addition, positive selection shaping the pattern of substitution for various transcription factor families in plants and animals (Sutton and Wilkinson 1997;Fares et al 2003;Jia et al 2003Jia et al , 2004Martinez-Castilla and Alvarez-Buylla 2003;Balakirev and Ayala 2004;Moore et al 2005) may have direct phenotypic consequences.…”

Phylogenetic relationships and the evolution of regulatory gene sequences in the parrotfishes

“…Also, it is noteworthy that the dN/dS rate ratio of dlx2 leading to the parrotfishes (0.33) is the highest of all six genes along this part of the phylogeny. An elevated level of variation in regulatory genes has often been shown to be associated with morphological diversity in plants (Aagard et al, 2006;Barrier et al, 2001). Recent exploration of skull function of labrid fishes in the context of a phylogeny has shown that the cheiline and scarine labrids are a hot-spot of structural and functional evolution in these fishes, and dlx2 is known to regulate formation of pharyngeal elements of the feeding apparatus during development (Qiu et al, 1997;Stock et al, 1996).…”

“…Many studies have used phylogenetic tools to generate evolutionary topologies of Hox genes and other regulatory loci (e.g., Kim et al, 2003;Purugganan, 1997;Santini and Bernardi, 2005;Wagner et al, 2005) yet there are few explorations of the phylogenetic utility of regulatory gene sequences in in larger, multi-locus phylogenetic analyses. Several recent examples in arthropods (Cook et al, 2001) and plants (Barrier et al, 2001;Fan et al, 2004) have shown that regulatory loci can make strong contributions to phylogenetic resolution. This work, particularly in plants, has shown that regulatory gene sequences and their protein products do not necessarily evolve more slowly than structural genes, and in fact may evolve significantly faster (Barrier et al, 2001).…”

“…Several recent examples in arthropods (Cook et al, 2001) and plants (Barrier et al, 2001;Fan et al, 2004) have shown that regulatory loci can make strong contributions to phylogenetic resolution. This work, particularly in plants, has shown that regulatory gene sequences and their protein products do not necessarily evolve more slowly than structural genes, and in fact may evolve significantly faster (Barrier et al, 2001).…”