Gene duplications, robustness and evolutionary innovations

Abstract

Gene duplications, robustness and evolutionary innovations Gene duplications, robustness and evolutionary innovations AbstractMutational robustness facilitates evolutionary innovations. Gene duplications are unique kinds of mutations, in that they generally increase such robustness. The frequent association of gene duplications in regulatory networks with evolutionary innovation is thus a special case of a general mechanism linking innovation to robustness. The potential power of this mechanism to promote evolutionary innovations on large time scales is illustrated here with several examples. These include the role of gene duplications in the vertebrate radiation, flowering plant evolution and heart development, which encompass some of the most striking innovations in the evolution of life. Gene duplications, robustness, and evolutionary innovationsAndreas Wagner AbstractMutational robustness facilitates evolutionary innovations in biological systems. Gene duplications are unique kinds of mutations, in that they generally increase such robustness. The frequent association of gene duplications in regulatory networks with evolutionary innovation thus exemplifies a general mechanism linking innovation to robustness. I illustrate the potential power of this mechanism on large time scales with the role of gene duplications in the vertebrate radiation, flowering plant evolution, and heart development, which encompass some of the most striking innovations in the evolution of life. Mutational robustnessMutational robustness is a biological's system ability to withstand mutations. Such robustness exists on multiple levels of biological organization. A case in point are random mutagenesis experiments of various proteins. They suggest that only a small fraction of mutations affect protein function adversely. For instance, a study of the bacteriophage T4 lysozyme generated more than 2000 random amino acid changes in the protein. Only 16% of them affected lysozyme function 1 . Other examples come from regulatory gene networks, such as the molecular network specifying fruit fly segments. Such networks may tolerate much quantitative variation in interactions among network genes 2-5 . Examples at the highest level of organization include macroscopic traits. Even substantial genetic variation -ultimately caused by mutations -may leave such traits unchanged. Take the vulva of the nematode worms Caenorhabditis elegans and Pristionchus pacificus 6 . These organisms shared a common ancestor 200-300 million years ago. Their vulvae are very similar, yet the genetic and cellular networks producing them have diverged greatly. For example, whereas in C. elegans one specific cell -the anchor cell -induces vulva development, multiple gonadal cells are responsible for this induction in P. pacificus 7 . Similarly, the same key signaling molecules, such as Wnt, may play a positive role in the network for vulval induction in C. elegans, but a negative role in P. pacificus 8,9 . In sum, mutational robustness is everywhere, from proteins to or...

Evolution of Double Positive Autoregulatory Feedback Loops in CYCLOIDEA2 Clade Genes Is Associated with the Origin of Floral Zygomorphy

“…Given that the same CYC binding sites are found in the zygomorphic lineages of both Asterids and Rosids, with no such site detected in their respective ancestral actinomorphic lineages, and the establishment of floral zygomorphy frequently involves the dorsal-specific activities of a pair of CYC2 genes, we suggest that the double positive autoregulatory feedback loops revealed in Lamiales might have become established independently in the Asterids and Rosids, in accordance with the independent origins of several major zygomorphic lineages in the core eudicots (Donoghue et al, 1998;Cubas, 2004;Jabbour et al, 2009). A growing amount of evidence shows that many polyploids experience extensive and rapid genomic alterations even within the first few generations, and changes in the architecture of gene regulatory networks and in particular functional changes within cis-regulatory elements are frequently associated with evolutionary innovations (Adams and Wendel, 2005;Moore and Purugganan, 2005;Soltis, 2005;Prud'homme et al, 2006Prud'homme et al, , 2007Wagner, 2008). Therefore, this neofunctionalization (i.e., the double positive autoregulatory feedback loops underlain by a key regulatory change in CYC2 clade genes) might have been subsequent to the second WGD event in angiosperms that provided novel opportunities for the evolutionary success of the core eudicots.…”

Survival and innovation: The role of mutational robustness in evolution

“…Support to the generation of neutral genotypic diversity after gene duplication comes from the classic belief that after duplication gene copies suffer relaxed selective constraints that allow one or both copies tolerating many-fold more mutations than otherwise, a fact with extensive experimental and theoretical support [2,86,87]. This phenomenon is more obvious when analyzing genomes populated with duplicates originated by whole-genome duplication, in which younger duplicates still preserve signatures of their larger tolerance to mutations than older duplicates [79,84,88,89].…”

Neutralism and selectionism: a network-based reconciliation

“…For example, shortly after a duplication, the ratio of amino acid replacement to silent nucleotide changes is greatly elevated in duplicate genes 40,41 . Gene and genome duplications have been associated with some of the most striking evolutionary innovations in life's history, such as the diversification of the vertebrate body plan, the radiation of flowering plants, and the evolution of highly integrated organs, such as the four-chambered mammalian heart [42][43][44][45] . This association, although circumstantial, is fully consistent with the notion that the increased potential for neutral change caused by gene duplication facilitates evolutionary adaptation 46 .…”