Causes and evolutionary significance of genetic convergence

Department of Ecology and Evolutionary Biology, Brown University, Providence, RI 02906, USA.
Trends in Genetics (Impact Factor: 9.92). 09/2010; 26(9):400-5. DOI: 10.1016/j.tig.2010.06.005
Source: PubMed


Convergent phenotypes provide extremely valuable systems for studying the genetics of new adaptations. Accumulating studies on this topic have reported surprising cases of convergent evolution at the molecular level, ranging from gene families being recurrently recruited to identical amino acid replacements in distant lineages. Together, these different examples of genetic convergence suggest that molecular evolution is in some cases strongly constrained by a combination of limited genetic material suitable for new functions and a restricted number of substitutions that can confer specific enzymatic properties. We discuss approaches for gaining further insights into the causes of genetic convergence and their potential contribution to our understanding of how the genetic background determines the evolvability of complex organismal traits.

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Available from: Guillaume Besnard
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    • "The repeated evolution of similar phenotypes in response to similar selective pressures, or convergent evolution, is a pervasive evolutionary phenomenon (Schluter, 2000; McGhee, 2011; Futuyma, 2013). Major questions remain regarding the ecological and evolutionary causes of convergence, including whether convergent evolution most often results from selection toward optimality, or from constraints on design, genetic architecture or other contingencies (Maynard Smith et al., 1985; Wake, 1991; Brakefield, 2006; Christin et al., 2010; Losos, 2011). Examining the genetic basis of convergence provides insight into these questions, because we can assume selection is relatively unconstrained when similar phenotypes are produced through diverse genetic routes and, conversely, that constraints may be important when phenotypes are determined by a limited subset of possible genetic mechanisms (Miller et al., 2006; Weinreich et al., 2006; Gompel and Prud'homme, 2009; Losos, 2011; Conte et al., 2012; Feldman et al., 2012). "
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    ABSTRACT: Convergent evolution of tetrodotoxin (TTX) resistance, at both the phenotypic and genetic levels, characterizes coevolutionary arms races between amphibians and their snake predators around the world, and reveals remarkable predictability in the process of adaptation. Here we examine the repeatability of the evolution of TTX resistance in an undescribed predator–prey relationship between TTX-bearing Eastern Newts (Notophthalmus viridescens) and Eastern Hog-nosed Snakes (Heterodon platirhinos). We found that that local newts contain levels of TTX dangerous enough to dissuade most predators, and that Eastern Hog-nosed Snakes within newt range are highly resistant to TTX. In fact, these populations of Eastern Hog-nosed Snakes are so resistant to TTX that the potential for current reciprocal selection might be limited. Unlike all other cases of TTX resistance in vertebrates, H. platirhinos lacks the adaptive amino acid substitutions in the skeletal muscle sodium channel that reduce TTX binding, suggesting that physiological resistance in Eastern Hog-nosed Snakes is conferred by an alternate genetic mechanism. Thus, phenotypic convergence in this case is not due to parallel molecular evolution, indicating that there may be more than one way for this adaptation to arise, even among closely related species.
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    • "One of the most documented convergent phenotypes in plants is the repeated development of C 4 photosynthesis, an adaptation that uses four carbon acids to increase photosynthesis under conditions where carbon assimilation can be limited by high photorespiration (Sage et al., 2012). The number of times that C 4 independently developed (at least 66) makes it an extremely useful phenotype for analysing the genetics of adaptations (Christin et al., 2010; Sage et al., 2011). The genetic mechanisms responsible for C 4 photosynthesis remain largely unknown, but they are thought to involve coordinated changes to genes that affect leaf anatomy, cell ultrastructure , energetics, metabolite transport, and the location, content, and regulation of many metabolic enzymes (Hibberd and Covshoff, 2010). "
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    ABSTRACT: The two carboxylation reactions performed by phosphoenolpyruvate carboxylase (PEPC) and ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) are vital in the fixation of inorganic carbon for C4 plants. The abundance of PEPC is substantially elevated in C4 leaves, while the location of Rubisco is restricted to one of two chloroplast types. These differences compared with C3 leaves have been shown to result in convergent enzyme optimization in some C4 species. Investigation into the kinetic properties of PEPC and Rubisco from Kranz C4, single cell C4, and C3 species in Chenopodiaceae s. s. subfamily Suaedoideae showed that these major carboxylases in C4 Suaedoideae species lack the same mutations found in other C4 systems which have been examined; but still have similar convergent kinetic properties. Positive selection analysis on the N-terminus of PEPC identified residues 364 and 368 to be under positive selection with a posterior probability >0.99 using Bayes empirical Bayes. Compared with previous analyses on other C4 species, PEPC from C4 Suaedoideae species have different convergent amino acids that result in a higher K m for PEP and malate tolerance compared with C3 species. Kinetic analysis of Rubisco showed that C4 species have a higher catalytic efficiency of Rubisco (k catc in mol CO2 mol–1 Rubisco active sites s–1), despite lacking convergent substitutions in the rbcL gene. The importance of kinetic changes to the two-carboxylation reactions in C4 leaves related to amino acid selection is discussed.
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    • "The mutational forces that generate novel variation introduce a stochasticity that dictates the paths that adaptation can take. This juxtaposition has led to a core question about evolution – how predictable are the details of phenotypic adaptations [DePristo, et al., 2005; Weinreich et al., 2006; Stern and Orgogozo, 2008, 2009; Christin et al., 2010a]? We know that when two populations or species experience a common set of selection pressures, they often converge on the same phenotype [Losos, 1992; Joron et al., 2006; Arendt and Reznick, 2008; Rosenblum et al., 2010; Dobler et al., 2012]. "
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    ABSTRACT: Evolution typically arrives at convergent phenotypic solutions to common challenges of natural selection. However, diverse molecular and physiological mechanisms may generate phenotypes that appear similar at the organismal level. How predictable are the molecular mechanisms of adaptation that underlie adaptive convergence? Interactions between toxic prey and their predators provide an excellent avenue to investigate the question of predictability because both taxa must adapt to the presence of defensive poisons. The evolution of resistance to tetrodotoxin (TTX), which binds to and blocks voltage-gated sodium channels (NaV1) in nerves and muscle, has been remarkably parallel across deep phylogenetic divides. In both predators and prey, representing three major vertebrate groups, TTX resistance has arisen through structural changes in NaV1 proteins. Fish, amphibians and reptiles, though they differ in the total number of NaV1 paralogs in their genomes, have each evolved common amino acid substitutions in the orthologous skeletal muscle NaV1.4. Many of these substitutions involve not only the same positions in the protein, but also the identical amino acid residues. Similarly, predictable convergence is observed across the family of sodium channel genes expressed in different tissues in puffer fish and in garter snakes. Trade-offs between the fundamental role of NaV1 proteins in selective permeability of Na+ and their ability to resist binding by TTX generate a highly constrained adaptive landscape at the level of the protein.
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