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Behavior and the Dynamic Genome Alison M. Bell, et al. Science 332, 1161 (2011); DOI: 10.1126/science.1203295 This copy is for your personal, non-commercial use only. If you wish to distribute this article to others, you can order high-quality copies for your colleagues, clients, or customers by clicking here. Permission to republish or repurpose articles or portions of articles can be obtained by following the guidelines here. The following resources related to this article are available online at www.sciencemag.org (this infomation is current as of June 6, 2011 ): Updated information and services, including high-resolution figures, can be found in the online version of this article at: http://www.sciencemag.org/content/332/6034/1161.full.html This article cites 17 articles, 7 of which can be accessed free: http://www.sciencemag.org/content/332/6034/1161.full.html#ref-list-1 on June 6, 2011 This article appears in the following subject collections: Genetics http://www.sciencemag.org/cgi/collection/genetics www.sciencemag.org Downloaded from Science (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright 2011 by the American Association for the Advancement of Science; all rights reserved. The title Science is a registered trademark of AAAS. PERSPECTIVES with the type of epistasis found among adap- whether experiments in simple environments, epistasis has been implicated in the evolu- tive mutations within a single protein ( 11). with only one or a few niches for coexisting tion of drug resistance in infl uenza viruses Notably, Weinreich et al. studied mutations strains, will refl ect the pattern of adaptation in ( 12) and in bacterial pathogens ( 13). Ulti- in an antibiotic resistance gene, β-lactamase, more complex ecologies, such as Pseudomo- mately, populations of bacteria tediously and found a prevalence of sign epistasis, nas fl uorescens in structured environments propagated in the lab may be key to predict- which limits the number of genetic paths ( 6). Nonetheless, the compelling consistency ing the next moves of the most mutable and that evolution can follow (11 ). In contrast, between these two studies should inspire dangerous human pathogens. the epistasis documented by Khan et al. and efforts to test the generality of their fi ndings, Chou et al. exerts less constraint on the order by measuring epistasis in a wide range of References 1. A. I. Khan, D. M. Dinh, D. Schneider, R. E. Lenski, T. F. of substitutions that increase fi tness, so that experimental and even natural systems. Cooper, Science 332, 1193 (2011). the specifi c path that evolution will take is These studies, and the long-term labora- 2. H.-H. Chou, H.-C. Chiu, N. F. Delaney, D. Segrè, C. J. less predictable. At the same time, the preva- tory evolution experiments from which they Marx, Science 332, 1190 (2011). lence of antagonistic epistasis measured by derive, represent a resounding achievement 3. S. F. Elena, R. E. Lenski, Nat. Rev. Genet. 4, 457 (2003). 4. P. D. Sniegowski, P. J. Gerrish, R. E. Lenski, Nature 387, the two groups ensures a predictable tempo for the reductionist approach to studying 703 (1997). of adaptation characterized by diminishing biology. The mechanistic picture they paint 5. Z. D. Blount, C. Z. Borland, R. E. Lenski, Proc. Natl. Acad. marginal returns ( 10). of evolution is complex but not incompre- Sci. U.S.A. 105, 7899 (2008). 6. P. B. Rainey, M. Travisano, Nature 394, 69 (1998). Although these new experiments suggest hensible; although epistatic interactions lead 7. R. J. Woods et al., Science 331, 1433 (2011). a consistent principle of how epistasis shapes to surprising phenomena, the advantages 8. A. S. Kondrashov, Nature 336, 435 (1988). the pattern of adaptation, many questions of a frozen “fossil record” of laboratory- 9. G. P. Wagner, L. Altenberg, Evolution 50, 967 (1996). 10. S. Kryazhimskiy, G. Tkačik, J. B. Plotkin, Proc. Natl. Acad. must be answered before their results can raised isolates, and the ease of manipulat- Sci. U.S.A. 106, 18638 (2009). be extended to evolution outside the labora- ing—and, now, fully sequencing—evolved 11. D. M. Weinreich, N. F. Delaney, M. A. Depristo, D. L. tory. It remains unclear, for instance, whether strains enables researchers to tease apart and Hartl, Science 312, 111 (2006). 12. J. D. Bloom, L. I. Gong, D. Baltimore, Science 328, 1272 these results would be altered by changing examine the underlying causes of these phe- (2010). 13. S. Trindade et al., PLoS Genet. 5, e1000578 (2009). fundamental evolutionary parameters, such nomena. Moreover, the theory and concepts on June 6, 2011 as population size, rate of mutation, and rate developed to explain these simple experi- of recombination. Likewise, it is unclear ments may have broad payoffs. Already, 10.1126/science.1208072 GENOMICS Does behavior evolve through gene expression Behavior and the Dynamic Genome changes in the brain in response to the environment? www.sciencemag.org Alison M. Bell 1, 3 and Gene E. Robinson 2 ,3 hen circumstances change, an ples ( 3), the latter as a driver of behavioral over both physiological and evolutionary organism’s fi rst response is often evolution has never been widely accepted, time scales, provide a possible mechanism W behavioral. But how does adap- perhaps as a reaction against Lamarckian- for how behavioral plasticity might drive tive behavior evolve, given that it requires ism—the idea that characteristics acquired rapid behavioral evolution through changes constant and often instantaneous interac- by habit, use, or disuse can be passed on in gene regulation. In an environment with Downloaded from tions between an individual and its environ- across generations. However, behavioral more predators, colonies producing more ment? The dominant view emphasizes new genetics and genomics, especially for ani- bees with lower thresholds for responding random DNA mutation as the starting point. mals in natural populations, lend some plau- to alarm pheromone would have fared bet- This may lead to behavioral variation. If sibility to the phenotypic plasticity view. ter, which would then result in a popula- the resulting variants have different fi tness The ability to analyze genome-wide gene tion with patterns of gene expression whose values, then natural selection could result expression through “transcriptomics” has output was an “aroused” behavior, even in in behavioral evolution through changes in shown that the genome responds dynami- the absence of alarm pheromone. Although allele frequencies across generations. An cally to stimuli ( 4). One illustrative exam- this view does not rule out the possibility alternative theory proposes environmentally ple is the honey bee. The African honey bee that these differences in aggression arose induced change in an organism’s behavior as (Apis mellifera scutellata) responds much through new mutation, the transcriptomics the starting point ( 1), and “phenotypic plas- more fi ercely when its hive is attacked than agrees with the idea of “genetic accommo- ticity” that is inherited across generations do other subspecies of honey bee. Evolu- dation” (3 ), the modern, more inclusive ver- through an unspecifi ed process of “genetic tionary changes in brain gene expression sion of genetic assimilation, which could assimilation” ( 2). Despite numerous exam- may have resulted in an increase in respon- involve either evolutionary increases or siveness to alarm pheromone (the chemical decreases in plasticity. In certain environ- 1Department of Animal Biology, University of Illinois, bees use to alert each other to danger) for ments, plastic genotypes might be favored, Urbana-Champaign, IL 61801, USA. 2Department of Ento- African honey bees ( 5). About 10% of the but in other environments, nonplastic gen- mology, University of Illinois, Urbana-Champaign, IL 61801, same genes regulated in the brain by alarm otypes might be preferred instead. Future 3 USA. Neuroscience Program, Program in Ecology, Evolution- pheromone are also differentially expressed studies will determine whether differences ary Biology and Conservation, Institute for Genomic Biology, University of Illinois, Urbana-Champaign, IL 61801, USA. between African and the less aggressive in honey bee aggression can be explained E-mail: [email protected] European honey bees. These genes, acting by selection on regulatory regions of the www.sciencemag.org SCIENCE VOL 332 3 JUNE 2011 1161 Published by AAAS PERSPECTIVES Behavioral evolution. Male dung beetles with horns (left) fi ght for mates, whereas horn- less males (right) sneak copula- tions. The morphs show different patterns of gene expression in developing brain tissue. Genes that are differentially expressed between these two morphs have diverged among species. genome, epigenetic (chemical) modifica- Transcriptomics and analysis of genetic can be expected for the relationship between tions to the genome, or both. variation may reveal whether genes linked gene expression and genetic variation, Genes that are responsive over differ- to phenotypic plasticity and behavior are including cryptic genetic variation, which ent time scales also may be involved in the common or rare; epigenomics can explain does not influence the phenotype unless evolution of animal personality (6 ). For how they might go from inducible to con- there is a change in the environment (18 ). example, after the retreat of the glaciers stitutively expressed; and molecular systems With the imminent sequencing of genomes during the early Holocene ~12,000 years biology can identify their positions in regu- of thousands of species, as well as thousands ago, marine stickleback fi sh (Gasterosteus latory networks (12 ). These kinds of genes of individuals of the same species, there will aculeatus) invaded new freshwater environ- might be used repeatedly in evolution to be ample new evidence to test these ideas, on June 6, 2011 ments fi lled with predators they had never build the circuits and systems underlying but with a twist.