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Gene Expression and the Evolution of Behavioral Plasticity

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Gene Expression and the Evolution of Behavioral Plasticity Copyright C Blackwell Munksgaard 2002 Genes, Brain and Behavior 2002; 1: 197–203 Blackwell Munksgaard ISSN 1601-1848 Commentary Social behavior and comparative genomics: new genes or new gene regulation? G. E. Robinson*,† and Y. Ben-Shahar* nematode Caenorhabditis elegans (de Bono & Bargmann 1998), but also in several organisms used as models for be- *Department of Entomology and †Neuroscience Program, havioral analysis: voles (reviewed by Insel & Young 2000), University of Illinois at Urbana-Champaign, Urbana, USA birds (reviewed by Clayton 2000b), fish (Hofmann & Fernald 2000), crayfish (Spitzer et al. 2001), ants (Krieger & Ross Corresponding author: Gene E. Robinson, Department of Ento- 2002), and bees (reviewed by Robinson 2002b). mology, University of Illinois at Urbana-Champaign, 320 Morrill Hall, 505 S. Goodwin Avenue, Urbana, IL 61801, USA. E-mail: A number of factors, including the following three, contrib- [email protected] ute to the diversity of models used to study genes and social behavior. First, employing Drosophila and C.elegans in this Molecular analyses of social behavior are distinguished context has, until now, been limited to studies of elemental by the use of an unusually broad array of animal social behaviors; mating behavior (Greenspan & Ferveur models. This is advantageous for a number of reasons, including the opportunity for comparative genomic 2000) and aggregation during feeding (de Bono & Bargmann analyses that address fundamental issues in the mol- 1998). Mating is the only activity in Drosophila known to ecular biology of social behavior. One issue relates to involve structured interactions with conspecifics (but see the kinds of changes in genome structure and function Chen et al. 2002), however, mating does not distinguish so- that occur to give rise to social behavior. This paper cial animals from most others, and is not featured promi- considers one aspect of this issue, whether social evo- nently in the authoritative Sociobiology (Wilson 1975). lution involves new genes, new gene regulation, or A second factor contributing to the diversity of models both. This is accomplished by briefly reviewing find- used to study genes and social behavior is that while power- ings from studies of the fish Haplochromis burtoni, the ful studies of social behavior can be performed in the labora- vole Microtus ochrogaster, and the honey bee Apis tory (Pfaff 1999), there is keen interest in understanding the mellifera, with a more detailed and prospective con- sideration of the honey bee. molecular machinery of social behavior in natural contexts (Jarvis et al. 1997). Studies conducted under ecologically rel- evant conditions make it easier to interpret molecular data Keywords: brain, gene regulation, GnRH, Haplochromis bur- within a broad integrative framework that includes both toni, honey bee, PKG, social behavior, sociogenomics, vaso- mechanistic and evolutionary perspectives (Wilson 1975; pressin, vole Robinson 1999; Robinson et al. 1999; Miklos & Maleszka Received 06 July 2002, revised 21 July 2002, accepted for 2000). publication 21 July 2002 A third factor contributing to the diversity of models used to study genes and social behavior is the diversity of social behavior itself. There are many types of social behaviors, ex- hibited by species that differ dramatically in their level of A major goal in the brain and behavioral sciences is to identify sociality. There are solitary species that interact with conspe- genes that influence social behavior and understand how cifics only when mating, and species that live in highly struc- their protein products influence the structure and function of tured societies with complex social lives in which nearly all the nervous system. Other forms of behavior studied at the activities are influenced by interactions with conspecifics. molecular level, such as learning (Dubnau & Tully 2001) and Sociality, a term used to describe such all-encompassing so- circadian rhythms (Panda et al. 2002), have focused mostly cial life, is highly derived and has evolved independently in on the traditional model organisms used for genetic analysis, many lineages of animals (Wilson 1975), providing diverse the fruit fly Drosophila melanogaster and the mouse Mus social systems for molecular analysis. Studying the most ex- musculus (a notable exception in learning studies is the use treme manifestations of social behavior, exhibited by animals of Aplysia californica (Kandel 2001)). Molecular analyses of living in complex societies, provides experimental access to social behavior, in contrast, involve a veritable menagerie. a process that is undoubtedly involved in all forms of social Genes related to social behavior have been studied in flies behavior, social regulation of gene expression. Studying di- (Greenspan & Ferveur 2000), mice (Pfaff 1999), and the verse animal societies also allows for analysis, in molecular 197 Robinson and Ben-Shahar terms, of the roles of convergence and conservation in social there are differences between humans and chimpanzees in evolution. the sequence of FOXP2 (Enard et al. 2002b), a gene impli- It is reasonable to assume that the evolution of social be- cated in human speech, while another study found evidence havior acted, in part, on conserved mechanisms that control for a gene (Neu5Gc) lacking in the human genome but pres- responses to stimuli in the environment. Social cues, like ent in other animals, including chimpanzees (Chou et al. other environmental cues, convey information critical for ani- 2002). These results suggest that evolution affecting protein mal survival and reproduction. The basics of how individuals coding sequences can have profound effects on social evolu- respond to their environment are similar in vertebrates and tion. invertebrates and involve sensory structures, signal transduc- Britten & Davidson (1971) and King & Wilson (1975) first tion cascades, and various forms of neural plasticity (Harris- suggested in general notion that changes in gene regulation, Warrick 2000; Kandel et al. 2000). Genes involved in orches- rather than gene sequences, can cause evolutionary novelty. trating the perception and processing of sensory information Evidence supporting this idea has recently been presented and the responses that are then triggered are thus likely to by Enard et al. (2002a), who reported results from cDNA figure prominently in social evolution. However, our under- microarrays made from human sequences that suggest that standing of social evolution is limited by the fact that the there are large differences between humans and chimpan- identification of genes involved in social behavior is still in the zees in patterns of gene expression in the brain. Given that early phases and no general principles have yet emerged. human and chimpanzee genomes are around 99% identical Compelling as they are as exemplars of social behavior, the (see Enard et al. 2002a), these findings highlight the possi- animals mentioned above, which are used as model behav- bility that similar genomes can produce different nervous sys- ioral systems, will never rival fruit flies and mice as engines tems with different bahavioral repertoires. With an estimated of gene discovery (Sokolowski 2001; Bucan & Abel 2002), 6 million years of divergence between humans and chimpan- at least in terms of elucidating basic molecular functions. zees (Hacia 2001), these results also suggest that evolution- However, using diverse animal species, in addition to being ary effects on brain transcriptomes can be relatively rapid. advantageous for the reasons mentioned above, also pro- We address the issue of whether social evolution involves vides the opportunity for comparative genomic analyses that new genes, new gene regulation, or both, by briefly review- address fundamental issues in the molecular biology of social ing findings from the fish Haplochromis burtoni, the vole behavior. One issue relates to the kinds of changes in ge- Microtus ochrogaster, and the honey bee Apis mellifera, with nome structure and function that occur to give rise to social a more detailed and prospective consideration of the honey behavior. This paper deals with one aspect of this issue: is bee. The same three systems were reviewed earlier the evolution of social behavior associated with the evolution (Robinson 1999), but from a more ecological perspective. of genes with new functions, genes that are regulated in new ways, or both? Harris-Warrick, (2000) discusses a larger set of evolution- GnRH genes and dominance behavior in fish ary changes in the structure and localization of molecules in the nervous system that can influence behavior: (1) gene Dominance in the African teleost (Astatotilapia) Haploch- duplication and diversification that results in protein coding romis burtoni provides an example of the evolution of a so- sequence; (2) changes in gene regulation that influence pro- cial behavior that is associated with gene diversification and tein abundance; (3) changes in gene regulation that influ- modification of sequence. H.burtoni has two forms of males. ence spatial patterns of gene expression; (4) changes in Dominant males, aggressively territorial, brightly colored and, gene regulation that influence the complement of neuro- with high levels of circulating testosterone, enjoy high levels transmitters released from single neurons; (5) changes in of reproductive success. Subordinate males, lacking all these patterns of alternative splicing; and (6) changes in neuromo- attributes, do not (reviewed
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