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Evolving Specialization of the Arthropod Nervous System

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Evolving Specialization of the Arthropod Nervous System Evolving specialization of the arthropod nervous system Erin Jarvisa, Heather S. Bruceb, and Nipam H. Patela,b,1 aDepartment of Integrative Biology, University of California, Berkeley, CA 94720-3140; and bDepartment of Molecular Cell Biology, Center for Integrative Genomics, University of California, Berkeley, CA 94720-3200 Edited by John C. Avise, University of California, Irvine, CA, and approved May 11, 2012 (received for review March 23, 2012) The diverse array of body plans possessed by arthropods is created studies revealed a remarkable level of evolutionary conservation by generating variations upon a design of repeated segments of these Hox gene transcription factors, and it appears that Hox formed during development, using a relatively small “toolbox” genes play a well-conserved role in patterning regional identity of conserved patterning genes. These attributes make the arthro- along the antero-posterior axis in all bilaterian animals. pod body plan a valuable model for elucidating how changes in Whereas Hox genes have provided developmental biologists development create diversity of form. As increasingly specialized with an outstanding example of a deeply conserved mechanism segments and appendages evolved in arthropods, the nervous of pattern formation, changes in these genes have also been systems of these animals also evolved to control the function of implicated in the evolutionary process that has led to the di- these structures. Although there is a remarkable degree of conser- versification of body plans both between and within animal vation in neural development both between individual segments phyla. For example, comparisons of Hox gene expression and in any given species and between the nervous systems of different function within the various groups of arthropods led to a number arthropod groups, the differences that do exist are informative of hypotheses regarding the possible role of these genes in for inferring general principles about the holistic evolution of body the evolution of the arthropod body plan (reviewed in ref. 2). plans. This review describes developmental processes control- Indeed, work on Hox genes played a key role in the renaissance ling neural segmentation and regionalization, highlighting seg- of evolutionary developmental biology (“evo-devo”) during the mentation mechanisms that create both ectodermal and neural past 30 years. segments, as well as recent studies of the role of Hox genes in One example of the potential role of Hox genes in mor- generating regional specification within the central nervous sys- phological evolution comes from work on Ultrabithorax (Ubx) tem. We argue that this system generates a modular design that in crustaceans. In this case, changes in the expression pattern allows the nervous system to evolve in concert with the body seg- of Ubx are associated with the evolution of a specifictypeof ments and their associated appendages. This information will be appendage, known as a maxilliped, which is a jaw-like feeding useful in future studies of macroevolutionary changes in arthropod appendage that is part of the anterior thorax. Depending on body plans, especially in understanding how these transformations the species, crustaceans possess anywhere from zero to three can be made in a way that retains the function of appendages pairs of maxillipeds, and, as illustrated in Fig. 2, the point of during evolutionary transitions in morphology. transition from maxilliped-bearing segments to more posterior thoracic-type segments (usually used for locomotion) is corre- he phylum Arthropoda derives its name from the Greek lated with the boundary of Ubx expression (3). This relationship Twords for “joint” and “foot” (or “leg”), and the remarkable between Ubx and the evolution of body patterning was moved functional diversity of these arthropod appendages has contrib- beyond correlation with functional studies in the amphipod uted to the notable evolutionary success of this animal group. crustacean, Parhyale hawaiensis. A combination of misexpression The basic arthropod body plan consists of serially repeated body and knockdown experiments revealed that the number of max- segments, with a pair of appendages on most of these segments. illipeds could be increased or reduced by knocking down or Individual segments (or groups of adjacent segments), along with misexpressing Ubx, respectively, in Parhyale (4, 5). The change their associated appendages, are often specialized for particular in the number of maxillipeds was not due to a change in the functions (1). These patterns of specialization vary enormously total number of appendages, but rather due to homeotic trans- between arthropod species, and this flexible, modular body plan formations altering the relative ratio of different appendage types, accounts for the superb mobility and specialized feeding mo- resembling the general pattern of differences seen between existing dalities that have enabled arthropods to fillawidevarietyof crustacean species. terrestrial and aquatic ecological niches. In turn, the great adapt- Whereas these experiments result in the striking transformation ability of arthropod body morphology may be a result of a highly of appendage morphology that mimics evolutionary transitions, coordinated patterning mechanism that uses a common regulatory reservations about the relevance of such Hox-mediated trans- network to align regional identity for the ectoderm, mesoderm, formation to the natural process of evolution still remain. Such and nervous system along the body axis. radical morphological transformations in a single step are prob- Genetic and molecular studies in the model arthropod, ably unlikely to be adaptive, but it is reasonable to consider that Drosophila melanogaster, have provided us with a detailed un- gradual morphological changes would simply require incremental derstanding of the mechanisms that subdivide the embryo into changes in the patterns and levels of Hox gene expression. segments and provide regional identity to these units. The se- quential action of maternal gradients and zygotic gap, pair-rule, This paper results from the Arthur M. Sackler Colloquium of the National Academy and segment polarity genes sequentially subdivides the embryos of Sciences, “In the Light of Evolution VI: Brain and Behavior,” held January 19–21, into smaller and smaller units, ultimately organizing the pattern 2012, at the Arnold and Mabel Beckman Center of the National Academies of Sciences of segmentation. A portion of this segmentation network also and Engineering in Irvine, CA. The complete program and audio files of most presentations regulates the expression of homeotic (Hox) genes, which provide are available on the NAS Web site at www.nasonline.org/evolution_vi. regional identity to the developing segments to make segments Author contributions: E.J., H.S.B., and N.H.P. wrote the paper. distinct from one another (Fig. 1). Altering the expression patterns The authors declare no conflict of interest. of these Hox genes leads to the transformation of one or more This article is a PNAS Direct Submission. segments toward the identity of adjacent segments. Subsequent 1To whom correspondence should be addressed. E-mail: [email protected]. 10634–10639 | PNAS | June 26, 2012 | vol. 109 | suppl. 1 www.pnas.org/cgi/doi/10.1073/pnas.1201876109 Downloaded by guest on September 29, 2021 Fig. 1. Early embryo patterning along the antero-posterior axis in Drosophila.(A) Hierarchy of maternal gradients and zygotic gap, pair-rule, and segment polarity genes establishes the repetition of segments, whereas the homeotic genes regionalize the body plan, making segments differ from one another. (B) Protein expression pattern produced by four (of the eight) Hox genes at midembryogenesis. Scr is in black, Antp in red, Ubx in blue, and Abd-B in brown. More intensely stained area in the middle is the central nervous system. Anterior is to the left in A and up in B. Indeed, some crustaceans, such as mysids, possess appendages microevolutionary changes in Hox gene regulation could occur of intermediate morphology (between a standard maxilliped over time to lead to macroevolutionary changes in morphology. and a swimming leg) that are associated with intermediate levels A more important consideration is that even gradual trans- and mosaic patterns of Ubx expression (3). Thus, it is likely that formation during evolution must occur in such a way that the appendage and associated segment remain functional and useful to the organism at each point in the transition. For this to hap- pen, more than just the external morphology of the appendage needs to be altered. Coordinated changes must also be made in the musculature and nervous system associated with the trans- forming appendage. It is reasonable to assume that the segment must evolve as a whole, with coordination between the ectoderm, mesoderm, and nervous system. We suggest that the Hox gene system functions in arthropods in a manner that facilitates such a coordinated transformation. Our purpose here is to review the manner in which the nervous system is patterned in arthropods, highlighting first that the same system used for ectodermal seg- mentation, particularly at the level of segment polarity genes, contributes to generating the segmental organization of the nervous system, and second, that Hox genes play a major role in the regionalization of the nervous system just as they do for the ectoderm. Most of the data come from studies in Drosophila, but comparative
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