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Selector Genes and the Cambrian Radiation of Bilateria (Evolutionary Constraint/Seginentation/Homeosis) DAVID K

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Selector Genes and the Cambrian Radiation of Bilateria (Evolutionary Constraint/Seginentation/Homeosis) DAVID K Proc. Natl. Acad. Sci. USA Vol. 87, pp. 4406-4410, June 1990 Evolution Selector genes and the Cambrian radiation of Bilateria (evolutionary constraint/seginentation/homeosis) DAVID K. JACOBS Department of Geological Sciences, Derring Hall, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061 Communicated by James W. Valentine, March 26, 1990 (received for review November 18, 1989) ABSTRACT There is a significantly greater post-Cam- tral serial/selector form of gene control in development; brian decline in frequency ofordinal origination among serially consequently, the same history of increased constraint in constructed Bilateria, such as arthropods, than in nonserially body-plan evolution is not expected in these groups. Evolu- constructed Bilateria. Greater decline in arthropod ordinal tion of new body plans in these nonserially organized forms origination is not predicted by ecologic, diversity-dependent did not decrease precipitously. models of decline in the production of higher taxa. Reduction Ordinal origination of serial forms peaked in the Cambrian in ordinal origination indicates increased constraint on arthro- period and descended to negligible values in the Post- pod body-plan evolution. The dispersal of selector genes in the Paleozoic era. In Bilateria lacking simple serial organization, genomes of arthropods in conjunction with the retention of a the peak in ordinal origination occurred in the Ordovician simple regulatory hierarchy in development may have caused period, and new orders continued to originate in the Post- the increased constraint seen. Increased constraint would not Paleozoic (Fig. 1). The different histories of serial and be expected in those organisms that are not serially constructed nonserial Bilateria predicted and observed here have not and presumably have not retained the simple ancestral regu- been previously recognized. Predictions of morphologic pat- latory hierarchy in development ofselector gene differentiation terns and the distribution of selector genes within organisms of serial elements. The hypothesis of differential constraint can be devised to further test this set of hypotheses. tested against the fossil record in this paper can be further tested by examination ofthe distribution ofselector genes in the Homology in Insect and Vertebrate Development genomes of arthropods. Ifgenes active in the development of divergent taxa are similar Evidence of homology in genes controlling body-plan devel- in sequence to each other and similar in their pattern of opment suggests a shared ancestry of genetic control of expression during development, then those genes probably development in highly divergent bilaterian taxa, including derived from an ancestral gene that played a similar role in the insects and vertebrates (1-6). In a phylogenetic context, development of a common ancestor of the divergent taxa. these shared features of development derive from a common Among sequence-similar genes expressed in insect and verte- ancestor in the stem ofthe bilaterian clade and evolved before brate development (and other Bilateria examined), genes that divergence of the higher metazoan groups we know today. also meet the additional criterion of similarity in pattern of The limited avenues of morphologic evolution permitted by expression include those involved in the construction of serial this ancestral form of development may have profoundly elements, such as the segments in Drosophila and the selector affected the evolution of body plans within the Bilateria. genes that differentiate serial elements. Consequently, genes In this paper, homology ofgenetic control of development involved in construction of serial elements and selector genes in insects and vertebrates is used to characterize the devel- that differentiate serial elements may have played a role in the opmental system of the shared ancestor of these Bilateria. development of the shared ancestor ofinsects and vertebrates. The inferred ancestral form ofdevelopment consists ofgenes Transcription and translation of a specific set of selector controlling construction ofserial elements along the anterior- genes in the cells of the individual segments ofDrosophila is posterior axis of the body, followed by the differentiation of responsible for the construction of the specific morphologic those serial elements through the activity of an additional set features of the segments composing the Drosophila body (7, of "selector" genes. This form ofdevelopment is here termed 8). Several lines of evidence indicate similarity of develop- serial/selector development. Selector genes of the Antenna- mental function and homology between the selector genes of pedia complex of Drosophila are used to model the likely Drosophila and sequence-similar selector genes found in limitations and avenues of body-plan evolution permitted by vertebrates. Evidence indicating homology include the fol- the ancestral serial/selector system of development. Bilate- lowing: (i) the greater similarity in sequences between indi- ria composed of a simple arrangement of anterior-posterior vidual selector genes of insects and vertebrates, rather than serial elements, such as annelids and arthropods, experi- among the different selector genes within either Drosophila enced a rapid early diversification of body plans; subse- or the mouse (1-5); (ii) the identical order ofexpression along quently body-plan evolution among serially organized forms the anterior-posterior axis of Drosophila and the mouse of declined. Increased constraint on body-plan evolution in these similar selector genes (2, 3); (iii) the identical order of serially organized forms may have resulted from separation the selector genes themselves in complexes on chromosomes in the genome of originally closely linked selector genes. in Drosophila and mouse (2, 3); and (iv) the similar expres- Dispersal of selector genes would have prevented the pro- sion of selector genes within the boundaries of comparable duction of additional body plans generated by the rearrange- serial elements in insects and the mouse (6). ment of closely linked selector genes. On the other hand, Given that selector genes in vertebrates and insects are those Bilateria that lack simple serial organization, such as homologous, they must have differentiated the same serial vertebrates and molluscs, probably did not retain the ances- elements in the shared ancestor. There is some evidence suggesting a shared ancestry of genes involved in construct- The publication costs of this article were defrayed in part by page charge ing serial morphogene fields along the anterior-posterior axis payment. This article must therefore be hereby marked "advertisement" of the body in addition to the presence of the selector genes in accordance with 18 U.S.C. §1734 solely to indicate this fact. that differentiate them. Among the numerous genes involved 4406 Downloaded by guest on October 2, 2021 Evolution: Jacobs Proc. Nail. Acad. Sci. USA 87 (1990) 4407 1.0 Similar arguments pertain to the relationship of the segmen- Serial Experimentation tation gene paired ofDrosophila, which is similar in sequence 0.8 to the Pax gene of mice expressed in intervertebral disks during development (12, 13). This pattern ofserial expression probably relates to the construction of serially repeated 0.6 morphogene fields, suggesting that a form of development in which serial morphogene fields are first constructed and then I- 0.4 differentiated by the differential expression of selector genes co may have been the ancestral form of development in both Co insects and vertebrates. 0.2 0 The Phylogenetic Context c I o D c& ~TTK Given that insects and vertebrates retain features of the serial/selector form of development, the clade for which Cn serial/selector development is a derived feature must contain Xo both insects and E vertebrates. Most phylogenies of the meta- C 1.0 zoa place the divergence of arthropods (and other prot- 0~ erostomes) and the chordates (and other deuterostomes) at a x fairly deep branch within the bilaterian metazoa. This place- w 0.8 ment is borne out by the ribosomal RNA phylogenies ofField et al. (14) and Lake (15). These phylogenies indicate that, 0.6 except for the flatworms, all bilaterian taxa diverged after the bifurcation of a molluscan-annelid-arthropod branch and an echinoderm-chordate branch. Consequently, the serial/ 0.4 selector form of development shared by vertebrates and insects is also a shared feature of all bilaterian taxa (with the 0.2 possible exception of flatworms). The evidence for expres- sion ofselector genes homologous to those ofvertebrates and Drosophila in the leech (16) and the suggestion of selector gene function indicated by the expression of homeobox- %O . O- % r I uI J F containing genes in discrete serial fields in larval echinoderms FIG. 1. In these histograms evolutionary novelty or "experi- (17) confirm that the vertebrate and Drosophila examples are ments" in the bilaterian metazoa are quantified for serially con- not a result of parallel evolution and that the serial/selector structed and nonserially constructed taxa for each period of Phan- form of development was present in the ancestor of the erozoic time (39). The experiments are ordinal origination (shaded) bilaterian clade. and origination of incertae sedis ofordinal or higher rank (hatched); these are expressed as a rate (experiments per million yr). Note the Increasing Constraint in Serial/Selector Development rapid production of experiments
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