Evolutionary developmental biology (evo-devo) has undergone dramatic transformations since its emergence as a distinct discipline. This paper aims to highlight the scope, power, and future promise of evo-devo to transform and unify diverse aspects of biology. We articulate key questions at the core of eleven biological disciplines-from Evolution, Development, Paleontology, and Neurobiology to Cellular and Molecular Biology, Quantitative Genetics, Human Diseases, Ecology, Agriculture and Science Education, and lastly, Evolutionary Developmental Biology itself-and discuss why evo-devo is uniquely situated to substantially improve our ability to find meaningful answers to these fundamental questions. We posit that the tools, concepts, and ways of thinking developed by evo-devo have profound potential to advance, integrate, and unify biological sciences as well as inform policy decisions and illuminate science education. We look to the next generation of evolutionary developmental biologists to help shape this process as we confront the scientific challenges of the 21st century.
Recognition that the transformation of one form into another is caused by both internal and external factors is the foundation and driving philosophy underlying all research in the field of biology. 10,11 In practice, however, studies of the internal (proximate) causes of biological transformation within the lifetime of an organism and of the external (ultimate) causes of transformation from one generation to the next (evolutionary transformation) have been pursued independently in two sub-disciplines, developmental and evolutionary biology, respectively. This situation has changed with the emergence of evolutionary developmental biology or "evo-devo," which seeks, by means of a comparative approach, to explain the evolution and development of morphological characters as well as the evolution of their underlying genetic and developmental mechanisms. 12 Essential to this approach is a well-defined and strongly supported phylogeny from which homology and the direction of morphological transformations can be accurately assessed. [13][14][15] Exciting and significant findings have been made in evo-devo. One is that the metazoan body plan is established by a surprisingly small set of highly conserved patterning genes. These homeobox (Hox) genes (Fig. 2), which originated early in metazoan evolution, are distributed throughout the animal kingdom. 16 -18 Another important finding is that homology at the genetic level is not necessarily correlated with homology at the morphological level. For example, the compound eyes of insects and the camera eyes of vertebrates evolved independently, but in both the initiation of eye formation requires expression of the same gene, Pax-6. 19 It also has been demonstrated that morphological novelties such as butterfly eye spots 20 or limbless tetrapods (snakes 21 ) result from alterations in the molecular mechanisms that control the development of major anatomical structures. Moreover, the evolution of developmental systems, which mediate morphological evolution, can occur by slight changes in the regulation of otherwise conserved patterning genes (Fig. 3). [22][23][24] While evo-devo research has focused primarily on broad taxonomic comparisons and major morphological transitions such as that from fish fins to tetrapod limbs, its potential for explaining phenotypic differences between and among closely related taxa is clearly recognized. [25][26][27] In this context, understanding how molecular evolution shapes genetic variation of patterning and growth genes in different primate lineages can be a powerful method for linking genetic and developmental variation to phenotypic (morphological) variation at both the microevolutionary and macroevolutionary scales. 28 -31 Indeed, the focus of evo- The order Primates is composed of many closely related lineages, each having a relatively well established phylogeny supported by both the fossil record and molecular data. 1 Primate evolution is characterized by a series of adaptive radiations beginning early in the Cenozoic era. Studies of th...
Conclusive evidence was provided that y', the upstream of the two linked simian y-globin loci (5'-y'-'y2-3'), is a pseudogene in a major group of New World monkeys. Sequence analysis of PCR-amplified genomic fragments of predicted sizes revealed that all extant genera of the platyrrhine family Atelidae [Lagothrix (woolly monkeys), Brachyteles (woolly spider monkeys), Ateles (spider monkeys), and Alouafta (howler monkeys)] share a large deletion that removed most of exon 2, all of intron 2 and exon 3, and much of the 3' flanking sequence of y. The fact that two functional 'y-globin genes were not present in early ancestors of the Atelidae (and that y1 was the dispensible gene) suggests that for much or even all of their evolution, platyrrhines have had ly2as the primary fetally expressed 'y-globin gene, in contrast to catarrhines (e.g., humans and chimpanzees) that have 'y' as the primary fetally expressed y-globin gene. Results from promoter sequences further suggest that all three platyrrhine families (Atelidae, Cebidae, and Pitheciidae) have y2 rather than y' as their primary fetally expressed y-globin gene. The implications of this suggestion were explored in terms of how gene redundancy, regulatory mutations, and distance of each 'y-globin gene from the locus control region were possibly involved in the acquisition and maintenance of fetal, rather than embryonic, expression.
Reverse phase chromatography of the globin chains of adult, newborn, and fetal erythrocytes from three species of New World monkeys (Cebus apella, Aotus azarae, and Callithrix jacchus) representing three of the seven platyrrhine clades showed that gamma-globin expression was fetal in these animals. The globins were identified by a combination of chemical sequencing and mass spectrometric analysis. Since gamma-globin expression is fetal in the other major simian branch, the catarrhines, but embryonic in prosimian primates and nonprimate placental mammals, the evolution of fetal recruitment can now be assigned to the period between the simian-prosimian divergence (55 million years ago) and the platyrrhine-catarrhine divergence (35 million years ago). The gamma-globin gene underwent tandem duplication during the same evolutionary epoch, in accord with a model that suggests that the downstream duplicated gamma-gene (gamma2) was free to acquire the mutations necessary for fetal recruitment. Mass spectrometric analysis of tryptic digests of the gamma-globins verified the amino acid sequences deduced from genomic sequencing. Detailed analysis of high performance liquid chromatography and matrix-assisted laser desorption/ionization mass spectrometry data showed that gamma2-globin in Cebus was expressed to a far greater extent than gamma1-globin, supporting inferences drawn from a study of the promoter sequences. A "pre-gamma"-globin was observed in C. apella and shown to be primarily the glutathionyl adduct. The other species, A. azarae and C. jacchus, also express only one gamma-globin polypeptide. This work provides biochemical evidence of an evolutionary trend in the platyrrhines to alter the duplicated gamma-globin gene locus so that only one gamma-globin polypeptide is expressed.
Nucleotide sequences were determined for the -yl and 9y2-globin loci from representatives of the seven anciently separated clades in the three extant platyrrhine families (Atelidae, Pitheciidae, and Cebidae). Comparative nucleotide sequence analysis of the f3-globin gene cluster and its locus control region (LCR) demonstrates that the linkage order (5'-LCR-s-y-qrq-8-f3-3') of the LCR and developmentally regulated (3-type globin genes was conserved during primate phylogeny (1-6). The temporal order of developmental expression of the functional genes was for the most part also conserved with the 5'-most genes, s and y, expressed during earlier ontogenetic stages and the 3'-most genes, 5 and ,3, expressed during the later stages (4, 7, 8). However, whereas both E and y were originally embryonically expressed and continue to be so in prosimians, y but not e became fetally expressed in anthropoid primates (2, 9-11).Before the anthropoids diverged into catarrhines (Old World monkeys, apes, and humans) and platyrrhines (New World monkeys) [35 million years ago (mya)] but after the stem anthropoids had diverged from both strepsirhine (galago and lemur) and haplorhine (tarsier) prosimians (60-55 mya), the stem anthropoid y gene tandemly duplicated to produce 5t_'y1-_y2-3' (12)(13)(14). This duplication was mediated by an unequal crossover between two LINE elements (Lla and Llb) that had inserted upstream and downstream, respectively, of the stem anthropoid y gene (12-15). During this same evolutionary time period (55-35 mya), y became fetally expressed in anthropoid primates (12,13,16). Different fetal y expression patterns then evolved in different anthropoid lineages. In humans and chimpanzees (and presumably other catarrhines), the upstream ryl gene is the primary fetally expressed gene, its expression level being three times higher than that of the downstream y2 gene (9, 10). In contrast, all four genera of the platyrrhine family Atelidae (Alouatta, Ateles, Brachyteles, and Lagothrix) share a 1.8-kb deletion in the 9yl gene, converting it into a pseudogene, thus leaving y2 as the sole functional y gene (17). The only other platyrrhine for which y-globin nucleotide sequences were previously reported is a capuchin monkey, Cebus albifrons (14,18). Although this capuchin monkey possesses two intact y genes, the promoter of its yl gene accumulated many nucleotide substitutions, including a point mutation in the proximal CCAAT box sequence (CCAAT -> CCAAc), a motif that is critically important for efficient expression of globin genes (19,20).The 16 extant platyrrhine genera belong to seven major clades (21-25), which in turn can be grouped into families Atelidae, Pitheciidae, and Cebidae (22) (Fig. 1). We have now determined y-globin nucleotide sequences for members of species from all seven clades of the three families and present evidence that (i) point mutations in the 9yI proximal CCAAT box motif have accumulated not only in Cebus but also in Callicebus and the pitheciins, and that (ii) recombinational crossove...
The expression of ϵ‐ and γ‐globin mRNA and protein has been determined in three Old World monkey species (Macaca mulatta, Macaca nemestrina, and Cercopithecus aethiops). Using RT‐PCR with primers for ϵ‐ and γ‐globin, both mRNAs were detected in early fetal stages, whereas at 128 days (85% of full term), only γ was expressed. High‐performance liquid chromatography was used for separation and quantitation, and matrix‐assisted laser desorption/ionization mass spectrometry was used for identification of globin polypeptides. An α‐globin polymorphism was observed in all of the species examined. During fetal life, γ‐globin was the predominant expressed β‐type globin. The red blood cells of infants still contained substantial amounts of γ‐globin, which declined to negligible levels in 14 weeks as β‐globin expression reached adult values. The ratio of γ1‐ to γ2‐globins (equivalent to Gγ/Aγ in humans) was approximately 2.5, similar to the Gγ/Aγ ratio observed in humans. Thus, γ‐globin gene expression in these Old World monkeys species has three features in common with human expression: expression of both duplicated γ genes, the relative preponderance of γ1 over γ2 expression, and the delay of the switch from γ‐ to β‐globin until the perinatal period. Thus, the catarrhines seem to share a common pattern of developmental switching in the β‐globin gene cluster, which is distinct from the timing of expression in either prosimians or the New World monkeys. Our results indicate that an Old World monkey, such as Rhesus, could serve as a model organism (resembling humans) for experimentally investigating globin gene expression patterns during the embryonic, fetal, and postnatal stages. J. Exp. Zool. (Mol. Dev. Evol.) 288:318–326, 2000. © 2000 Wiley‐Liss, Inc.
The identification of cis-sequences responsible for spatiotemporal patterns of gene expression often requires the functional analysis of large genomic regions. In this study a 100-kb zebrafish Hoxa-11b-lacZ reporter gene was constructed and expressed in transgenic mice. PAC clone 10-O19, containing a portion of the zebrafish HoxA-b cluster, was captured into the yeast-bacterial shuttle vector, pPAC-ResQ, by recombinogenic targeting. A lacZ reporter gene was then inserted in-frame into exon 1 of the zfHoxa-11b locus by a second round of recombinogenic targeting. Expression of the zfHoxa-11b-lacZ reporter gene in 10.5 d.p.f. transgenic mouse embryos was observed only in the posterior portion of the A-P axis, in the paraxial mesoderm, neural tube, and somites. These findings demonstrate the utility of recombinogenic targeting for the modification and expression of large inserts captured from P1/PAC clones.
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