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Evolution


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Alfred R. Wallace
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The Evolution of Jaws
Genetics and Molecular Evolution

Concept for Proposed Webpage

The first two links to Science (just below) for 11 October, along with others given further down the page, suggest to me the possibility of a story to be told, in laymen's language if possible. The following points should be addressed:

  • 1. Scientists build upon the work of earlier studies. Several research papers mentioned here span five years, each suggesting possibilites for future work that has been done.

  • 2. A series of fossils may show us the results of evolution (changes in jaw structure, or the adaptation of bones for new purposes) without being able to explain how such changes were made possible.

  • 3. The popular conception is that evolutionary change must occur through many insensibly fine steps and not by rapid modification of one or a few genes.

  • 4. Modern genetic research permits the kind of experiments that can tell us not only how something might have happened hundreds of millions of years ago, but also how rapidly major events might have ocurred.

  • 5. Each advance in research leads to predictions that can be confirmed by additional studies.

  • 6. Additional studies often confirm past work and continue the process of discovery and prediction, further confirming evolutionary theory and solidifying our base of knowledge.

I sense that the papers cited below provide the material to tell this story, but I do not have the necessary background to (1) properly evaluate the situation, or (2) to convert the technical jargon into language that would be convincing to a non-technical reader.

I invite anyone who has the competancy that I lack, and who also has an interest in advancing the comprehension by laymen of evolution, to consider undertaking the explanation of this material. Illustrations shown below, or those from other sources may be used. I will obtain permissions where necessary.

Hox and Other Genes Control Large Development Patterns

Hypothesized role of Dlx genes in BA patterning. (A) Diagram of a proto-gnathostome neurocranium (Nc) and associated BA (1 to 7) skeletal derivatives. Gnathostome BA are metameric structures within which develop a proximodistal series of skeletal elements. Inter-BA identity is regulated by Hox, Pbx, and Otx genes. It is hypothesized that the nested expression of Dlx genes regulates intra-BA identity. (B) In situ hybridization of Dlx2 and Dlx5 (E10.5) and diagram highlighting the nested Dlx expression within BA mesenchyme. AP, anteroposterior; BA, branchial arch; BA1, first branchial arch; BA2, second branchial arch; Bb, basibranchial; Cb, ceratobranchial; Eb, epibranchial; Hb, hypobranchial; hy, hyoid arch; md, mdBA1; mx, mxBA1; ; Pb, pharyngeobranchial; PD, proximodistal. From Michael J. Depew, M. J. et al., Specification of Jaw Subdivisions by Dlx Genes. Science, 298 (5592) :381-385, October 11, 2024

Suppression of Control Genes Produces Ancestral Structures

A more symmetrical smile. (A) Skeleton of the head of a jawed vertebrate, Acanthodes, showing symmetry between upper and lower jaw elements (green) and hyoid elements (yellow). The upper jaw (palatoquadrate) and lower jaw are both subdivided in two by a cartilaginous bridge. (B) Jaws of the acanthodian Poracanthodes with symmetrical jaws and dentition (yellow). The success of jawed vertebrates is partly attributable to the morphological independence (that is, asymmetry) of upper and lower jaws encoded by differentially expressed Dlx genes. Elaboration of this developmental code imbued vertebrates with hearing machinery and a wide variety of feeding capabilities. From Koentges G. and T. Matsuoka, Enhanced: Jaws of the Fates. Science 298 (5592) :371-373, 11 Oct 2024. (requires subscription to see full article).

The Following two paragraphs are also from this Perspectives article.

Jawed vertebrates have three pairs of Dlx homeobox genes--Dlx1/2, Dlx5/6, and Dlx3/7--that are expressed in restricted domains across the proximodistal axis of the branchial arches. Their nested expression within the branchial arches and the fact that their Drosophila homolog distalless [HN11] is a master regulator of distal leg identity make the Dlx genes excellent candidates for encoding distal identity in vertebrates. In all bilateral organisms, distalless genes appear to be involved in controlling the outgrowth of body appendages. Thus, the idea that the vertebrate Dlx homologs serve a similar function is attractive. Rather disappointingly, mice missing a single Dlx gene exhibit only piecemeal changes in the identities of isolated skeletal elements and teeth. This finding suggested that Dlx genes act as "micromanagers" rather than as "master regulators." Now, Depew and colleagues report the striking phenotype of the Dlx5/6 double mutant mouse [HN12]. They provide evidence that Dlx5 and Dlx6 are indeed the selectors of distal branchial arch identity. Their work suggests that the absence of a clear phenotype in mice lacking one Dlx gene is due to compensation by other coexpressed Dlx genes. Thanks to their discovery, the concept of a proximodistal molecular identity code is alive and well.

The Depew et al. work suggests that lower jaw patterning that is dependent on Dlx5/6 expression may have been elaborated and embellished between the phylogenetic nodes of jawed vertebrate and bony fish ancestors. Going back one step further in evolutionary history, jawless vertebrates such as lampreys [HN18] only have four Dlx genes with unclear homologies to their jawed vertebrate counterparts. All lamprey Dlx genes are expressed in branchial arches, but a nested expression pattern appears to be the invention of the jawed vertebrates. Our knowledge of the enhancer organization that controls this nested Dlx gene expression in jawed vertebrates is still rudimentary. Comparative genomic and functional studies of the regulatory elements controlling Dlx gene expression in lampreys, sharks, bony fish, coelacanths, and tetrapods will reveal the molecular evolution of the proximodistal code that underlies the shapes and fates of jaws.

Control Genes and Early Vertebrate Evolution

Abstract from Neidert A. et al., Lamprey Dlx Genes and Early Vertebrate Evolution. Proceedings National Academy of Sciences 98 (4) pp. 1665-1670, February 13, 2024.

Gnathostome vertebrates have multiple members of the Dlx family of transcription factors that are expressed during the development of several tissues considered to be vertebrate synapomorphies, including the forebrain, cranial neural crest, placodes, and pharyngeal arches. The Dlx gene family thus presents an ideal system in which to examine the relationship between gene duplication and morphological innovation during vertebrate evolution. Toward this end, we have cloned Dlx genes from the lamprey Petromyzon marinus, an agnathan vertebrate that occupies a critical phylogenetic position between cephalochordates and gnathostomes. We have identified four Dlx genes in P. marinus, whose orthology with gnathostome Dlx genes provides a model for how this gene family evolved in the vertebrate lineage. Differential expression of these lamprey Dlx genes in the forebrain, cranial neural crest, pharyngeal arches, and sensory placodes of lamprey embryos provides insight into the developmental evolution of these structures as well as a model of regulatory evolution after Dlx gene duplication events.

When Important Characters Evolved

Dlx genes are associated with morphological novelty in the vertebrate lineage. This cladogram depicts hypothesized phylogenetic relationships of extant lineages within the chordates. A partial listing of morphological characters supporting this phylogenetic hypothesis is shown. Asterisked characters are those that have been shown, in gnathostomes, to be associated with Dlx gene expression. Note that some analyses using molecular characteristics indicate that hagfish and lampreys are monophyletic (dashed line), suggesting that modern hagfish secondarily lost certain morphological characters. The position of neural crest and placodes is speculative because hagfish embryos have not been characterized. From Neidert A. et al., Lamprey Dlx Genes and Early Vertebrate Evolution. Proceedings National Academy of Sciences  98 (4) :1665-1670, Feb. 13, 2024.

Vertebrate Jaw Evolution


Jaw evolution and functions of signaling molecules in the mandibular arch. (A) Hypothetical evolutionary transition of the jaw. The first two pharyngeal arches [mandibular (ma) and hyoid (hy) arches] are labeled. Although the arches resemble each other in the ancestral condition, the mandibular arch is enlarged toward gnathostomes (right). Finally, palatoquadrate (pq) and Meckel's (Mc) cartilages differentiate in the upper and lower jaw, respectively. Only a portion of the published graphic is shown here. From Shigetani Y. et al., Heterotopic Shift of Epithelial-Mesenchymal Interactions in Vertebrate Jaw Evolution. See Science 296 (5571) 17 May 2024, pp. 1316-1319.


A scenario for jaw evolution. (Top) Patterning of crest cells is compared between lampreys and gnathostomes. In both the animals, the ectomesenchyme contains postoptic (po) and mandibular arch (ma) subdomains. Growth factors secreted by the epidermis (blue line) induce target homeobox genes (pink and blue) in the entire lamprey ectomesenchyme, whereas in gnathostomes the same signaling is effective only in the mandibular component. Thus, the phenotypically similar protrusions originate from nonequivalent cell populations in the two animals. Heterotopic shift of epithelial-mesenchymal interactions is assumed to be behind this difference. The postoptic crest cells occupy the site of prechordal cranium (prc) in gnathostomes. Broken lines indicate the boundary between postoptic (po) and mandibular (ma) ectomesenchyme. (Bottom) The evolutionary sequence of the changes in developmental patterning is summarized on the phylogenetic tree. The vertebrate ancestor had acquired neural crest-derived ectomesenchyme after the split from amphioxus, as an element for epithelial-mesenchymal interactions. The molecular cascades for the interactions may have already been present in the ancestral vertebrates. Although these genes may have already been involved in oral patterning in agnathans, a heterotopic shift must be assumed in the lineage leading to gnathostomes to explain the topographic discrepancy shown at top. From Shigetani Y. et al., Heterotopic Shift of Epithelial-Mesenchymal Interactions in Vertebrate Jaw Evolution. See Science 296 (5571) 17 May 2024, pp. 1316-1319.

The Origin and Evolution of Animal Appendages

Another paper that might be usefule in this analysis is: Abstract from Panganiban G. et al., The Origin and Evolution of Animal Appendages. Proc. Natl. Acad. Sci. USA  94, pp. 5162-5166, May 1997.

Animals have evolved diverse appendages adapted for locomotion, feeding and other functions. The genetics underlying appendage formation are best understood in insects and vertebrates. The expression of the Distal-less (Dll) homeoprotein during arthropod limb outgrowth and of Dll orthologs (Dlx) in fish fin and tetrapod limb buds led us to examine whether expression of this regulatory gene may be a general feature of appendage formation in protostomes and deuterostomes. We find that Dll is expressed along the proximodistal axis of developing polychaete annelid parapodia, onychophoran lobopodia, ascidian ampullae, and even echinoderm tube feet. Dll/Dlx expression in such diverse appendages in these six coelomate phyla could be convergent, but this would have required the independent co-option of Dll/Dlx several times in evolution. It appears more likely that ectodermal Dll/Dlx expression along proximodistal axes originated once in a common ancestor and has been used subsequently to pattern body wall outgrowths in a variety of organisms. We suggest that this pre-Cambrian ancestor of most protostomes and the deuterostomes possessed elements of the genetic machinery for and may have even borne appendages.

References From Science
Dictionaries and Glossaries


The On-line Medical Dictionary is available on CancerWEB.

The Life Sciences Dictionary is provided by the BioTech Web site of the University of Texas Institute for Cellular and Molecular Biology.

The xrefer Web site provides scientific dictionaries and other reference works.

A Database of Embryological Terms is provided by M. Cavey, Department of Biological Sciences, University of Calgary, for an embryology course.

Web Collections, References, and Resource Lists


Biology Links are provided by the Dept. of Molecular and Cellular Biology, Harvard University.

The Google Web Directory provides links to Internet resources related to developmental biology.

The Virtual Library-Developmental Biology is provided by the Society for Developmental Biology.

The WWW Virtual Library of Cell Biology includes sections of Internet links for gene expression and cellular aspects of development.

W. Wasserman, Department of Biology, Loyola University of Chicago, provides a resource page on developmental biology.

Developmental Biology Online is a supplemental education resource provided by S. Scadding, Department of Zoology, University of Guelph, Canada. Included are links to Internet resources on developmental biology and cell biology and a glossary. Definitions of terms for direction and orientation are provided.

Online Texts and Lecture Notes


J. Kimball provides Kimball's Biology Pages, an online biology textbook. Three articles on embryonic development are included.

Embryo Images is a tutorial on mammalian development using scanning electron micrographs provided by the School of Medicine, University of North Carolina.

The UNSW Embryology Web site is an educational resource on embryological development provided by M. Hill, School of Anatomy, University of New South Wales, Australia.

Virtual Embryo/Dynamic Development is a Web resource provided by L. Browder, Department of Biochemistry and Molecular Biology, University of Calgary.

A Web supplement to the sixth edition of the textbook Developmental Biology is provided by the author S. Gilbert, Department of Biology, Swarthmore College, PA. Additional supplemental material is provided on Gilbert's Zygote Web site.

J. Armbruster, Department of Biological Sciences, Auburn University , provides lecture notes for a course on vertebrate comparative anatomy.

L. Zwiebel and L. Solnica-Krezel, Department of Biological Sciences, Vanderbilt University, provide lecture notes for a developmental biology course.

L. Sweeney, Department of Biology, Bryn Mawr College, PA, offers lecture notes for a developmental biology course.

G. Podgorski, Department of Biology, Utah State University, offers lecture notes for a course on developmental biology.

D. Linden, Biology Department, Occidental College, Los Angeles, offers lecture notes for a course in developmental cell biology.

W. Powell, Biology Department, Kenyon College, OH, provides lecture notes for a course on genetics and development.

C. Kimmel, Department of Biology, University of Oregon, offers lecture notes for a course on vertebrate evolution and development.

D. Rand, Program in Ecology and Evolutionary Biology, Brown University, offers lecture notes for a course on evolutionary biology.

General Reports and Articles


Developmental Dynamics, the journal of the American Association of Anatomists, makes available an online collection of review articles.

The Atlas of Genetics and Cytogenetics in Oncology and Haematology offers a presentation by J. Bonaventure titled "Skeletal development in human: A model for the study of developmental genes."

The 4 July 1997 issue of Science had a news article by E. Pennisi and W. Roush titled "Developing a new view of evolution." The 25 June 1999 issue had a review by A. H. Knoll and S. B. Carroll titled "Early animal evolution: Emerging views from comparative biology and geology."

The May 1997 issue of the Proceedings of the National Academy of Sciences had an article by G. Panganiban et al. titled "The origin and evolution of animal appendages." The 25 April 2024 issue had a special feature on evolutionary developmental biology with perspective and review articles as well as topical research articles.

Numbered Hypernotes

  • el
  • pt
    1. Herman Melville's poem "The Maldive Shark" is available in the Poetry Archive. D. Campbell, Department of English, Gonzaga University, provides a resource page about Melville.

    2. Sharks and pilot fish. A photograph by E. Robinson of a shark with pilot fish is provided on the ScubaDuba Web site. An entry for pilot fish is included in xrefer's Oxford Paperback Encyclopedia. FishBase has an entry for Naucrates ductor (pilot fish). The NOAA Photo Library displays a 19th-century etching of a pilot fish. EnchantedLearning.com offers an educational presentation about sharks. The Ichthyology Department of the Florida Museum of Natural History offers a resource page on sharks. Fiona's Shark Mania Web site provides links to Internet resources on sharks.

    3. M. J. Depew and J. L. R. Rubenstein are in the Neuroscience Graduate Program and the Department of Psychiatry, University of California, San Francisco; the Rubenstein Lab has a Web page. T Lufkin is at the Brookdale Center for Developmental and Molecular Biology, Mount Sinai School of Medicine, New York.

    4. Homeobox genes Dlx5 and Dlx6. Homeobox is defined in xrefer's Dictionary of Biology. SWISS-PROT has a keyword entry for homeobox . InterPro has an entry for the homeobox domain. S. Gilbert makes available a student presentation by K. Panfilio on the Dlx gene family prepared for a seminar on developmental genetics. C. Kimmel offers lecture notes on Dlx genes for a course on vertebrate evolution and development. The GeneCards database from the Weizmann Institute of Science has entries for Dlx5 and Dlx6 genes with links to other Internet resources provided. The Jackson Laboratory's Mouse Genome Informatics Web site has entries for the Dlx5 and Dlx6 genes of mice.

    5. Congenital disorders possibly related to Dlx genes. Online Mendelian Inheritance in Man, a catalog of human genes and genetic disorders, has entries for members of the Dlx gene family: Dlx1, Dlx2, Dlx3, Dlx7 (Dlx4), Dlx5, and Dlx6.

    6. Formation of the vertebrate face. Embryo Images has a section on craniofacial development. T. Marino, Department of Anatomy and Cell Biology, Temple University School of Medicine, provides a presentation on the development of the face as part of an embryology resource page. A student presentation on human facial development is made available on the anatomy resource page provided by the School of Biological Sciences, University of Manchester, UK. R. Tucker, University of California, Davis, Department of Cell Biology and Human Anatomy, provides lecture notes on the development of the head, neck, and face (parts one and two) for a course on developmental, gross, and radiologic anatomy.

    7. Neural crest. M. Hill's UNSW Embryology offers a presentation on the neural crest. S. Gilbert makes available a student presentation by K. Panfilio on neural crest cells, which was prepared for a seminar on developmental genetics. D. O'Day, Department of Zoology, University of Toronto at Mississauga, provides lecture notes on the neural crest for a course on human development. A student project on the neural crest was prepared by K. Moran for a course on developmental biology offered by the School of Biological Sciences, University of Manchester. The October 1996 issue of Development had an article (full text available in PDF format) by G. Koentges and A. Lumsden titled "Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny" (3).

    8. Branchial arches. Pharyngeal arch (branchial or visceral arch) is defined in xrefer's Concise Medical Dictionary. The 1918 edition of Gray's Anatomy of the Human Body, made available by Bartleby.com, has a section on the branchial region. The Gross Anatomy Homepage at Marshall University's School of Medicine makes available notes on the development of branchial arches for a course on medical gross anatomy. The Department of Anatomy, Howard University College of Medicine, makes available lecture notes on the branchial apparatus for an anatomical sciences course. T. Marino provides a presentation on pharyngeal (branchial arches) as part of an embryology resource page. P. Hunt, Department of Biological Sciences, University of Durham, UK, offers a research presentation on branchial arches.

    9. Proximodistal and other axes of development. Distal and proximal are defined in the introduction to anatomy terminology provided by the Faculty of Medicine, University of Calgary School of Medicine. L. Solnica-Krezel defines proximodistal and other axes of developing limbs in lecture notes on limb development for a course on developmental biology. UNSW Embryology offers a presentation on the axes of limb molecular development with a section on proximal/distal patterning.

    10. Hox homeobox genes. Kimball's Biology Pages includes a section on the Hox cluster of homeobox genes in the presentation titled "Embryonic development: Putting on the finishing touches." UNSW Embryology offers a presentation on Hox homeobox genes in the section on molecular development and a presentation on the development of the rostrocaudal axis. L. Browder's Dynamic Development makes available a presentation by D. Rancourt titled "Establishment of spatial patterns of gene expression during early vertebrate development: Hox genes." C. Kimmel provides lecture notes on Hox genes and anterior-posterior patterning for a course on vertebrate evolution and development. D. O'Day offers lecture notes on limb development and Hox genes for a course on human development. W. Powell provides lecture notes on Hox genes and molecular evolution for a course on genetics and development.

    11. Drosophila homolog distalless. S. Gilbert's Zygote Web site includes a presentation on distalless. FlyBase offers a report on the gene Dll (distal-less). The Interactive Fly offers a presentation on Dll, including a section on evolutionary homologs.

    12. Dlx5/6 double mutant mouse. The Jackson Laboratory's TBASE (Transgenic/Targeted Mutation Database) has an entry for the Dlx5/6 (-/-) mouse, as well as an April 2024 Knockout of the Month feature on this mouse with links to Internet resources.

    13. Mammalian middle ear. An Anatomical Tour of the Ear includes a description of bones of the human middle ear. The vertebrates section of the Palaeos Web site provides an overview of the ear and a presentation on the incus. Promenade 'round the Cochlea, a tutorial on the human ear and auditory system, offers a presentation on the middle ear. Embryo Images has a Section on ear development. R. Tucker provides lecture notes on the development of the ear for a course on developmental, gross, and radiologic anatomy.

    14. Evolution of the mammalian jaw and ear. Animal Diversity Web, a presentation of the University of Michigan Museum of Zoology, offers an article on mammalian jaws and ears. S. Carr, Department of Biology, Memorial University of Newfoundland, presents a graphic introduction to the evolution of the mammalian jaw in lecture notes on systematics for a course on the principles of evolution and systematics. Evolution of the mammalian jaw and ear is discussed in an article by M. Benton titled "Evidence of evolutionary transitions," which is available on the Actionbioscience.org Web site. The 23 April 1999 issue of Science had a News Focus article by E. Pennisi titled "From embryos and fossils, new clues to vertebrate evolution" that discussed the origin of jaws. C. Kimmel offers lecture notes titled "Gills make jaws make ears" for a course on vertebrate evolution and development.

    15. Couly et al. paper. The February 2024 issue of Development had an article by G. Couly, S. Creuzet, S. Bennaceur, C. Vincent, and N. M. Le Douarin (at the Institut d'Embryologie Cellulaire et Moléculaire du CNRS et du Collège de France) titled "Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head."

    16. Endoderm is defined in the BioTech Life Sciences Dictionary and in xrefer's Dictionary of Biology. Developmental Biology Online provides a presentation on the derivatives of endoderm. D. Linden offers lecture notes on the endoderm for a course in developmental cell biology.

    17. Acanthodians. An entry for Acanthodii (acanthodians) is included in xrefer's Dictionary of Earth Sciences. The Palaeos Web site provides an introduction to Acanthodii. J. Armbruster includes a section on Acanthodii in lecture notes on fish for a course on vertebrate comparative anatomy.

    18. Lampreys. The online Columbia Encyclopedia has an entry for lamprey. The University of California Museum of Paleontology offers an introduction to lampreys. The Tree of Life Web Project offers a presentation on lampreys. An information page on lampreys is provided by the SAREP Web site at the Department of Natural Resources, Cornell University. J. Armbruster includes a section on jawless fishes (including lampreys) in lecture notes for a course on vertebrate comparative anatomy. The 17 May 2024 issue of Science had a report by Y. Shigetani et al. titled "Heterotopic shift of epithelial-mesenchymal interactions in vertebrate jaw evolution" (10). The 13 February 2024 issue of the Proceedings of the National Academy of Sciences had an article by A. H. Neidert, V. Virupannavar, G. W. Hooker, and J. A. Langeland titled "Lamprey Dlx genes and early vertebrate evolution" (9).





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    jaws.htm Last Updated April 22, 2024     Links verified April 22, 2024