Key Points
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Evo–devo is tied to geological time through the necessity of placing developmental evolution in its context within geological history. This involves finding when and how rapidly developmental features evolved, and the integration of developmental evolution into major transitions in body plans.
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The inclusion of fossils into phylogenetic trees yields other kinds of information that are crucial to evo–devo, the direction of change in evolving homologous features in a lineage and the identification of convergent evolution of features that appear to be homologous but have evolved independently on separate branches of a phylogenetic tree.
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It is crucial for developmental evolution to know the time of divergence of taxa, the time of appearance of evolving features within taxa and their rates of evolutionary change. This information is obtained from geochronology combined with the fossil record of living taxa. These data underlie the calibration of 'molecular clocks'.
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Fossils are crucial for constraining hypotheses derived from evo–devo, such as the case of the homology of digits in the bird wing, the origins of paired appendages and the gene regulation of appendage development, as well as the evolution of the mammalian middle ear.
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Fossils in some cases allow evo–devo studies on now extinct organisms.
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There is an important complementarity between the search for the earliest animals in the fossil record and the identification of the genetic toolkit of the most ancient animal groups.
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Occasionally, unexpected fossils that exceed the expected limits of fossilization give data on the evo–devo of soft parts, such as feathers on dinosaurs or the well-preserved embryos and larvae from the late Precambrian and Cambrian.
Abstract
Fossils give evo–devo a past. They inform phylogenetic trees to show the direction of evolution of developmental features, and they can reveal ancient body plans. Fossils also provide the primary data that are used to date past events, including divergence times needed to estimate molecular clocks, which provide rates of developmental evolution. Fossils can set boundaries for hypotheses that are generated from living developmental systems, and for predictions of ancestral development and morphologies. Finally, although fossils rarely yield data on developmental processes directly, informative examples occur of extraordinary preservation of soft body parts, embryos and genomic information.
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References
Raff, R. A. Evo–devo: the evolution of a new discipline. Nature Rev. Genet. 1, 74–79 (2000).
Lemons, D. & McGinnis, W. Genomic evolution of Hox gene clusters. Science 313, 1918–1922 (2006).
Love, A. C. & Raff, R. A. Knowing your ancestors: themes in the history of evo–devo. Evol. Dev. 5, 327–330 (2003).
Amundson, R. The Changing Role of the Embryo in Evolutionary Thought. Roots of Evo–Devo. (Cambridge University Press, Cambridge, 2005).
Austin, J. J., Smith, A. B. & Richard H. Thomas, R. H. Palaeontology in a molecular world: the search for authentic ancient DNA. Trends Ecol. Evol. 12, 303–306 (1997).
Marota, I. & Rollo, F. Molecular paleontology. Cell. Mol. Life Sci. 59, 97–111 (2002).
Green, R. E. et al. Analysis of one million base pairs of Neanderthal DNA. Nature 444, 330–336 (2006).
Wagner, G. P. The developmental genetics of homology. Nature Rev. Genet. 8, 473–479 (2007).
Butterfield, N. J. Hooking some stem-group “worms”: fossil lophotrochozoans in the Burgess Shale. Bioessays 28, 1161–1166 (2006).
Conway Morris, S. & Peel, J. S. Articulated halkieriids from the lower Cambrian of north Greenland and their role in early protostome evolution. Phil. Trans. R. Soc. B. Biol. Sci. 347, 305–358 (1995).
Conway Morris, S. & Caron, J.-B. Halwaxiids and the early evolution of the lophotrochozoans. Science 315, 1255–1258 (2007).
Swalla, B. J. & Smith, A. B. Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Proc. R. Soc. London B Biol. Sci. (in the press). These two papers show how Cambrian animal fossils can be reconstructed to give information about features of taxa that are basal to crown group phyla.
Smith, A. B. The pre-radial history of echinoderms. Geol. J. 40, 255–280 (2005).
Sereno, P. C. The logical basis of phylogenetic taxonomy. Syst. Biol. 54, 595–619 (2005).
Smith, A. B. Systematics and the Fossil Record. (Blackwell Scientific, Oxford, 1994).
Gauthier, J., Kluge, A. G. & Rowe, T. Amniote phylogeny and the importance of fossils. Cladistics 4, 105–209 (1988).
Donoghue, M. J., Doyle, J. A., Gauthier, J., Kluge, A. G. & Rowe, T. The importance of fossils in phylogeny reconstruction. Annu. Rev. Ecol. Syst. 20, 431–460 (1989).
Smith, A. B. What does paleontology contribute to systematics in a molecular world. Mol. Phylogenet. Evol. 9, 437–447 (1998).
Wiens, J. J. Can incomplete taxa rescue phylogenetic analyses from long-branch attraction? Syst. Biol. 54, 731–742 (2005).
Clouthier, R. & Ahlberg, P. E. Sarcopterygian interrelationships: how far are we from a phylogenetic consensus? Geobios 19, 241–248 (1995).
Donoghue, P. C. J. & Benton, M. J. Rocks and clocks: calibrating the tree of life using fossils and molecules. Trends Ecol. Evol. 22, 424–431 (2007).
Benton, M. J. & Donoghue, P. C. J. Paleontological evidence to date the tree of life. Mol. Biol. Evol. 24, 26–53 (2007). These two papers discuss in detail the use of fossils in generating minimum divergence times for taxa, and using fossils and molecules in dating the tree of life.
Bromham, L. & Penny, D. The modern molecular clock. Nature Rev. Genet. 4, 216–224 (2003).
Welch, J. J. & Bromham, L. Molecular dating when rates vary. Trends Ecol Evol. 20, 320–327 (2005).
Peterson, K. J. et al. Estimating metazoan divergence times with a molecular clock. Proc. Natl Acad. Sci. USA 101, 6536–6541 (2004).
Knoll, A. H. Learning to tell Neoproterozoic time. Precambrian Res. 100, 3–20 (2000).
Blair, J. E. & Hedges, S. B. Molecular phylogeny and divergence times of deuterostome animals. Mol. Biol. Evol. 22, 2275–2284 (2005).
Hart, M. W., Byrne, M. & Smith, M. J. Molecular phylogenetic analysis of life-history evolution in asterinid starfish. Evolution 51, 1848–1861 (1997).
Zigler, K. S., Raff, E. C., Popodi, E., Raff, R. A. & Lessios, H. A. Adaptive evolution of bindin in the genus Heliocidaris is correlated with the shift to direct development. Evolution 57, 2293–2302 (2003).
Peterson, K. J., Summons, R. E. & Donoghue, P. C. J. Molecular paleobiology. Paleontology 50, 775–809 (2007).
Vargas, A. O. & Fallon, J. F. The digits of the wing of birds are 1, 2, and 3. A review. J. Exp. Zool. Mol. Dev. Evol. 304B, 206–219 (2005). This paper discusses how fossil data can constrain hypotheses about developmental evolution that are based on living forms. The discussion focuses on the identities of bones in the modified hands of birds.
Bolker, J. A. Model systems in developmental biology. Bioessays 17, 451–455 (1995).
Crompton, A. W. & Jenkins, F. A. Jr. in Mesozoic Mammals (eds J. A. Lillegraven, Z. Kielen-Jaworowska & W. A. Clemens) 59–73 (Univ. California. Press, Berkeley, 1979).
Wilson, J. & Tucker, A. S. Fgf and Bmp signals repress the expression of Bapx1 in the mandibular mesenchyme and control the position of the developing jaw joint. Dev. Biol. 266, 138–150 (2004).
Tucker, A. S., Watson, R. P., Lettice, L. A., Yamada, G. & Hill, R. E. Bapx1 regulates patterning in the middle ear: altered regulatory role in the transition from the proximal jaw during vertebrate evolution. Development 131, 1235–1245 (2004).
Rich, T. H., Hopson, J. A., Musser, A. M., Flannery, T. F. & Vickers-Rich, P. Independent orgins of middle ear bones in monotremes and therians. Science 307, 910–914 (2005).
Kavanagh, K. D., Evans, A. R. & Jernvall, J. Predicting evolutionary patterns of mammalian teeth from development. Nature 449, 427–433 (2007).
Polly, P. D. Development with a bite. Nature 449, 413–415 (2007).
Tanaka, M. & Tickle, C. in Fins into Limbs. Evolution, Development, and Transformation (ed. B. K. Hall) 65–78 (Univ. Chicago Press, Chicago, 2007).
Friedman, M., Coates, M. I. & Anderson, P. First discovery of a primitive coelacanth fin fills a major gap in the evolution of lobed fins and limbs. Evol. Dev. 9, 329–337 (2007).
Zhang, X. G. & Hou, X. G. Evidence for a single median fin-fold and tail in the Lower Cambrian vertebrate, Haikouichthys ercaicunensis. J. Evol. Biol. 17, 1162–1166 (2004).
Freitas, R., Zhang, G. & Cohn, M. J. Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature 442, 1033–1037 (2006).
Metscher, B. D. et al. Expression of Hoxa-11 and Hoxa-13 in the pectoral fin of a basal ray-finned fish, Polyodon spathula: implications for the origin of tetrapod limbs. Evol. Dev. 7, 186–195 (2005).
Davis, M. C., Dahn, R. D. & Shubin, N. H. An autopodial-like pattern of Hox expression in the fins of a basal actinopterygian fish. Nature 447, 473–477 (2007).
Sordino, P., van der Hoeven, F. & Duboule, D. Hox gene expression in teleost fins and the origin of vertebrate digits. Nature 375, 678–681 (1995).
Neumann, C. J., Grandel, H., Gaffield, W., Schulte-Merker, S. & Nüsslein-Volhard, C. Transient establishment of anteroposterior polarity in the zebrafish pectoral fin bud in the absence of sonic hedgehog activity. Development 126, 4817–4826 (1999).
Nomura, R. et al. Fgf16 is essential for pectoral fin bud formation in zebrafish. Biochem. Biophys. Res. Commun. 347, 340–346 (2006).
Mabee, P. M. Developmental data and phylogenetic systematics: evolution of the vertebrate limb. Am. Zool. 40, 789–800 (2000).
Coates, M. I. & Clack, J. A. Polydactyly in the earliest known tetrapod limbs. Nature 347, 66–69 (1990).
Tabin, C. J. Why we have (only) five fingers per hand: Hox genes and the evolution of paired limbs. Development 116, 289–296 (1992).
Walossek, D. The Upper Cambrian Rehbachiella and the phylogeny of Branchiopoda and Crustacea. Fossils Strata 32, 1–202 (1993).
Hughes, N. C., Minelli, A. & Fusco, G. The ontogeny of trilobite segmentation: a comparative approach. Paleobiology 32, 602–627 (2006).
Hunda, B. R. & Hughes, N. C. Evaluating paedomorphic heterochrony in trilobites: the case of the diminutive trilobite Flexicalymene retrorsa minuens from the Cincinnatian Series (Upper Ordovician), Cincinnati region. Evol. Dev. 9, 483–498 (2007).
Webster, M. A Cambrian peak in morphological variation within trilobite species. Science 317, 499–502 (2007).
Bowring, S. A. et al. Calibrating rates of early Cambrian evolution. Science 261, 1293–1298 (1993).
Martin, M. W. et al. Age of Neoproterozoic bilaterian body and trace fossils, White Sea, Russia: implications for metazoan evolution. Science 288, 841–845 (2000).
Rothman, D. H., Hayes, J. M. & Summons, R. E. Dynamics of the Neoproterozoic carbon cycle. Proc. Natl Acad. Sci. USA. 100, 8124–8129 (2003).
Erwin, D. H. & Davidson, E. H. The last common bilaterian ancestor. Development 129, 3021–3032 (2002).
Raff, R. A. The Shape of Life. Genes, Development, and the Evolution of Animal Form. (Univ. Chicago Press, Chicago, 1996).
Davidson, E. H. & Erwin, D. H. Gene regulatory networks and the evolution of animal body plans. Science 311, 796–800 (2006).
Larroux, C. et al. Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity. Evol. Dev. 8, 150–173 (2006).
Nichols, S. A., Dirks, W., Pearse, J. S. & King, N. Early evolution of animal cell signaling and adhesion genes. Proc. Natl Acad. Sci. USA 103, 12451–12456 (2006).
Donoghue, P. C. J. et al. Fossilized embryos are widespread but the record is temporally and taxonomically biased. Evol. Dev. 8, 232–238 (2006).
Steiner, M., Zhu, M., Li, G., Qian, Y. & Erdtmann, B.-D. New Early Cambrian bilaterian embryos and larvae from China. Geology 32, 833–836 (2004).
Briggs, D. E. G. The role of decay and mineralization in the preservation of soft-bodied fossils. Annu. Rev. Earth Planet Sci. 31, 275–301 (2003).
Raff, E. C., Villinski, J. T., Turner, F. R., Donoghue, P. C. & Raff, R. A. Experimental taphonomy shows the feasibility of fossil embryos. Proc. Natl Acad. Sci. USA 103, 5846–5851 (2006).
Hagadorn, J. W. et al. Cellular and subcellular structure of neoproterozoic animal embryos. Science 314, 291–294 (2006).
Dunn, E. F. et al. Molecular paleoecology: using gene regulatory analysis to address the origins of complex life cycles in the Late Precambrian. Evol. Dev. 9, 10–24 (2007). References 63 and 68 examine two approaches to the evolution of animal larvae and life history in the metazoan radiation. Fossil data and comparative developmental molecular data are complementary.
Nützel, A., Lehnert, O. & Frýda, J. Origin of planktotrophy — evidence from early mollusks. Evol. Dev. 8, 325–330 (2006).
Valentine, J. W. Ancestors and urbilateria. Evol. Dev. 8, 391–393 (2006).
Coates, M. & Ruta, M. Nice snake, shame about the legs. Trends Ecol. Evol. 15, 503–507 (2000).
Cohn, M. J. & Tickle, C. Developmental basis of limblessness and axial patterning in snakes. Nature 399, 474–479 (1999).
Xu, X. et al. Four-winged dinosaurs from China. Nature 421, 335–340 (2003).
Lin, C. M., Jiang, T. X., Widelitz, R. B. & Chuong, C. M. Molecular signaling in feather morphogenesis. Curr. Opin. Cell Biol. 18, 730–741 (2006).
Kukalova-Peck, J. Origin of the insect wing and wing articulation from the arthropodal leg. Can. J. Zool. 61, 1618–1669 (1983).
Jockusch, E. L. & Ober, K. A. Hypothesis testing in evolutionary developmental biology: a case study from insect wings. J. Hered. 95, 382–396 (2004).
Sun, G., Ji, Q., Dilcher, D. L., Zheng, S., Nixon, K. C. & Wang, X. Archaefructaceae, a new basal angiosperm family. Science 296, 899–904 (2002).
Hernández-Hernández, T., Martínez-Castilla, L. P. & Alvarez-Buylla, E. R. Functional diversification of B MADS-box homeotic regulators of flower development: adaptive evolution in protein–protein interaction domains after major gene duplication events. Mol. Biol. Evol. 24, 465–481 (2007).
Purugganan, M. D. The MADS-box floral homeotic gene lineages predate the origin of seed plants: phylogenetic and molecular clock estimates. J. Mol. Evol. 45, 392–396 (1997).
Acknowledgements
I thank M. Friedman and M. I. Coates for the figure used in Figure 5, S. Conway Morris and J. B. Caron for providing Figure 1, A. Moczek and P. C. J. Donoghue for helpful advice and M. I. Coates, E. C. Raff, J. W. Valentine and two anonymous reviewers for their critical reading and suggestions.
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Glossary
- Protostome
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(First mouth). The animal superphylum that contains annelids, molluscs, arthropods and several other phyla that are linked by a pattern of development and body organization that is distinct from deuterostomes, especially in development of the larval mouth.
- Deuterostome
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(Second mouth). The animal superphylum containing chordates, hemichordates and echinoderms. These are linked by their pattern of development, notably of the larval mouth.
- Bilaterians
-
Animals with a bilaterally symmetrical body plan.
- Tetrapod
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Vertebrates ancestrally having four legs.
- Taxon
-
Named groups of organisms that are arranged in the hierarchical taxonomic order: species, genus, family, order, class and phylum (plural taxa).
- Clade
-
A group of species in a phylogenetic tree that share a single ancestral species.
- Radula
-
A rasping organ in the mouth of molluscs that is equipped with chitinous teeth.
- Setae
-
Spine-like projections found in annelid worms and brachiopods.
- Chordates
-
Deuterostomes that possess a notochord. Vertebrates belong to the chordates.
- Hemichordates
-
Worm-like deuterostomes that are related to echinoderms.
- Crown groups
-
Crown groups represent the most derived living taxa in a clade.
- Pentameral
-
A fivefold radial body plan.
- Stem groups
-
Stem groups represent the less derived extinct branches of the phylogenetic tree.
- Stereom
-
The porous calcitic endoskeleton that is characteristic of echinoderms.
- Phylogeny
-
Evolutionary relationships among organisms shown in the diagrammatical form of phylogenetic trees.
- Sarcopterygians
-
A group that includes the lobe-fin fish, a once diverse fish group, and their tetrapod descendants.
- Homology
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Similarity in structural features such as genes or morphology that are derived from a shared ancestor by common descent.
- Lophotrochozoans
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A major division of protostome animals, including such phyla as brachiopods and other lophophore-bearing animals, plus molluscs, annelids and other phyla that develop via a trochophore larva.
- Metazoan
-
A multicellular animal.
- Homoplasy
-
False homology. Similar features that have evolved independently, as identified by their position in phylogenetic trees, are homoplastic.
- Orthologue
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Refers to a member of a gene families. The orthologue is the same member of a family across species.
- Cnidarians
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Jellyfish and their kin, which have a two-cell layer (diploblastic) organization that is simpler than that of bilaterians.
- Bayesian inference of phylogeny
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A method for inference of phylogenetic trees from data that gives the probability that a tree and model is correct given the data, using Bayes theorem to find posterior probability.
- Geminate species
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Species that were recently derived from a common ancestor.
- Meckel's cartilage
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The ancestral jaw of vertebrates, which evolved from an ancestral gill arch. Its derivatives include the bones of the lower jaw that are now parts of the mammalian middle ear.
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Raff, R. Written in stone: fossils, genes and evo–devo. Nat Rev Genet 8, 911–920 (2007). https://doi.org/10.1038/nrg2225
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DOI: https://doi.org/10.1038/nrg2225
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