The origin of higher taxa: macroevolutionary processes, and the case of the mammals
Abstract
Abstract The origin of a new higher taxon is characterized by a long‐term phylogenetic trend, involving evolutionary changes in a large number of characters. At this phylogenetic level, the conflict between internal integration of the phenotype and its evolvability can be resolved by the correlated progression model, in which many disparate traits evolve by a sequence of small increments in loose correlation with one another, rather than by the modularity model. The trend leading to the new higher taxon implies the existence of a long ridge in an adaptive landscape. An evolutionary lineage tracking it requires adaptive changes in broad biological characteristics, involving many traits. Species selection is a possible additional driver of the trend. These conclusions are tested against the synapsid fossil record of the origin of mammals. The reconstructed sequence of acquisition of mammalian traits supports the correlated progression model. The adaptive ridge involved is postulated to have been a sequence of overlapping niches requiring increasing ability to remain active in daily and seasonally fluctuating environments by means of increasing internal regulation. An inferred speciation bias in favour of relatively small, relatively more progressive carnivores indicates that species selection was also involved in driving the trend. Palaeoenvironmental evidence indicates that ecological opportunity probably played a role at certain points along the lineage.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The expectation of morphological novelty differs depending on the specific drivers of an individual adaptive radiation.
“Thus, the expectation of morphological novelty differs depending on the specific drivers of an individual adaptive radiation [74–80].”
From Novelty and Innovation in the History of Life (2015) · cites this paper as [79]
Cites
The Origins of Order: Self-Organization and Selection in Evolution
Kauffman, S. A. (1993) · doi:10.1093/oso/9780195079517.001.0001 · Cited by 7,855 · see citing works
The Neutral Theory of Molecular Evolution
Kimura, M. (1979) · Scientific American · doi:10.1038/scientificamerican1179-98 · Cited by 7,698 · see citing works
The origins of order; self organization and selection in evolution
Kauffman, S. A. (1994) · International Journal of Biochemistry · doi:10.1016/0020-711x(94)90119-8 · Cited by 6,753 · see citing works
The Neutral Theory of Molecular Evolution
Kimura, M. (1983) · Cambridge University Press eBooks · doi:10.1017/cbo9780511623486 · Cited by 6,300 · see citing works
The Ecology of Adaptive Radiation
Schluter, D. (2000) · doi:10.1093/oso/9780198505235.001.0001 · Cited by 4,974 · see citing works
The Structure of Evolutionary Theory
Gould, S. J. (2002) · Harvard University Press eBooks · doi:10.4159/9780674417922 · Cited by 3,150 · see citing works
The structure of evolutionary theory
Gould, S. J. (2002) · Choice Reviews Online · doi:10.5860/choice.39-6411 · Cited by 2,764 · see citing works
QUANTITATIVE GENETIC ANALYSIS OF MULTIVARIATE EVOLUTION, APPLIED TO BRAIN:BODY SIZE ALLOMETRY
Lande, R. (1979) · Evolution · doi:10.1111/j.1558-5646.1979.tb04694.x · Cited by 2,648 · see citing works
Quantitative genetic analysis of multivariate evolution, applied to brain: body size allometry
Lande, R. (1979) · Evolution · doi:10.2307/2407630 · Cited by 2,648 · see citing works
The growth of biological thought. Diversity, evolution, and inheritance
Farner, D. S. (1983) · The Auk · doi:10.1093/auk/100.2.507 · Cited by 2,511 · see citing works
The Growth of Biological Thought: Diversity, Evolution, and Inheritance
Mayr, E. (1982) · CERN Document Server (European Organization for Nuclear Research) · Cited by 2,295 · see citing works
PERSPECTIVE: COMPLEX ADAPTATIONS AND THE EVOLUTION OF EVOLVABILITY
Wagner, G. P., & Altenberg, L. (1996) · Evolution · doi:10.1111/j.1558-5646.1996.tb02339.x · Cited by 2,065 · see citing works
(1945) · Annals of the Entomological Society of America · doi:10.1093/aesa/38.3.396 · Cited by 1,859 · see citing works
Simpson, G. G. (2005) · Kluwer Academic Publishers eBooks · doi:10.1007/0-306-47468-9_7 · Cited by 1,657 · see citing works
DESATURASE‐2 , ENVIRONMENTAL ADAPTATION, AND SEXUAL ISOLATION IN DROSOPHILA MELANOGASTER
Coyne, J. A., & Elwyn, S. (2006) · Evolution · doi:10.1111/j.0014-3820.2006.tb01143.x · Cited by 1,576 · see citing works
Raff, R. A. (1996) · University of Chicago Press eBooks · doi:10.7208/chicago/9780226256573.001.0001 · Cited by 1,249 · see citing works
Kirschner, M., & Gerhart, J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.15.8420 · Cited by 1,129 · see citing works
Wolpert, L., Tickle, C. A., Arias, A. M., Lawrence, P. A., & Locke, J. C. W. (2019) · Oxford University Press eBooks · doi:10.1093/hesc/9780198800569.001.0001 · Cited by 991 · see citing works
Lewontin, R. C. (1978) · Scientific American · doi:10.1038/scientificamerican0978-212 · Cited by 851 · see citing works
Mammals from the Age of Dinosaurs
Kielan‐Jaworowska, Z., Cifelli, R. L., & Luo, Z. (2004) · Columbia University Press eBooks · doi:10.7312/kiel11918 · Cited by 841 · see citing works
Haldane, J. B. S. (1957) · Journal of Genetics · doi:10.1007/bf02984069 · Cited by 761 · see citing works
Natural Selection: Domains, Levels and Challenges
Williams, G. C. (1992) · doi:10.1093/oso/9780195069327.001.0001 · Cited by 741 · see citing works
Heterochrony and allometry: the analysis of evolutionary change in ontogeny
Klingenberg, C. P. (1998) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1017/s000632319800512x · Cited by 712 · see citing works
Evolutionary Strategies and Morphological Innovations: Cichlid Pharyngeal Jaws
Liem, K. (1973) · Systematic Zoology · doi:10.2307/2412950 · Cited by 684 · see citing works
Natural Selection: Domains, Levels, and Challenges
Pagel, M. D., & Williams, G. C. (1994) · Journal of Animal Ecology · doi:10.2307/5601 · Cited by 649 · see citing works
The Evolution of Morphological Diversity
Foote, M. (1997) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.ecolsys.28.1.129 · Cited by 648 · see citing works
Gould, S. J. (1996) · Art Journal · doi:10.1080/00043249.1996.10791738 · Cited by 562 · see citing works
Cope's Rule and the Dynamics of Body Mass Evolution in North American Fossil Mammals
Alroy, J. (1998) · Science · doi:10.1126/science.280.5364.731 · Cited by 539 · see citing works
Romer, A. S., & Price, L. I. (1940) · Geological Society of America Special Papers · doi:10.1130/spe28-p1 · Cited by 507 · see citing works
The Origin and Evolution of Mammals
Kemp, T. S. (2004) · Oxford University Press eBooks · doi:10.1093/oso/9780198507604.001.0001 · Cited by 494 · see citing works
Self-citationThe adaptive landscape as a conceptual bridge between micro- and macroevolution
Arnold, S. J., Pfrender, M. E., & Jones, A. G. (2001) · Genetica · doi:10.1023/a:1013373907708 · Cited by 485 · see citing works
Mammal-Like Reptiles and the Origin of Mammals.
Gaffney, E. S., & Kemp, T. S. (1982) · Systematic Zoology · doi:10.2307/2413376 · Cited by 472 · see citing works
Self-citationA Devonian tetrapod-like fish and the evolution of the tetrapod body plan
Daeschler, E. B., Shubin, N. H., & Jenkins, F. A. (2006) · Nature · doi:10.1038/nature04639 · Cited by 442 · see citing works
The adaptive landscape as a conceptual bridge between micro- and macroevolution
Arnold, S. J., Pfrender, M. E., & Jones, A. G. (2001) · Contemporary issues in genetics and evolution · doi:10.1007/978-94-010-0585-2_2 · Cited by 438 · see citing works
INDIVIDUAL-LEVEL SELECTION AS A CAUSE OF COPE'S RULE OF PHYLETIC SIZE INCREASE
Kingsolver, J. G., & Pfennig, D. W. (2004) · Evolution · doi:10.1111/j.0014-3820.2004.tb01740.x · Cited by 391 · see citing works
MECHANISMS OF LARGE-SCALE EVOLUTIONARY TRENDS
McShea, D. W. (1994) · Evolution · doi:10.1111/j.1558-5646.1994.tb02211.x · Cited by 383 · see citing works
The pectoral fin of Tiktaalik roseae and the origin of the tetrapod limb
Shubin, N. H., Daeschler, E. B., & Jenkins, F. A. (2006) · Nature · doi:10.1038/nature04637 · Cited by 377 · see citing works
Order in Living Organisms: A Systems Analysis of Evolution.
(1980) · doi:10.2307/2412636 · Cited by 359 · see citing works
Comparative Physiology: Primitive Mammals
Schmidt‐Nielsen, K., Bolis, L. C., & Taylor, C. R. (2009) · Medical Entomology and Zoology · Cited by 357 · see citing works
Key innovations and the ecology of macroevolution
Hunter, J. P. (1998) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(97)01273-1 · Cited by 340 · see citing works
Evolution of homeothermy in mammals
Crompton, A. W., Taylor, C. R., & Jagger, J. A. (1978) · Nature · doi:10.1038/272333a0 · Cited by 317 · see citing works
Is modularity necessary for evolvability?
Hansen, T. F. (2003) · Biosystems · doi:10.1016/s0303-2647(02)00132-6 · Cited by 313 · see citing works
Heterochrony and allometry: the analysis of evolutionary change in ontogeny
Klingenberg, C. P. (1998) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.1997.tb00026.x · Cited by 292 · see citing works
History of the Concept of Allometry
Gayon, J. (2000) · American Zoologist · doi:10.1093/icb/40.5.748 · Cited by 283 · see citing works
Evolutionary change and heterochrony
(1996) · Choice Reviews Online · doi:10.5860/choice.34-1531 · Cited by 276 · see citing works
Species selection on variability.
Lloyd, E. A., & Gould, S. J. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.2.595 · Cited by 270 · see citing works
The Evolution of Endothermy in Mammals and Birds: From Physiology to Fossils
Ruben, J. A. (1995) · Annual Review of Physiology · doi:10.1146/annurev.ph.57.030195.000441 · Cited by 267 · see citing works
Farmer, C. G. (2000) · The American Naturalist · doi:10.1086/303323 · Cited by 266 · see citing works
The hypocone as a key innovation in mammalian evolution.
Hunter, J. P., & Jernvall, J. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.23.10718 · Cited by 259 · see citing works
Gould, S. J. (1991) · Paleobiology · doi:10.1017/s0094837300010745 · Cited by 236 · see citing works
Evolvability, Stabilizing Selection, and the Problem of Stasis
Hansen, T. F., & Houle, D. (2004) · doi:10.1093/oso/9780195160437.003.0006 · Cited by 229 · see citing works
Revealing the factors that promote speciation
Barraclough, T. G., Vogler, A. P., & Harvey, P. (1998) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1998.0206 · Cited by 228 · see citing works
Darwinism evolving: systems dynamics and the genealogy of natural selection
(1995) · Choice Reviews Online · doi:10.5860/choice.33-0913 · Cited by 223 · see citing works
Gould, S. J., & Lloyd, E. A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.21.11904 · Cited by 214 · see citing works
Modularity in Development and Why It Matters to Evo-Devo1
Bolker, J. A. (2000) · American Zoologist · doi:10.1668/0003-1569(2000)040[0770:midawi]2.0.co;2 · Cited by 213 · see citing works
History of the Concept of Allometry1
Gayon, J. (2000) · American Zoologist · doi:10.1668/0003-1569(2000)040[0748:hotcoa]2.0.co;2 · Cited by 206 · see citing works
The postcranial skeletons of the Triassic mammals Eozostrodon, Megazostrodon and Erythrotherium
F. A. Jenkins, Jr., & Parrington, F. R. (1976) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1976.0022 · Cited by 194 · see citing works
Wagner, G. P. (1988) · Journal of Evolutionary Biology · doi:10.1046/j.1420-9101.1988.1010045.x · Cited by 192 · see citing works
Gaining ground: the origin and evolution of tetrapods
(2002) · Choice Reviews Online · doi:10.5860/choice.40-2180 · Cited by 192 · see citing works
Energy assimilation, parental care and the evolution of endothermy
Koteja, P. (2000) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2000.1025 · Cited by 189 · see citing works
PLEIOTROPIC EFFECTS OF INDIVIDUAL GENE LOCI ON MANDIBULAR MORPHOLOGY
Cheverud, J. M., Routman, E. J., & Irschick, D. J. (1997) · Evolution · doi:10.1111/j.1558-5646.1997.tb05122.x · Cited by 189 · see citing works
Evidence-Based Practice in Augmentative and Alternative Communication
Schlosser, R. W., & Raghavendra, P. (2004) · Augmentative and Alternative Communication · doi:10.1080/07434610310001621083 · Cited by 184 · see citing works
Macroevolution is more than repeated rounds of microevolution
Erwin, D. H. (2000) · Evolution & Development · doi:10.1046/j.1525-142x.2000.00045.x · Cited by 177 · see citing works
Yang, A. S. (2001) · Evolution & Development · doi:10.1046/j.1525-142x.2001.003002059.x · Cited by 171 · see citing works
Darwinism Evolving: Systems Dynamics and the Genealogy of Natural Selection
Depew, D. J., & Weber, B. H. F. (1994) · Cited by 167 · see citing works
The Evolution of Endothermy in the Phylogeny of Mammals
McNab, B. K. (1978) · The American Naturalist · doi:10.1086/283249 · Cited by 161 · see citing works
Strachan, T., & Read, A. F. (2018) · Human Molecular Genetics · doi:10.4324/9780203833544-5 · Cited by 157 · see citing works
Cheetham, A. H. (1986) · Paleobiology · doi:10.1017/s0094837300013658 · Cited by 156 · see citing works
Ruta, M., Wagner, P. J., & Coates, M. I. (2006) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2006.3577 · Cited by 155 · see citing works
Monteiro, L. R., Bonato, V., & dos Reis, S. F. (2005) · Evolution & Development · doi:10.1111/j.1525-142x.2005.05047.x · Cited by 153 · see citing works
Whyte, L. L. (1964) · Acta Biotheoretica · doi:10.1007/bf01602054 · Cited by 150 · see citing works
Sidor, C. A., & Hopson, J. A. (1998) · Paleobiology · doi:10.1666/0094-8373(1998)024[0254:glaatt]2.3.co;2 · Cited by 145 · see citing works
The origin of mammalian endothermy: a paradigm for the evolution of complex biological structure
Kemp, T. S. (2006) · Zoological Journal of the Linnean Society · doi:10.1111/j.1096-3642.2006.00226.x · Cited by 145 · see citing works
Self-citationHill, G. E., & McGraw, K. J. (2006) · Harvard University Press eBooks · Cited by 143 · see citing works
Arthropod body‐plan evolution in the Cambrian with an example from anomalocaridid muscle
Budd, G. E. (1998) · Lethaia · doi:10.1111/j.1502-3931.1998.tb00508.x · Cited by 130 · see citing works
POSSIBLE LARGEST-SCALE TRENDS IN ORGANISMAL EVOLUTION: Eight “Live Hypotheses”
McShea, D. W. (1998) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.ecolsys.29.1.293 · Cited by 125 · see citing works
The origin and early radiation of the therapsid mammal-like reptiles: a palaeobiological hypothesis
Kemp, T. S. (2006) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2005.01076.x · Cited by 110 · see citing works
Self-citationGrantham, T. A. (1995) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.es.26.110195.001505 · Cited by 110 · see citing works
Abdala, F. (2007) · Palaeontology · doi:10.1111/j.1475-4983.2007.00646.x · Cited by 108 · see citing works
Correlated progression and the origin of turtles
Lee, M. S. Y. (1996) · Nature · doi:10.1038/379812a0 · Cited by 105 · see citing works
Function and the Evolution of Phenotypic Stability: Connecting Pattern to Process
Schwenk, K., & Wagner, G. P. (2001) · American Zoologist · doi:10.1093/icb/41.3.552 · Cited by 98 · see citing works
THE EVOLUTION OF MAMMALIAN CHARACTERS
Olson, E. C. (1959) · Evolution · doi:10.1111/j.1558-5646.1959.tb03021.x · Cited by 84 · see citing works
Integration, Modules, and Development: Molecules to Morphology to Evolution
Klingenberg, C. P. (2004) · Oxford University Press eBooks · doi:10.1093/oso/9780195160437.003.0010 · Cited by 82 · see citing works
Modularity and the units of evolution
Schlosser, G. (2002) · Theory in Biosciences · doi:10.1078/1431-7613-00049 · Cited by 80 · see citing works
Phenotypic Integration as a Constraint and Adaptation
Merilä, J., & Björklund, M. (2004) · doi:10.1093/oso/9780195160437.003.0005 · Cited by 77 · see citing works
(1965) · doi:10.1063/1.3046950 · Cited by 66 · see citing works
Pleiotropic mutation, modularity and evolvability
Griswold, C. K. (2006) · Evolution & Development · doi:10.1111/j.1525-142x.2006.05077.x · Cited by 65 · see citing works
Tempo of evolution in a Neogene bryozoan: are trends in single morphologic characters misleading?
Cheetham, A. H. (1987) · Paleobiology · doi:10.1017/s0094837300008873 · Cited by 62 · see citing works
Closing the gaps among a web of DNA repair disorders
Michelson, R. J., & Weinert, T. A. (2000) · BioEssays · doi:10.1002/1521-1878(200011)22:11 · Cited by 61 · see citing works
The Evolution of the Tetrapod Middle Ear in the Rhipidistian-Amphibian Transition
Thomson, K. S. (1966) · American Zoologist · doi:10.1093/icb/6.3.379 · Cited by 56 · see citing works
Jenkins, F. A. (1970) · Biodiversity Heritage Library (Smithsonian Institution) · doi:10.5962/bhl.part.6259 · Cited by 56 · see citing works
The phenogenetic logic of life
Weiss, K. M. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1502 · Cited by 55 · see citing works
Wall, W. J. (2021) · doi:10.1002/9781119828624.ch6 · Cited by 48 · see citing works
Speciation and sorting as the source of evolutionary trends, or 'things are seldom what they seem'
Gould, S. J., & McNamara, K. J. (1990) · Cited by 47 · see citing works
Farmer (2000) · The American Naturalist · doi:10.2307/3078869 · Cited by 43 · see citing works
Basic questions in paleontology: Geologic time, organic evolution, and biological systematics
Morris, S. C. (1994) · Trends in Ecology & Evolution · doi:10.1016/0169-5347(94)90070-1 · Cited by 41 · see citing works
The Evolution of Mammalian Characters
Olson, E. C. (1959) · Evolution · doi:10.2307/2406111 · Cited by 37 · see citing works
The Evolution of Allometry in Modular Organisms
Preston, K. A., & Ackerly, D. D. (2004) · doi:10.1093/oso/9780195160437.003.0004 · Cited by 36 · see citing works
Thermal physiology and the origin of terrestriality in vertebrates
Carroll, R. L., Irwin, J. T., & Green, D. M. (2005) · Zoological Journal of the Linnean Society · doi:10.1111/j.1096-3642.2005.00151.x · Cited by 35 · see citing works
Bardack, D. (1972) · Evolution · doi:10.1111/j.1558-5646.1972.tb01954.x · Cited by 26 · see citing works
Form, Function, and Life History: Spatial and Temporal Dynamics of Integration
Zelditch, M. L., & Moscarella, R. A. (2004) · doi:10.1093/oso/9780195160437.003.0013 · Cited by 11 · see citing works
Form, function, and life history
Zelditch, M. L., & Moscarella, R. A. (2004) · Cited by 1 · see citing works
Collins, A. G. (2000) · doi:10.1666/0094-8373(2000)026
Flagged first, then by citations
Cited by
Sorted by citations
Novelty and Innovation in the History of Life
Erwin, D. H. (2015) · Current Biology · doi:10.1016/j.cub.2015.08.019 · Cited by 211 · see citing works
Distinguishing heat from light in debate over controversial fossils
Donoghue, P. C. J., & Purnell, M. A. (2009) · BioEssays · doi:10.1002/bies.200800128 · Cited by 160 · see citing works
Macroevolutionary patterns of body plan canalization in euarthropods
Aria, C. (2020) · Paleobiology · doi:10.1017/pab.2020.36 · Cited by 28 · see citing works
- Authors
- Kemp, T. S.
- Affiliations
- University of Oxford (GB)
- Corresponding author
- Kemp, T. S.
- Venue
- Acta Zoologica
- Publisher
- Wiley
- Published
- 2006-12-15
- Volume
- 88
- Issue
- 1
- Pages
- 3-22
- ISSN
- 0001-7272 (ISSN-L)
- 1463-6395
- OpenAlex
- W2106540379
- Cited by
- 49
- References
- 104
- Citations by year
- 2025: 3 · 2024: 2 · 2023: 2 · 2022: 2 · 2020: 3 · 2019: 1 · 2018: 1 · 2017: 2 · 2016: 1 · 2015: 3 · 2014: 7 · 2013: 1 · 2012: 4
- FWCI
- 3.65
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Acta Zoologica (publishedVersion)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Physical Sciences › Mathematics › Geometry and Topology › Morphological variations and asymmetry
- Keywords
- macroevolution, mammals, synapsids, fitness landscape, species selection, phylogenetic trends, ecological opportunity, carnivores, fossil record, paleoenvironment
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review