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Cited by 360Morphological variations and asymmetryEvolution and Paleontology StudiesEvolution and Genetic Dynamics

The macroevolutionary consequences of phenotypic integration: from development to deep time

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Goswami, A., Smaers, J. B., Soligo, C., Polly, P. D.·2014·Philosophical Transactions of the Royal Society B: Biological Sciences
DOI 10.1098/rstb.2013.0254PMC PMC4084539
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Abstract

Phenotypic integration is a pervasive characteristic of organisms. Numerous analyses have demonstrated that patterns of phenotypic integration are conserved across large clades, but that significant variation also exists. For example, heterochronic shifts related to different mammalian reproductive strategies are reflected in postcranial skeletal integration and in coordination of bone ossification. Phenotypic integration and modularity have been hypothesized to shape morphological evolution, and we extended simulations to confirm that trait integration can influence both the trajectory and magnitude of response to selection. We further demonstrate that phenotypic integration can produce both more and less disparate organisms than would be expected under random walk models by repartitioning variance in preferred directions. This effect can also be expected to favour homoplasy and convergent evolution. New empirical analyses of the carnivoran cranium show that rates of evolution, in contrast, are not strongly influenced by phenotypic integration and show little relationship to morphological disparity, suggesting that phenotypic integration may shape the direction of evolutionary change, but not necessarily the speed of it. Nonetheless, phenotypic integration is problematic for morphological clocks and should be incorporated more widely into models that seek to accurately reconstruct both trait and organismal evolution.

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Integrity signals

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Crossref · 10.1098/rstb.2013.0254

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  • The macroevolutionary consequences of integration are likely to be highly dependent on the direction and magnitude of selection on each module.

    “Rather, the macroevolutionary consequences of integration are likely to be highly dependent on the direction and magnitude of selection on each module (13).”

    From Developmental origins of mosaic evolution in the avian cranium (2018) · cites this paper as [13]

    In “Phenotypic integration mediates evolutionary responses to selection” (page unavailable), the paper says that the direction of selection relative to the major axes of integrated traits affects the evolutionary response. It does not establish that macroevolutionary consequences depend on the magnitude of selection on each module: its simulations use selection vectors of unit length, and the magnitudes discussed are magnitudes of response or integration. (LLM, conf=0.85)

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  • Taken together, the results support the fundamental prediction that macroevolutionary patterns are shaped by phenotypic modularity and integration, which are in turn determined by developmental processes.

    “Taken together, these results support the fundamental prediction that macroevolutionary patterns are shaped by phenotypic modularity and integration, which are in turn determined by developmental processes (7, 11, 13, 16, 23).”

    From Developmental origins of mosaic evolution in the avian cranium (2018) · cites this paper as [13]

    The Conclusion reports that integration influences the trajectory and magnitude of evolutionary responses, supporting the link to macroevolutionary patterns. The “Integrating developmental timing” section describes developmental influences on integration, but also says functional influences may dominate later in ontogeny. The source therefore does not support the unqualified assertion that developmental processes determine modularity and integration. (LLM, conf=0.85)

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Cites

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Research works printed but not linked: 6

  1. [18]Schlosser G Wagner GP (eds) 2004 Modularity in development and evolution. Chicago, IL: University of Chicago Press.
  2. [28]Atchley WR 1993 Genetic and developmental aspects of variability in the mammalian mandible. In The skull. 1 Development (eds Hanken J Hall BK), pp. 207– 247. Chicago, IL: University of Chicago Press.
  3. [32]Cheverud JM 2004 Modular pleiotropic effects of quantitative trait loci on morphological traits. In Modularity in development and evolution (eds Schlosser G Wagner GP), pp. 132– 153. Chicago, IL: University of Chicago.
  4. [74]Schlosser G 2005 The role of modules in development and evolution. In Modularity in development and evolution (eds Schlosser G Wagner GP), pp. 519– 582. Chicago, IL: University of Chicago Press.
  5. [81]Shubin N Davis MC 2004 Modularity in the evolution of vertebrate appendages. In Modularity in development and evolution (eds Schlosser G Wagner GP), pp. 429– 440. Chicago, IL: University of Chicago Press.
  6. [97]Zelditch ML Sheets HD Fink WL 2001 The spatial complexity and evolutionary dynamics of growth. In Beyond heterochrony: the evolution of development (ed. Zelditch ML), pp. 145– 194. New York, NY: Wiley-Liss, Inc.

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Authors
Goswami, A., Smaers, J. B., Soligo, C., & Polly, P. D.
Affiliations
  • University College London (GB)
  • Indiana University Bloomington (US)
Corresponding author
Goswami, A.
ORCID
Venue
Philosophical Transactions of the Royal Society B: Biological Sciences
Publisher
The Royal Society
Published
2014-08-19
Volume
369
Issue
1649
Pages
20130254
ISSN
  • 0962-8436 (ISSN-L)
  • 1471-2970
DOI
10.1098/rstb.2013.0254
PMC
PMC4084539
OpenAlex
W2158213278
Cited by
359
References
133
Citations by year
2026: 20 · 2025: 30 · 2024: 27 · 2023: 39 · 2022: 30 · 2021: 40 · 2020: 30 · 2019: 42 · 2018: 34 · 2017: 19 · 2016: 26 · 2015: 17 · 2014: 5
FWCI
31.00
Type
journal article
Language
en
Open access
Licence
Locations
  • Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • UCL Discovery (University College London) (submittedVersion)
Funders
  • National Science Foundation (0308765, 0502186)
  • American Museum of Natural History
  • University of Chicago
  • Field Museum
  • Royal Society
  • University of New South Wales
  • National Museum of Natural History
  • Natural Environment Research Council (NE/J012432/1, NE/H022937/1)
  • Office of International Science and Engineering
  • University of California Museum of Paleontology
Topics
  • Physical Sciences › Mathematics › Geometry and Topology › Morphological variations and asymmetry
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Keywords
phenotypic integration, modularity, morphological evolution, heterochrony, postcranial skeleton, ossification, selection response, morphological disparity, homoplasy, convergent evolution, evolutionary rates, random walks
MeSH terms
Animals, Biological Evolution, Models, Biological, Phenotype, Phylogeny, Selection, Genetic, Time Factors, Vertebrates, Developmental Biology, Body Patterning, Biodiversity, Systems Biology

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