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Evolution; international journal of organic evolution2013; 67(12); 3645-3652; doi: 10.1111/evo.12204

Constraints on Mammalian forelimb development: insights from developmental disparity.

Abstract: Tetrapod limb development has been studied extensively for decades, yet the strength and role of developmental constraints in this process remains unresolved. Mammals exhibit a particularly wide array of limb morphologies associated with various locomotion modes and behaviors, providing a useful system for identifying periods of developmental constraint and conserved developmental mechanisms or morphologies. In this study, landmark-based geometric morphometrics are used to investigate levels and patterns of morphological diversity (disparity) among the developing forelimbs of four mammals with diverse limb morphologies: mice, opossums, horses, and pigs. Results indicate that disparity among the forelimbs of these species slightly decreases or stays the same from the appearance of the limb ridge to the bud stage, and increases dramatically from the paddle through tissue regression stages. Heterochrony exhibited by the precocial opossum limb was not found to drive these patterns of morphological disparity, suggesting that the low disparity of the middle stages of limb development (e.g., paddle stage) is driven by processes operating within the limb and is likely not a result of embryo-wide constraint.
Publication Date: 2013-09-12 PubMed ID: 24299415DOI: 10.1111/evo.12204Google Scholar: Lookup
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  • Journal Article
  • Research Support
  • N.I.H.
  • Extramural
  • Research Support
  • Non-U.S. Gov't
  • Research Support
  • U.S. Gov't
  • Non-P.H.S.

Summary

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This study explores the variations in the development of forelimbs in four different types of mammals to understand the role of developmental constraints. The research found that the differences in forelimb development amongst these creatures either slightly decreases or remains the same at early developmental stages, but then markedly increases at later stages.

Understanding the Context

In this research, the authors are investigating a concept in evolutionary biology termed ‘developmental constraints.’ These are restrictions and biases on the course of an organism’s development, which limit the phenotypic variability (variation in physical and physiological traits) that natural selection can act upon. Developmental constraints can shape the course of evolution by restricting certain morphologies (shapes) from developing, while enabling and preserving others. Here, the authors want to understand the influence of these constraints on mammalian forelimb development.

The Study Subjects

  • The species studied are mice, opossums, horses, and pigs, each possessing distinct forelimb configurations and capabilities needed for their unique behaviors and locomotion modes.

Methods Employed: Geometric Morphometrics

  • The researchers used a technique called ‘landmark-based geometric morphometrics’ to compare shape variations among the forelimbs of the four chosen mammals during their development.
  • Geometric morphometrics is a method of statistically analyzing and comparing biological forms (shapes and configurations) based on spatial data on the locations of certain ‘landmarks’ on their structure.

Research Findings: Disparity in Limb Development

  • The study shows that in the early stages of limb development, up until the bud stage, disparity between these species either decreases or stays the same.
  • A significant increase in disparity is seen from the paddle stage through tissue regression stages, indicating a greater degree of morphological variation between the species as development progresses.
  • The research did not find evidence to suggest that the differing timings of limb development in the four species (heterochrony), apprehended here by examining the precocial opossum limb, influence this disparity in forelimb shape.

Interpreting the Results: Constraints and Morphological Variation

  • The researchers concluded that the lesser disparity during the middle stages of limb development (exemplified by the paddle stage) is governed by processes intrinsic to the limb’s development and not by constraints affecting the entire embryo.
  • This could suggest a period of developmental constraint where the forelimb morphology is conserved across species.

Cite This Article

APA
Ross D, Marcot JD, Betteridge KJ, Nascone-Yoder N, Bailey CS, Sears KE. (2013). Constraints on Mammalian forelimb development: insights from developmental disparity. Evolution, 67(12), 3645-3652. https://doi.org/10.1111/evo.12204

Publication

ISSN: 1558-5646
NlmUniqueID: 0373224
Country: United States
Language: English
Volume: 67
Issue: 12
Pages: 3645-3652

Researcher Affiliations

Ross, Darcy
  • School of Integrative Biology, 505 South Goodwin Avenue, University of Illinois, Urbana, Illiniosis, 61801; Current address: Department of Organismal Biology and Anatomy, University of Chicago, Chicago, Illiniosis, 60637.
Marcot, Jonathan D
    Betteridge, Keith J
      Nascone-Yoder, Nanette
        Bailey, C Scott
          Sears, Karen E

            MeSH Terms

            • Animals
            • Evolution, Molecular
            • Forelimb / anatomy & histology
            • Forelimb / embryology
            • Horses / embryology
            • Horses / genetics
            • Mice / embryology
            • Mice / genetics
            • Opossums / embryology
            • Opossums / genetics
            • Swine / embryology
            • Swine / genetics

            Grant Funding

            • HD050042-01 / NICHD NIH HHS

            Citations

            This article has been cited 6 times.
            1. Rothier PS, Fabre AC, Clavel J, Benson RBJ, Herrel A. Mammalian forelimb evolution is driven by uneven proximal-to-distal morphological diversity.. Elife 2023 Jan 26;12.
              doi: 10.7554/eLife.81492pubmed: 36700542google scholar: lookup
            2. Botton-Divet L, Nyakatura JA. Vertical clinging and leaping induced evolutionary rate shifts in postcranial evolution of tamarins and marmosets (Primates, Callitrichidae).. BMC Ecol Evol 2021 Jun 25;21(1):132.
              doi: 10.1186/s12862-021-01848-zpubmed: 34171986google scholar: lookup
            3. Howenstine AO, Sadier A, Anthwal N, Lau CL, Sears KE. Non-model systems in mammalian forelimb evo-devo.. Curr Opin Genet Dev 2021 Aug;69:65-71.
              doi: 10.1016/j.gde.2021.01.012pubmed: 33684847google scholar: lookup
            4. López-Aguirre C, Hand SJ, Koyabu D, Son NT, Wilson LAB. Postcranial heterochrony, modularity, integration and disparity in the prenatal ossification in bats (Chiroptera).. BMC Evol Biol 2019 Mar 12;19(1):75.
              doi: 10.1186/s12862-019-1396-1pubmed: 30866800google scholar: lookup
            5. Maier JA, Rivas-Astroza M, Deng J, Dowling A, Oboikovitz P, Cao X, Behringer RR, Cretekos CJ, Rasweiler JJ 4th, Zhong S, Sears KE. Transcriptomic insights into the genetic basis of mammalian limb diversity.. BMC Evol Biol 2017 Mar 23;17(1):86.
              doi: 10.1186/s12862-017-0902-6pubmed: 28335721google scholar: lookup
            6. Marcy AE, Hadly EA, Sherratt E, Garland K, Weisbecker V. Getting a head in hard soils: Convergent skull evolution and divergent allometric patterns explain shape variation in a highly diverse genus of pocket gophers (Thomomys).. BMC Evol Biol 2016 Oct 10;16(1):207.
              doi: 10.1186/s12862-016-0782-1pubmed: 27724858google scholar: lookup