Developmental Plasticity and the Origin of Tetrapods

Overview

Journal Nature

Specialty Science

Date 2014 Aug 28

PMID 25162530

Citations 57

Authors

Emily M Standen

Trina Y Du

Hans C E Larsson

Affiliations

Soon will be listed here.

Abstract

The origin of tetrapods from their fish antecedents, approximately 400 million years ago, was coupled with the origin of terrestrial locomotion and the evolution of supporting limbs. Polypterus is a member of the basal-most group of ray-finned fish (actinopterygians) and has many plesiomorphic morphologies that are comparable to elpistostegid fishes, which are stem tetrapods. Polypterus therefore serves as an extant analogue of stem tetrapods, allowing us to examine how developmental plasticity affects the 'terrestrialization' of fish. We measured the developmental plasticity of anatomical and biomechanical responses in Polypterus reared on land. Here we show the remarkable correspondence between the environmentally induced phenotypes of terrestrialized Polypterus and the ancient anatomical changes in stem tetrapods, and we provide insight into stem tetrapod behavioural evolution. Our results raise the possibility that environmentally induced developmental plasticity facilitated the origin of the terrestrial traits that led to tetrapods.

Citing Articles

Co-option of neck muscles supported the vertebrate water-to-land transition.

Heude E, Dutel H, Sanchez-Garrido F, Prummel K, Lalonde R, Lam F Nat Commun. 2024; 15(1):10564.

PMID: 39632846 PMC: 11618326. DOI: 10.1038/s41467-024-54724-x.

Comparisons of developmental processes of air-breathing organs among terrestrial isopods (Crustacea, Oniscidea): implications for their evolutionary origins.

Inui N, Miura T Evodevo. 2024; 15(1):9.

PMID: 39026371 PMC: 11264735. DOI: 10.1186/s13227-024-00229-z.

Anatomical insights into fish terrestrial locomotion: A study of barred mudskipper (Periophthalmus argentilineatus) fins based on μCT 3D reconstructions.

Ziadi-Kunzli F, Maeda K, Puchenkov P, Bandi M J Anat. 2024; 245(4):593-624.

PMID: 38845054 PMC: 11424826. DOI: 10.1111/joa.14071.

Early onset of urea synthesis and ammonia detoxification pathways in three terrestrially developing frogs.

Mendez-Narvaez J, Warkentin K J Comp Physiol B. 2023; 193(5):523-543.

PMID: 37639061 DOI: 10.1007/s00360-023-01506-4.

Darwin's agential materials: evolutionary implications of multiscale competency in developmental biology.

Levin M Cell Mol Life Sci. 2023; 80(6):142.

PMID: 37156924 PMC: 10167196. DOI: 10.1007/s00018-023-04790-z.

References

Inoue J, Miya M, Tsukamoto K, Nishida M . Basal actinopterygian relationships: a mitogenomic perspective on the phylogeny of the "ancient fish". Mol Phylogenet Evol. 2002; 26(1):110-20. DOI: 10.1016/s1055-7903(02)00331-7. View

Ahlberg P, Clack J . Palaeontology: a firm step from water to land. Nature. 2006; 440(7085):747-9. DOI: 10.1038/440747a. View

Frost H . On our age-related bone loss: insights from a new paradigm. J Bone Miner Res. 1997; 12(10):1539-46. DOI: 10.1359/jbmr.1997.12.10.1539. View

Shen L, Farid H, McPeek M . Modeling three-dimensional morphological structures using spherical harmonics. Evolution. 2009; 63(4):1003-16. PMC: 2936781. DOI: 10.1111/j.1558-5646.2008.00557.x. View

Styner M, Oguz I, Xu S, Brechbuhler C, Pantazis D, Levitt J . Framework for the Statistical Shape Analysis of Brain Structures using SPHARM-PDM. Insight J. 2011; (1071):242-250. PMC: 3062073. View

Le Rouzic A, Carlborg O . Evolutionary potential of hidden genetic variation. Trends Ecol Evol. 2007; 23(1):33-7. DOI: 10.1016/j.tree.2007.09.014. View

Yeh P, Price T . Adaptive phenotypic plasticity and the successful colonization of a novel environment. Am Nat. 2004; 164(4):531-42. DOI: 10.1086/423825. View

Suzuki Y, Nijhout H . Evolution of a polyphenism by genetic accommodation. Science. 2006; 311(5761):650-2. DOI: 10.1126/science.1118888. View

Kawano S, Blob R . Propulsive forces of mudskipper fins and salamander limbs during terrestrial locomotion: implications for the invasion of land. Integr Comp Biol. 2013; 53(2):283-94. DOI: 10.1093/icb/ict051. View

10.

Biewener A . Scaling body support in mammals: limb posture and muscle mechanics. Science. 1989; 245(4913):45-8. DOI: 10.1126/science.2740914. View

11.

Moczek A, Sultan S, Foster S, Ledon-Rettig C, Dworkin I, Nijhout H . The role of developmental plasticity in evolutionary innovation. Proc Biol Sci. 2011; 278(1719):2705-13. PMC: 3145196. DOI: 10.1098/rspb.2011.0971. View

12.

Wund M, Baker J, Clancy B, Golub J, Foster S . A test of the "flexible stem" model of evolution: ancestral plasticity, genetic accommodation, and morphological divergence in the threespine stickleback radiation. Am Nat. 2008; 172(4):449-62. DOI: 10.1086/590966. View

13.

Callier V, Clack J, Ahlberg P . Contrasting developmental trajectories in the earliest known tetrapod forelimbs. Science. 2009; 324(5925):364-7. DOI: 10.1126/science.1167542. View

14.

Crispo E . The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. Evolution. 2007; 61(11):2469-79. DOI: 10.1111/j.1558-5646.2007.00203.x. View

15.

Niedzwiedzki G, Szrek P, Narkiewicz K, Narkiewicz M, Ahlberg P . Tetrapod trackways from the early Middle Devonian period of Poland. Nature. 2010; 463(7277):43-8. DOI: 10.1038/nature08623. View

16.

Price T, Qvarnstrom A, Irwin D . The role of phenotypic plasticity in driving genetic evolution. Proc Biol Sci. 2003; 270(1523):1433-40. PMC: 1691402. DOI: 10.1098/rspb.2003.2372. View

17.

Rajakumar R, San Mauro D, Dijkstra M, Huang M, Wheeler D, Hiou-Tim F . Ancestral developmental potential facilitates parallel evolution in ants. Science. 2012; 335(6064):79-82. DOI: 10.1126/science.1211451. View

18.

Badyaev A . Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation. Proc Biol Sci. 2005; 272(1566):877-86. PMC: 1564094. DOI: 10.1098/rspb.2004.3045. View

19.

Gomez-Mestre I, Buchholz D . Developmental plasticity mirrors differences among taxa in spadefoot toads linking plasticity and diversity. Proc Natl Acad Sci U S A. 2006; 103(50):19021-6. PMC: 1748170. DOI: 10.1073/pnas.0603562103. View

20.

Hedrick T . Software techniques for two- and three-dimensional kinematic measurements of biological and biomimetic systems. Bioinspir Biomim. 2008; 3(3):034001. DOI: 10.1088/1748-3182/3/3/034001. View