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Developmental plasticity and the origin of tetrapods

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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.

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Figure 1: Kinematic behaviour of swimming and walking Polypterus.
Figure 2: Timing of kinematic variables for the left fin during walking in control and treatment group fish.
Figure 3: Anatomical plasticity of Polypterus pectoral girdles.
Figure 4: Scenario for the contribution of developmental plasticity to large-scale evolutionary change in stem tetrapods.

Change history

  • 03 September 2014

    The Fig. 4 legend has been updated.

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Acknowledgements

We thank F. A. Jenkins Jr and C. R. Marshall for encouragement and discussions with E.M.S. during the initial phases of this project. We also thank E. Abouheif for discussions and editing of the manuscript. We thank J. Dawson for the loan of camera equipment, S. Bertram for access to laboratory space while running the experiment and B. Bongfeldt for animal care and preliminary data analysis. We are grateful for the Tomlinson Post-doctoral Fellowship (E.M.S.), for grants from the National Sciences and Engineering Research Council of Canada (PDF to E.M.S., CGS-M to T.Y.D. and Discovery Grant #261796-2011 to H.C.E.L.), for the Robert G. Goelet Research Award (E.M.S.) and to Canada Research Chairs (H.C.E.L.).

Author information

Authors and Affiliations

Authors

Contributions

E.M.S. conceived, designed and conducted the experiments and biomechanical analyses. T.Y.D. scanned, segmented and analysed the micro-computed tomography images. H.C.E.L. provided palaeontological and evolutionary expertise that shaped the project. E.M.S., T.Y.D. and H.C.E.L. wrote the manuscript.

Corresponding authors

Correspondence to Emily M. Standen or Hans C. E. Larsson.

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Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Timing of kinematic variables for the left fin during swimming in control and treatment group fish.

The polar plot represents a complete stroke cycle, starting at 0° with the fin fully adducted. At mid-stroke (180°), the fin is fully abducted, and then it adducts again (360°/0°). The data are plotted for the treatment group (dark grey, n = 12) and the control group (light grey, n = 6). Only data with significant directionality are plotted (Rayleigh’s test, P < 0.05). If the groups did not differ significantly in the timing of a given variable, they were binned and plotted together (black). The symbols represent the mean timing ( ± angular variance) of different kinematic variables.

Extended Data Figure 2 Variance in bone shape in control and treatment group fish.

Bone-shape variances between the control group (light grey, n = 7) and the treatment group (dark grey, n = 15). Dots indicate observed variance; error bars indicate bootstrapped 95% confidence intervals.

Extended Data Figure 3 Body length and mass in control and treatment group fish.

Bootstrapped differences in mean body length and mass between water-raised and land-raised fish at the start (a) and end (b) of the experiment. At the start of the experiment, land-raised fish were smaller than water-raised fish (Extended Data Table 6). Similar size relationships existed between the control (light grey) and treatment (dark grey) groups at the end of the experiment, but the differences were much greater (Extended Data Table 6). Length and weight data at the start (control, n = 38; treatment, n = 111) and the end (control, n = 30; treatment, n = 69) of the experiment were bootstrapped 10,000 times, and means were generated from each bootstrap. These values were used to test how the mean difference between the groups changed from the start to the end of the experiment. In all cases, the differences between the control and treatment groups increased over time.

Extended Data Table 1 Magnitudes of kinematic variables during walking and swimming
Extended Data Table 2 Magnitudes of kinematic variables during walking
Extended Data Table 3 Timing of kinematic variables during walking
Extended Data Table 4 Timing of kinematic variables during swimming
Extended Data Table 5 Analysis of variance (ANOVA) comparison of size regression models
Extended Data Table 6 Fish size

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Polypterus senegalus walking on a smooth surface

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Standen, E., Du, T. & Larsson, H. Developmental plasticity and the origin of tetrapods. Nature 513, 54–58 (2014). https://doi.org/10.1038/nature13708

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