What's In John's Freezer?

[This is the original, unedited text of my shorter, tighter (and I think actually better) News & Views piece for Nature, on the paper described below)

Ambitious experimental and morphological studies of a modern fish show how a flexible phenotype may have helped early “fishapods” to make the long transition from finned aquatic animals into tetrapods able to walk on land.

Stomach-Churning Rating: 1/10. Cute fish. Good science. Happy stomachs!

Photo by Antoine Morin, showing Polypterus on land.

Napoleon Bonaparte’s military excursions into Egypt in 1798-1799 led a young French naturalist, Ètienne Geoffroy Saint-Hilaire, to cross paths with a strange fish that had paired lungs and could “walk” across land on its stubby, lobelike fins. In 1802, he dubbed this fish “Polyptère bichir”¹, today known as the Nile bichir, Polypterus bichir La Cepède 1803. The bichir’s mélange of primitive and advanced traits helped to catapult Geoffroy into scholarly conflict with the reigning naturalist Georges Cuvier back in France and to establish Ètienne as a leading anatomist, embryologist and early evolutionary researcher of repute even today². Now, on their own excursion under the very “evo-devo” flag that the discoverer of Polypterus helped raise, Canadian scientists Standen et al.³ suggest how the remarkable plasticity of the skeleton of Polypterus (the smaller west African relative of P. bichir, P. senegalus or “Cuvier’s bichir”) reveals a key part of the mechanism that might have facilitated the gradual transition from water to land and thus from “fishapods” to tetrapods (four-limbed vertebrates).

In a bold experiment, the authors raised 149 young bichirs on land and in water for eight months, then studied how they moved on land vs. in water, and also how the ultimate shape of the skeletal elements of the paired front fin bases differed between the land- and water-raised bichirs. Standen et al.³ discovered that both the form and function of the fins’ foundations transformed to better satisfy the constraints of moving on land. Land-acclimated bichirs took faster steps on land, their fins slipped across the substrate less, they held their fins closer to their body, their noses stayed more aloft and their tails undulated less, with less variable motions overall—behaviours that the authors had predicted should appear to enhance walking abilities on land. In turn, the bones of the neck and shoulder region altered their shape to produce a more mobile fin base with greater independence of fin from neck motion, along with improved bracing of the ventral “collarbone” region. These environmentally-induced traits should have fostered the locomotor changes observed in “terrestrialized” fish and aided the animals in resisting gravity, and they represent a common biological phenomenon termed developmental plasticity^4,5. Interestingly, the land-reared fish could still swim about as well as the wholly aquatic cohort, so there was not a clear trade-off between being a good swimmer and a good walker, which is surprising.

Considered alone, the developmental plasticity of bichir form and function shows how impressive these amphibious fish are. But Standen et al.’s study³  ventured further, to apply the lessons learned from bichir ontogeny to a phylogenetic context and macroevolutionary question. The phenotypic plasticity during bichir development, they infer, could have been harnessed during the evolutionary transformation of fins for swimming into limbs for walking, in the “fishapod” ancestors of tetrapods. Indeed, bichirs are close to the base of the family tree of fishes⁶, and other living relatives of tetrapods have reduced or lost their fins (lungfishes) or adapted to strange deep-sea swimming lifestyles, never walking on land (coelacanths). Thus perhaps bichirs and the “fishapod” lineage share what Geoffroy would have called “unity of type”, today termed homology, of their developmental plasticity in response to a land environment. Surveying the fossil record of early “fishapods” and tetrapods, Standen et al.³ found that the macroevolutionary changes of neck and shoulder anatomy in these gradually more land-adapted animals parallel those they observed in terrestrialized Polypterus, providing ancillary support for their hypothesis.

A further test of the application of Polypterus’s plasticity to fossil tetrapods is naturally difficult. However, the “fishapod” lineage has some exceptional examples of fossil preservation. With sufficient sample sizes (e.g. fossil beds that reveal growth series, such as the Late Devonian Miguasha site in Canada⁷) and palaeoenvironmental gradients in fish or tetrapods, one could imagine performing a rigorous indirect test. Even small samples could be helpful– for example, the early tetrapod Ichthyostega exhibits some developmental changes in its forelimb suggesting that it became more terrestrial as it grew, whereas the related Acanthostega does not evidence such changes⁸— this hints at some developmental plasticity in the former animal.

During the Devonian period (~360-420 million years ago), were the “fishapod” ancestors of tetrapods floundering about on land now and then, gradually shifting from anatomy and behaviours that were more developmentally plastic (as in bichirs) to ones that were more canalized into the terrestrialized forms and functions that more land-adapted tetrapods retained? An attractive possibility is that the developmental plasticity could have led to fixation (reduction of plasticity), an evolutionary phenomenon called genetic assimilation, which another intellectual descendant of Geoffroy, Conrad Hal Waddington, promoted from the 1950s onwards⁹, a concept that now enjoys numerous cases of empirical support¹⁰ that this one may eventually join.

The nature of the genetic and developmental mechanism that bichirs use to achieve the observed developmental plasticity is still unclear. If it has a high enough degree of heritability, then it could be selected for in cross-generational experiments with bichirs. With sufficient time and luck raising these unusual fish, the hypothesis that their plastic response to a terrestrial environment can become genetically assimilated could be directly tested. This study could thus become an epic exemplar of how genetic assimilation can contribute not only to microevolutionary change but also to major macroevolutionary events, as was presciently suggested in a seminal review of developmental plasticity⁴.

This genetic assimilation is the Polypterus study’s reasonable speculation, and one that Geoffroy likely would have applauded, all the more for involving his beloved bichirs. Much as Napoleon’s landfall in Egypt was not a lasting success, bichirs never left wholly terrestrial descendants despite their malleable locomotor system. But the same type of plastic developmental mechanism that bichirs use today to make tentative, floppy incursions of the terrestrial realm might have been harnessed by our own “fishapod” forebears, leaving a far more revolutionary dynasty upon the Earth.

References

1.  Geoffroy, E. (1802). Histoire naturelle et description anatomique d’un nouveau genre de poisson du Nil, nommé polyptère. Annales du Muséum d’Histoire Naturelle 1:57-68.
2. Le Guyader, H., & Grene, M. (2004) Geoffroy Saint-Hilaire: A Visionary Naturalist. Univ. Chicago Press.
3. Standen, E. M., Du, T. Y., & Larsson, H. C. E. (2014). Developmental plasticity and the origin of tetrapods. Nature, published online.
4. West-Eberhard, M. J. (1989). Phenotypic plasticity and the origins of diversity. Annual Review of Ecology and Systematics 20:249-278.
5. Pigliucci, M., Murren, C. J., & Schlichting, C. D. (2006). Phenotypic plasticity and evolution by genetic assimilation. Journal of Experimental Biology 209(12):2362-2367.
6. Near, T. J., Dornburg, A., Tokita, M., Suzuki, D., Brandley, M. C., & Friedman, M. (2014). Boom and bust: ancient and recent diversification in bichirs (Polypteridae: Actinopterygii), a relictual lineage of ray‐finned fishes. Evolution 68:1014-1026.
7. Cloutier, R. (2013). Great Canadian Lagerstätten 4. The Devonian Miguasha Biota (Québec): UNESCO World Heritage Site and a Time Capsule in the Early History of Vertebrates.Geoscience Canada40:149-163.
8. Callier, V., Clack, J. A., & Ahlberg, P. E. (2009). Contrasting developmental trajectories in the earliest known tetrapod forelimbs.Science324:364-367.
9. Waddington, C. H. (1953). Genetic assimilation of an acquired character. Evolution 7:118-126.
10. Crispo, E. (2007). The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. Evolution 61:2469-2479.