Developmental bias in the evolution of phalanges

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 110; no. 45; pp. 18190 - 18195
• Main Authors: Kavanagh, Kathryn D., Shoval, Oren, Winslow, Benjamin B., Alon, Uri, Leary, Brian P., Kan, Akinori, Tabin, Clifford J.
• Format: Journal Article
• Language: English
• Published: United States NATIONAL ACADEMY OF SCIENCES 05.11.2013; National Acad Sciences; National Academy of Sciences
• Subjects: Animals; Biological Evolution; Biological Sciences; Birds; Birds of prey; Bones; Bones of Upper Extremity - diagnostic imaging; Bones of Upper Extremity - growth & development; Condensation; Embryos; Evolution; Finches; Foot bones; Joints; Models, Biological; Morphology; Motor ability; Nonnative species; Organ Size; Osteogenesis - physiology; Phalanges; Radiography; Ratios; Selection, Genetic; Species Specificity; Toe Phalanges - diagnostic imaging; Toe Phalanges - growth & development; Vertebrates - growth & development; developmental constraint; developmental module; phalanx
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1315213110

Evolutionary theory has long argued that the entrenched rules of development constrain the range of variations in a given form, but few empirical examples are known. Here we provide evidence for a very deeply conserved skeletal module constraining the morphology of the phalanges within a digit. We measured the sizes of phalanges within populations of two bird species and found that successive phalanges within a digit exhibit predictable relative proportions, whether those phalanges are nearly equal in size or exhibit a more striking gradient in size from large to small. Experimental perturbations during early stages of digit formation demonstrate that the sizes of the phalanges within a digit are regulated as a system rather than individually. However, the sizes of the phalanges are independent of the metatarsals. Temporal studies indicate that the relative sizes of the phalanges are established at the time of initial cell condensation. Measurements of phalanges across species from six major taxonomic lineages showed that the same predictable range of variants is conserved across vast taxonomic diversity and evolutionary time, starting with the very origins of tetrapods. Although in general phalangeal variations fall within a range of nearly equal-sized phalanges to those following a steep large-to-small gradient, a novel derived condition of excessive elongation of the distal-most phalanges has evolved convergently in multiple lineages, for example under selection for grasping rather than walking or swimming. Even in the context of this exception, phalangeal variations observed in nature are a small subset of potential morphospace.