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Contributed by Clifford J. Tabin, October 3, 2013 (sent for review April 2, 2013)
Significance
It has long been proposed that rules stemming from the mechanisms used during development can constrain the range of evolvable variations in a given form, but few empirical examples are known. We have focused on developmental processes determining proportions of phalanx size along individual digits (fingers/toes) of vertebrates. We find that phalangeal variation seen in nature is indeed constrained by an ancestral developmental program, limiting morphologies to a continuum from nearly equal-sized phalanges to a large-to-small gradient of relative sizes. Nonetheless, later innovations in distal regulation expanded variational possibilities for groups that needed greater grasping ability. These data provide a better understanding of how properties of developmental systems work in combination with natural selection to guide evolution of skeletal proportions.
Abstract
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.
Footnotes
↵1Present address: Orthopedic Surgery, Gifu Central Hospital, Gifu, Gifu 501-1198, Japan.
- ↵2To whom correspondence should be addressed. E-mail: tabin{at}genetics.med.harvard.edu.
Author contributions: K.D.K., O.S., and C.J.T. designed research; K.D.K., O.S., B.B.W., U.A., and B.P.L. performed research; A.K. contributed new reagents/analytic tools; K.D.K., O.S., U.A., and C.J.T. analyzed data; and K.D.K., O.S., and C.J.T. wrote the paper.
The authors declare no conflict of interest.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1315213110/-/DCSupplemental.
- Kathryn D. Kavanagha,
- Oren Shovalb,
- Benjamin B. Winslowa,
- Uri Alonb,
- Brian P. Learya,
- Akinori Kanc,1, and
- Clifford J. Tabinc,2
- aDepartment of Biology, University of Massachusetts Dartmouth, North Dartmouth, MA 02747;
- bDepartment of Molecular Cell Biology, Weizmann Institute, Rehovat 76100, Israel; and
- cDepartment of Genetics, Harvard Medical School, Boston, MA 02115
Contributed by Clifford J. Tabin, October 3, 2013 (sent for review April 2, 2013)
Significance
It has long been proposed that rules stemming from the mechanisms used during development can constrain the range of evolvable variations in a given form, but few empirical examples are known. We have focused on developmental processes determining proportions of phalanx size along individual digits (fingers/toes) of vertebrates. We find that phalangeal variation seen in nature is indeed constrained by an ancestral developmental program, limiting morphologies to a continuum from nearly equal-sized phalanges to a large-to-small gradient of relative sizes. Nonetheless, later innovations in distal regulation expanded variational possibilities for groups that needed greater grasping ability. These data provide a better understanding of how properties of developmental systems work in combination with natural selection to guide evolution of skeletal proportions.
Abstract
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.
- developmental module
- developmental constraint
- phalanx
Footnotes
↵1Present address: Orthopedic Surgery, Gifu Central Hospital, Gifu, Gifu 501-1198, Japan.
- ↵2To whom correspondence should be addressed. E-mail: tabin{at}genetics.med.harvard.edu.
Author contributions: K.D.K., O.S., and C.J.T. designed research; K.D.K., O.S., B.B.W., U.A., and B.P.L. performed research; A.K. contributed new reagents/analytic tools; K.D.K., O.S., U.A., and C.J.T. analyzed data; and K.D.K., O.S., and C.J.T. wrote the paper.
The authors declare no conflict of interest.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1315213110/-/DCSupplemental.
Developmental bias in the evolution of phalanges
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