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Developmental origins of mosaic evolution in the avian cranium - PubMed

  • ️Mon Jan 01 2018

Developmental origins of mosaic evolution in the avian cranium

Ryan N Felice et al. Proc Natl Acad Sci U S A. 2018.

Abstract

Mosaic evolution, which results from multiple influences shaping morphological traits and can lead to the presence of a mixture of ancestral and derived characteristics, has been frequently invoked in describing evolutionary patterns in birds. Mosaicism implies the hierarchical organization of organismal traits into semiautonomous subsets, or modules, which reflect differential genetic and developmental origins. Here, we analyze mosaic evolution in the avian skull using high-dimensional 3D surface morphometric data across a broad phylogenetic sample encompassing nearly all extant families. We find that the avian cranium is highly modular, consisting of seven independently evolving anatomical regions. The face and cranial vault evolve faster than other regions, showing several bursts of rapid evolution. Other modules evolve more slowly following an early burst. Both the evolutionary rate and disparity of skull modules are associated with their developmental origin, with regions derived from the anterior mandibular-stream cranial neural crest or from multiple embryonic cell populations evolving most quickly and into a greater variety of forms. Strong integration of traits is also associated with low evolutionary rate and low disparity. Individual clades are characterized by disparate evolutionary rates among cranial regions. For example, Psittaciformes (parrots) exhibit high evolutionary rates throughout the skull, but their close relatives, Falconiformes, exhibit rapid evolution in only the rostrum. Our dense sampling of cranial shape variation demonstrates that the bird skull has evolved in a mosaic fashion reflecting the developmental origins of cranial regions, with a semi-independent tempo and mode of evolution across phenotypic modules facilitating this hyperdiverse evolutionary radiation.

Keywords: evolutionary development; evolutionary rates; modularity; morphological diversity; morphometrics.

Copyright © 2018 the Author(s). Published by PNAS.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.

Cranial modularity in the avian skull. Cranial morphology was quantified using 757 3D landmarks, here illustrated on Pandion haliaetus (USNM 623422) in lateral (A) and ventral (B) perspective. Landmark colors reflect the reconstructed pattern of seven cranial modules. (C) Rate through time plots for each of the seven modules and the whole skull.

Fig. 2.
Fig. 2.

Module integration and evolution reflects developmental origin. Evolutionary rate vs. within-module correlation (A) and disparity vs. within-module correlation (B). Disparity is quantified for each module using Procrustes variance divided by the number of landmarks. Disparity and rate are highest in modules that are composed of anterior mandibular CNC or multiple embryonic cell types. Embryonic origin of cranial elements is shown in C, modified from ref. .

Fig. 3.
Fig. 3.

Evolutionary rates in the avian rostrum. Estimated using BayesTraitsV3 using a variable-rates model and lambda tree transformation. (Inset) Reconstruction of the ancestral neornithine skull (Materials and Methods).

Fig. 4.
Fig. 4.

Evolutionary rates across cranial modules. Palate (A), cranial vault (B), and occiput (C). Clade abbreviations: Acc, Accipitriformes; Ans, Anseriformes; Apod, Apodiformes; Buc, Bucerotiformes; Ca, Cariamiformes; Cap, Caprimulgiformes; Cha, Charadriiformes; Cic, Ciconiiformes; Col, Columbiformes; Cor, Coraciiformes; Cu, Cuculifomes; Fal, Falconiformes; Gall, Galliformes; Gru, Gruiformes; Mus, Musophagiformes; Oti, Otidiformes; Pas, Passeri; Pel, Pelecaniformes; Phae, Phaethontiformes; Pic, Piciformes; Pro, Procellariiformes; Ps, Psittaciformes; Ra, Ratites; Sph, Sphenisciformes; Strig, Strigiformes; Sul, Suliformes; Tin, Tinamiformes; Ty, Tyranni.

Comment in

  • Endless skulls most beautiful.

    Field DJ. Field DJ. Proc Natl Acad Sci U S A. 2018 Jan 16;115(3):448-450. doi: 10.1073/pnas.1721208115. Epub 2017 Dec 29. Proc Natl Acad Sci U S A. 2018. PMID: 29288219 Free PMC article. No abstract available.

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