Cargando…

Developmental origins of mosaic evolution in the avian cranium

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 organ...

Descripción completa

Detalles Bibliográficos
Autores principales: Felice, Ryan N., Goswami, Anjali
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5776993/
https://www.ncbi.nlm.nih.gov/pubmed/29279399
http://dx.doi.org/10.1073/pnas.1716437115
_version_ 1783294160740024320
author Felice, Ryan N.
Goswami, Anjali
author_facet Felice, Ryan N.
Goswami, Anjali
author_sort Felice, Ryan N.
collection PubMed
description 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.
format Online
Article
Text
id pubmed-5776993
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher National Academy of Sciences
record_format MEDLINE/PubMed
spelling pubmed-57769932018-01-23 Developmental origins of mosaic evolution in the avian cranium Felice, Ryan N. Goswami, Anjali Proc Natl Acad Sci U S A Biological Sciences 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. National Academy of Sciences 2018-01-16 2017-12-26 /pmc/articles/PMC5776993/ /pubmed/29279399 http://dx.doi.org/10.1073/pnas.1716437115 Text en Copyright © 2018 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Felice, Ryan N.
Goswami, Anjali
Developmental origins of mosaic evolution in the avian cranium
title Developmental origins of mosaic evolution in the avian cranium
title_full Developmental origins of mosaic evolution in the avian cranium
title_fullStr Developmental origins of mosaic evolution in the avian cranium
title_full_unstemmed Developmental origins of mosaic evolution in the avian cranium
title_short Developmental origins of mosaic evolution in the avian cranium
title_sort developmental origins of mosaic evolution in the avian cranium
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5776993/
https://www.ncbi.nlm.nih.gov/pubmed/29279399
http://dx.doi.org/10.1073/pnas.1716437115
work_keys_str_mv AT feliceryann developmentaloriginsofmosaicevolutionintheaviancranium
AT goswamianjali developmentaloriginsofmosaicevolutionintheaviancranium