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Developmental origins of mosaic evolution in the avian cranium

Year: 2018
Authors: Ryan N. Felice and Anjali Goswami
Journal: Proceedings of the National Academy of Sciences, U.S.A.
Files: Aythya valisineria, Bombycilla garrulus, Gallinula chloropus, Grus antigone, Gyps fulvus, Haematopus ostralegus, Todiramphus pyrrhopygius, Haliaeetus leucocephalus, Himantopus himantopus, Hirundo rustica, Hymenops perspicillatus, Ibycter americanus, Irena puella, Larus marinus, Leiothrix lutea, Leptotila verreauxi, Limosa lapponica, Lophorina superba, Megalaima haemacephala, Melanocharis versteri, Meleagris gallopavo, Meliphaga lewinii, Melopsittacus undulatus, Menura novaehollandiae, Merops viridis, Merops nubicus, Mesembrinibis cayennensis, Micrastur semitorquatus, Micropygia schomburgkii, Momotus momota, Motacilla alba, Buceros rhinoceros, Bucco capensis, Bubo bubo, Baryphthengus ruficapillus, Baryphthengus martii, Branta canadensis, Accipiter nisus, Aegotheles cristatus, Amazilia tzacatl, Amazona guildingii, Anas platyrhynchos, Aramus guarauna, Anser anser, Anseranas semipalmata, Casmerodius albus, Athene noctua, Balaeniceps rex, Balearica regulorum, Monias benschi, Atelornis pittoides, Buphagus erythrorhynchus, Burhinus bistriatus, Cacatua alba, Caprimulgis aegyptius, Caprimulgis europaeus, Caprimulgis macrurus, Casuarius unappendiculatus, Cathartes aura, Catharus fruscescens, Cepphus grylle, Megaceryle alcyon, Chaetura pelagica, Charadrius vociferus, Chelidoptera tenebrosa, Chloroceryle aenea, Chauna torquata, Ciconia ciconia, Strix nigrolineata, Clamator glandarius, Colinus virginianus, Colius striatus, Columbina passerina, Coracias benghalensis, Corvus brachyrhynchos, Coturnix coturnix, Crypturellus cinereus, Cuculus canorus, Cursorius cursor, Dicaeum ignipectus, Dicrurus macrocercus, Dicrurus megarhynchus, Dromaius novaehollandiae, Phoebastria nigripes, Drymodes brunneopygia, Egretta garzetta, Eubucco bourcierii, Eudocimus ruber, Eudromia elegans, Eurostopodus macrotis, Eurystomus gularis, Falco peregrinus, Formicarius analis, Formicarius rufipectus, Fregata magnificens, Galbula dea, Gampsonyx swainsonii, Gavia stellata, Geococcyx californianus, Geospiza fortis, Geospiza fuliginosa, Grus americana, Gymnorhina tibicen, Indicator indicator, Haliaeetus albicilla, Indicator maculatus, Himantopus mexicanus, Ixobrychus minutus, Jacana spinosa, Jynx torquilla, Lanius ludovicianus, Leptoptilos dubius, Leucopsar rothschildi, Lorius lory, Loxia leucoptera, Musophaga violacea, Myiagra hebetior, Neophron percnopterus, Nestor notabilis, Nicator chloris, Nothoprocta ornata, Numenius arquata, Numida meleagris, Nyctibius grandis, Nyctibius griseus, Nycticorax nycticorax, Rostratula semicollaris, Oceanodroma tethys, Odontophorus capueira, Odontophorus gujanensis, Opisthocomus hoazin, Oriolus oriolus, Ortalis motmot, Otis tarda, Oxylabes madagascariensis, Oxyura jamaicensis, Pachycephala philippinensis, Pachyramphus minor, Pandion haliaetus, Paradisaea raggiana, Paradisaea rudolphi, Passer domesticus, Pelagodroma marina, Pelecanus occidentalis, Perdix perdix, Penelope purpurascens, Phalacrocorax carbo, Phaethon aethereus, Phalcoboenus australis, Picoides pubescens, Pitta sordida, Podargus strigoides, Porzana atra, Podiceps cristatus, Probosciger aterrimus, Pterocles gutturalis, Pterodroma macroptera, Ptilonorhynchus violaceus, Ramphastos sulfuratus, Rhinoptilus africanus, Bucanetes githagineus, Rostratula semicollaris, Sakesphorus luctuosus, Semnornis ramphastinus, Steatornis caripensis, Stercorarius parasiticus, Streptoprocne semicollaris, Struthidea cinerea, Theristicus caerulescens, Thinocorus orbignyianus, Threskiornis aethiopicus, Tigrisoma lineatum, Tockus erythrorhynchus, Toxostoma redivivum, Turnix suscitator, Tyrannus savana, Vanga curvirostris, Paradisaea minor, Pardalotus striatus, Pelecanoides urinatrix, Pernis apivorus, Phaethon lepturus, Phaethornis superciliosus, Phainopepla nitens, Philepitta castanea, Phoenicopterus ruber, Phylloscopus ruficapilla, Platalea ajaja, Platalea leucorodia, Plectrophenax nivalis, Pluvialis squatarola, Parus atricapillus, Porphyrio porphyrio, Prunella modularis, Psarocolius wagleri, Psittacus erithacus, Psophia crepitans, Lugensa brevirostris, Ptilinopus roseicapilla, Puffinus puffinus, Pygoscelis adeliae, Quiscalus mexicanus, Recurvirostra avosetta, Regulus satrapa, Rhea americana, Rhipidura albicollis, Rhynchocyclus brevirostris, Rhynchotus rufescens, Rollulus rouloul, Rupicola peruvianus, Sarcoramphus papa, Scopus umbretta, Sericulus chrysocephalus, Sitta europaea, Yuhina brunneiceps, Xenicus longipes, Bernieria zosterops, Vultur gryphus, Vidua macroura, Vanellus vanellus, Uria aalge, Upupa epops, Tyto alba, Turdus philomelos, Turdus merula, Tringa totanus, Illadopsis cleaveri, Treron curvirostra, Thryothorus ludovicianus, Thalassarche chlororhynchos, Tetrao urogallus, Ruwenzorornis johnstoni, Tapera naevia, Tangara schrankii, Taeniopygia guttata, Sylvietta leucophrys, Sula dactylatra, Morus bassanus, Sturnus unicolor, Struthio camelus, Strix aluco, Sterna hirundo, Smithornis capensis, Spheniscus humboldti, Spizella passerina, Stachyris whiteheadi, Hypothetical Ancestral Neornithine, Balearica pavonina, Ardeotis australis, Asio otus, Ardea purpurea, Archilochus colubris, Apus apus, Aquila chrysaetos, Aptenodytes forsteri, Caprimulgus carolinensis, Anthropoides virgo, Anodorhynchus leari, Anhinga anhinga, Alectura lathami, Rhopocichla atriceps, Alcedo atthis, Bombycilla cedrorum, Bonasa umbellus, Brachypteracias leptosomus, Bubulcus ibis, Bucorvus abyssinicus, Burhinus oedicnemus, Buteo buteo, Calcarius lapponicus, Calandrella rufescens, Calonectris diomedea, Calyptomena viridis, Campylorhamphus trochilirostris, Capito niger, Casuarius bennetti, Cariama cristata, Centropus phasianinus, Cephalopterus ornatus, Ceratopipra rubrocapilla, Acrocephalus arundinaceus, Bombycilla garrulus, Chauna chavaria, Chionis albus, Chlamydotis undulata, Chloropsis aurifrons, Chordeiles minor, Larus philadelphia, Chunga burmeisteri, Ciconia maguari, Cichladusa guttata, Cinclus mexicanus, Cisticola cantans, Climacteris rufus, Cnemophilus loriae, Colluricincla harmonica, Columba livia, Conopophaga ardesiaca, Coracina novaehollandiae, Corvus corone, Coua gigas, Crax rubra, Cuculus pallidus, Culicicapa ceylonensis, Cygnus cygnus, Dendrocygna arcuata, Dendroica petechia, Deroptyus accipitrinus, Diomedea exulans, Donacobius atricapilla, Dromas ardeola, Dryocopus pileatus, Emberiza cirlus, Eurylaimus ochromalus, Eurypyga helias, Eutoxeres condamini, Fratercula arctica, Fregata minor, Fulmarus glacialis, Furnarius rufus, Gallus gallus, Garrulax galbanus, Garrulus glandarius, Holiday Ancestral Neornithine

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 skullusing high-dimensional 3D surface morphometric data across a broad phylogenetic sample encompassing nearly all extant families. We find that the avian cranium is highlymodular, 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.


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