Fossil evidence of the avian vocal organ from the Mesozoic

• Julia A. Clarke
• , Sankar Chatterjee
• , Zhiheng Li
• , Tobias Riede
• , Federico Agnolin
• , Franz Goller
• , Marcelo P. Isasi
• , Daniel R. Martinioni
• , Francisco J. Mussel
•  & Fernando E. Novas

Nature volume 538, pages 502–505 (27 October 2016) | Download Citation

Abstract

From complex songs to simple honks, birds produce sounds using a unique vocal organ called the syrinx^1,2. Located close to the heart at the tracheobronchial junction, vocal folds or membranes attached to modified mineralized rings vibrate to produce sound^{1,2,3,4,5,6,7}. Syringeal components were not thought to commonly enter the fossil record⁶, and the few reported fossilized parts of the syrinx are geologically young^8,9,10,11 (from the Pleistocene and Holocene (approximately 2.5 million years ago to the present)).

The only known older syrinx is an Eocene specimen that was not described or illustrated¹². Data on the relationship between soft tissue structures and syringeal three-dimensional geometry are also exceptionally limited⁵. Here we describe the first remains, to our knowledge, of a fossil syrinx from the Mesozoic Era, which are preserved in three dimensions in a specimen from the Late Cretaceous (approximately 66 to 69 million years ago) of Antarctica. 


With both cranial and postcranial remains, the new Vegavis iaai specimen is the most complete to be recovered from a part of the radiation of living birds (Aves). Enhanced-contrast X-ray computed tomography (CT) of syrinx structure in twelve extant non-passerine birds, as well as CT imaging of the Vegavis and Eocene syrinxes, informs both the reconstruction of ancestral states in birds and properties of the vocal organ in the extinct species. Fused rings in Vegavis form a well-mineralized pessulus, a derived neognath bird feature, proposed to anchor enlarged vocal folds or labia⁵. Left-right bronchial asymmetry, as seen in Vegavis, is only known in extant birds with two sets of vocal fold sound sources.

The new data show the fossilization potential of the avian vocal organ and beg the question why these remains have not been found in other dinosaurs. The lack of other Mesozoic tracheobronchial remains, and the poorly mineralized condition in archosaurian taxa without a syrinx, may indicate that a complex syrinx was a late arising feature in the evolution of birds, well after the origin of flight and respiratory innovations.

This male spotted bluethroat bursts into song by activating an organ deep in its throat.

Hans Glader/Minden Pictures

A caixa de voz de pássaros é única no reino animal

By Elizabeth PennisiOct. 5, 2018 , 4:30 PM

The melodious call of many birds comes from a mysterious organ buried deep within their chests: a one-of-a-kind voice box called a syrinx. Now, scientists have concluded that this voice box evolved only once, and that it represents a rare example of a true evolutionary novelty.

“It’s something that comes out of nothing,” says Denis Dubuole, a geneticist at the University of Geneva in Switzerland who was not involved with the work. “There is nothing that looks like a syrinx in any related animal groups in vertebrates. This is very bizarre.”

Reptiles, amphibians, and mammals all have a larynx, a voice box at the top of the throat that protects the airways. Folds of tissue there—the vocal cords—can also vibrate to enable humans to talk, pigs to grunt, and lions to roar. Birds have larynxes, too. But the organ they use to sing their tunes is lower down—where the windpipe splits to go into the two lungs. The syrinx, named in 1872 after a Greek nymph who was transformed into panpipes, has a similar structure: Both are tubes supported by cartilage with folds of tissue.

The oldest known syrinx belongs to a bird fossil some 67 million years old; that’s about the same time all modern bird groups became established. To figure out where the bizarre organ came from, Julia Clarke, a paleontologist at the University of Texas in Austin, who made the syrinx discovery in 2013, assembled a team of developmental biologists, evolutionary biologists, and other researchers. 

The group combed the literature and compared the anatomy, genetics, and development of bird syrinxes and larynxes from a range of modern reptiles. The organs are quite different—even more so than early biologists believed—they discovered. To work the vocal cords, larynxes depend on muscles that attach to that organ’s cartilage. But the syrinx relies, at least in part, on muscles that in other animals extend from the back of the tongue to the bones that connect the arms to the body.

A 3D image of where the windpipe splits to go into the lungs shows how elaborate the junction became in birds (right) compared with alligators (left), resulting in a new avian voice box.

Julia Clarke et al.

The two organs also appear to develop differently. The larynx is made from a mix of mesoderm and neural crest cells, which make up muscles and some facial bone and nerve cells, respectively. But the syrinx is made of just mesoderm cells—there are no neural crest cells involved. “It presents a rather interesting rare case of how new structures and developmental programs evolve,” Clarke says. These differences, however, still resulted in organs with the same function.

Clarke and her colleagues suspect the ancestors of modern birds also had a larynx. Then, at some point before birds became birds, the cartilage in the windpipe just above the lungs expanded to form the syrinx. This expansion may have initially provided additional support for the split in the windpipe; eventually, it developed rings of muscle that enabled the complex avian sound repertoire heard today. Over millions of years, the syrinx took over sound production from the larynx, possibly because the syrinx was more versatile at producing a wide variety of sounds

Thrush song

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This means that the syrinx is an evolutionary novelty, Clarke and her colleagues reported last week in the Proceedings of the National Academy of Sciences. True novelties in evolution are hard to come by. They are innovations—new traits or new structures—that arise without any clear connections to existing traits or structures. Most previously suspected novelties, such as fingers and toes in land animals, have turned out to be the result of evolution tinkering with something that already exists, like fish fins in the case of fingers and toes.

Such new innovations can “trigger further evolutionary steps,” says Johannes Müller, a paleozoologist at the Museum of Natural History in Berlin. By enabling songs to get more complex, he adds, the syrinx could have prompted birds with new variations of their songs to split into new species.

And the study may have implications beyond avian crooners. Behavioral ecologist Richard Vogt from the National Institute of Amazonian Research in Manaus, Brazil, says it gives him a starting point to search for the structures that make sounds in turtles. Since 2008, Vogt and conservation biologist Camila Rudge Ferrara of the Wildlife Conservation Society in Manaus have shown that turtles, particularly social species, make a variety of sounds, even in their egg cases. It’s currently unclear whether they are using their larynx or generating these noises in just their mouths.

Turtle sounds

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Neither turtles nor the later-evolving crocodiles has a syrinx, says Nicolas Mathevon, an ethologist at the University of Lyon/St. Etienne in France, who studies the sounds crocodiles and their relatives—the only modern representatives of dinosaurs apart from birds—make. Crocodiles diverged from birds 240 million years ago, and many are famous for their calls.

Caiman call

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But crocs have a very basic larynx, with structures that vibrate in airflow. If the syrinx evolved as birds came into existence, then “some dinosaurs may have had two sound sources,” Mathevon says. “Maybe one day we will find a fossil of a dinosaur with a larynx together with a syrinx.”

Posted in:

• Plants & Animals

doi:10.1126/science.aav6415

Robert Lachlan

This swamp sparrow’s song is more than 1500 years old

By Victoria DavisJun. 20, 2018 , 2:35 PM

Some people can trace their traditions back decades; the swamp sparrow has passed its songs down for more than 1500 years. The findings, published today in Nature Communications, suggest humans are not alone in keeping practices alive for long periods of time.

To conduct the study, researchers recorded a collection of songs from 615 adult male swamp sparrows from six densely populated areas across the northeastern United States. They dissected each bird’s song repertoire, identifying only 160 different syllable types within all the recorded sample. Most swamp swallows sang the same tunes, using the same common syllables, but there were a few rare types in each population, just as there are variations in human oral histories over time.

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Sample of a male swamp sparrow song 

http://www.sciencemag.org/news/2018/06/swamp-sparrow-s-song-more-1500-years-old?utm_campaign=news_daily_2018-06-20&et_rid=17136612&et_cid=2127511 

Using a statistical method of calculation called approximate Bayesian computation and models that measure the diversity of syllable types present in each population, the scientists were able to calculate how the songs of each male would have changed over time. They also found that all but two of the most common syllables used during their sampling in 2009 were also the most common during an earlier study of the species when recordings were made in the 1970s. Overall, the analysis indicated that the average age of the oldest tune dated back about 1537 years.
Other bird and animal species may also be capable of similar feats, the researchers say. Even animals with relatively small brains can have long-lasting traditions.

Posted in:

• Plants & Animals

doi:10.1126/science.aau5398

Ornitologia: Cantadas constantes

Mecanismos neuronais explicam a estabilidade vocal de passarinhos 

MARIA GUIMARÃES e RODRIGO DE OLIVEIRA ANDRADE | ED. 249 | NOVEMBRO 2016

Revista Pesquisa FAPESP

Podcast: Tarciso Velho

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Quem já ouviu o insistente canto do sabiá-laranjeira durante os dias, ou em horas inusitadas das madrugadas de primavera nas cidades brasileiras, há de ter percebido as notas repetidas incansavelmente. Uma possível explicação para os aspectos repetitivos desse canto acaba de surgir do estudo do cérebro de outro passarinho: o mandarim (Taeniopygia guttata), uma espécie muito usada em experimentos comportamentais em laboratório. Um dos tipos de células da complexa e adaptável rede neuronal responsável pelas manifestações vocais em pássaros canoros se mantém estável nos mandarins, de acordo com artigo publicado em outubro na Nature Neuroscience.

“O canto dos adultos tem repetições praticamente idênticas umas às outras”, explica o neurocientista Tarciso Velho, professor no Instituto do Cérebro da Universidade Federal do Rio Grande do Norte (UFRN) e um dos autores do estudo. “Isso faz desses animais um modelo ideal para o estudo da relação entre a atividade neuronal e o comportamento.” O grupo, coordenado pelo físico norte-americano Timothy Gardner, da Universidade de Boston, nos Estados Unidos, analisou a ação de dois grupos de neurônios em uma área específica do cérebro responsável pelo controle do canto, conhecida como HVC. Os neurônios inibitórios têm uma ação intensa local, dentro do HVC. A hipótese vigente é de que quando a atividade deles diminui, outro tipo de célula neuronal, os neurônios excitatórios, entra em ação e ativa uma cadeia de neurônios que controla a musculatura ligada à produção do canto.

O mistério quanto à estabilidade vocal vem da plasticidade que caracteriza o núcleo cerebral que controla o canto. No cérebro do pássaro, e em algumas áreas do de mamíferos, há um processo constante em que algumas células morrem enquanto novas são geradas. Além disso, mesmo em uma população estável de células, as conexões entre elas podem passar por rearranjos. Essas alterações na conectividade neuronal são interpretadas como as bases neurais do aprendizado, um processo no qual o sono parece exercer um papel importante. “Quando registramos imagens durante o canto, observamos que a atividade dos neurônios excitatórios variava de um dia para o outro, com células entrando e saindo do conjunto que participava da produção do canto, de maneira que os participantes da atividade neural não eram sempre os mesmos”, explica Velho. Mas apesar desse cenário dinâmico, o canto permanece estável. O segredo parece estar nas células inibitórias: nos experimentos feitos em Boston, sua atividade variou pouco (ver infográfico). Isso parece ser responsável pela constância de um atributo central ao reconhecimento dentro da espécie, sem o qual as fêmeas teriam mais dificuldade de encontrar seus pares reprodutivos.

A cabeça por dentro
 
Esses resultados foram possíveis graças a minúsculos equipamentos desenvolvidos por Gardner. “Se o pássaro fica preso, ele não canta”, explica Velho. “Precisamos deixá-lo solto na gaiola, com aparelhos que não atrapalhem a sua movimentação.” Atendendo a essa necessidade, os pesquisadores implantaram eletrodos no cérebro dos passarinhos para monitorar as células inibitórias por vários meses. Ainda mais impressionantes são microscópios miniaturizados pesando menos de 2 gramas. Produzidos com o auxílio de uma impressora 3D, esses microscópios foram implantados no cérebro dos pássaros e permitiram detectar a fluorescência emitida pela atividade das células excitatórias graças a uma proteína inserida por meio de vírus para funcionar como sensor de cálcio – elemento central à atividade elétrica dos neurônios. “Ambos os métodos permitiram fazer registros do cérebro em aves que estavam acordadas, se comportando e movimentando livremente”, afirma Gardner.

https://media.giphy.com/media/3oriNRnN3PA0zcFBug/giphy.gif 

Para o físico norte-americano, o comportamento distinto que essas técnicas detectaram nos dois tipos de células é o que está por trás da estabilidade do canto. Mesmo que a atividade de cada neurônio excitatório varie, eventuais falhas são compensadas pela ação de células vizinhas, que tendem a disparar simultaneamente. “Essa redundância sugere que, se uma célula deixa de funcionar, outra poderá desempenhar um papel semelhante e manter a estabilidade da rede e, consequentemente, o resultado motor”, analisa. O estudo mostrou também que a ação local das células inibitórias é o que modula o funcionamento dessa rede. “Neurônios individuais poderiam otimizar sua atividade dentro de uma estrutura maior que permanece imutável por anos.”

Com seus comportamentos previsíveis e inalterados na vida em gaiola imposta pela condição de cobaia de laboratório, os mandarins são os queridinhos de pesquisadores concentrados em compreender o desenvolvimento vocal – um comportamento aprendido, repetitivo e estereotipado. Gardner defende que eles podem contribuir ainda para a elucidação de aspectos da fala humana. “Redes neurais no cérebro de mamíferos precisam resolver problemas semelhantes”, diz. “Seria interessante investigar se esses programas motores são controlados e mantidos de maneira parecida.” Dizem que uma vez que se aprende a andar de bicicleta, nunca mais se esquece. Resta saber se mecanismos envolvendo neurônios inibitórios e excitatórios podem estar por trás desse tipo de capacidade motora de longa duração.

Artigo científico
 
LIBERTI III, W. A. et al. Unstable neurons underlie a stable learned behavior. Nature Neuroscience. On-line. 10 out. 2016.