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Reversal to air-driven sound production revealed by a molecular phylogeny of tongueless frogs, family Pipidae.

Irisarri I, Vences M, San Mauro D, Glaw F, Zardoya R - BMC Evol. Biol. (2011)

Bottom Line: To place this paradoxical pattern into an evolutionary framework, we reconstructed robust molecular phylogenies of pipids based on complete mitochondrial genomes and nine nuclear protein-coding genes that coincided in placing Pseudhymenochirus nested among other pipids.We conclude that although Pseudhymenochirus probably has evolved a reversal to the ancestral non-pipid condition of air-driven sound production, the mechanism through which it occurs is an evolutionary innovation based on the derived larynx of pipids.This strengthens the idea that evolutionary solutions to functional problems often emerge based on previous structures, and for this reason, innovations largely depend on possibilities and constraints predefined by the particular history of each lineage.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biodiversity and Evolutionary Biology, Museo Nacional de Ciencias Naturales, CSIC, Madrid, Spain.

ABSTRACT

Background: Evolutionary novelties often appear by conferring completely new functions to pre-existing structures or by innovating the mechanism through which a particular function is performed. Sound production plays a central role in the behavior of frogs, which use their calls to delimit territories and attract mates. Therefore, frogs have evolved complex vocal structures capable of producing a wide variety of advertising sounds. It is generally acknowledged that most frogs call by moving an air column from the lungs through the glottis with the remarkable exception of the family Pipidae, whose members share a highly specialized sound production mechanism independent of air movement.

Results: Here, we performed behavioral observations in the poorly known African pipid genus Pseudhymenochirus and document that the sound production in this aquatic frog is almost certainly air-driven. However, morphological comparisons revealed an indisputable pipid nature of Pseudhymenochirus larynx. To place this paradoxical pattern into an evolutionary framework, we reconstructed robust molecular phylogenies of pipids based on complete mitochondrial genomes and nine nuclear protein-coding genes that coincided in placing Pseudhymenochirus nested among other pipids.

Conclusions: We conclude that although Pseudhymenochirus probably has evolved a reversal to the ancestral non-pipid condition of air-driven sound production, the mechanism through which it occurs is an evolutionary innovation based on the derived larynx of pipids. This strengthens the idea that evolutionary solutions to functional problems often emerge based on previous structures, and for this reason, innovations largely depend on possibilities and constraints predefined by the particular history of each lineage.

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Sound production in Pseudhymenochirus merlini. (a) Time series of emission of one note in a male, showing movement of throat and flanks indicative of movement of an air column (also see Aditional file 2: Movie). (b) Spectrogram and oscillogram of a male advertisement call with five notes. (c) Reconstruction under ML of ancestral character states of sound production mechanism (red without, and blue, with movement of air column) using BayesMultistate. (d) Preferred ancestral character state reconstruction of origin (red bar) and reversal (blue bar) of sound production mechanism; white bars represent the less parsimonious hypothesis of three independent origins of the implosion mechanism. (e) Same reconstruction under the alternative pipid phylogeny suggested by morphology.
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Figure 2: Sound production in Pseudhymenochirus merlini. (a) Time series of emission of one note in a male, showing movement of throat and flanks indicative of movement of an air column (also see Aditional file 2: Movie). (b) Spectrogram and oscillogram of a male advertisement call with five notes. (c) Reconstruction under ML of ancestral character states of sound production mechanism (red without, and blue, with movement of air column) using BayesMultistate. (d) Preferred ancestral character state reconstruction of origin (red bar) and reversal (blue bar) of sound production mechanism; white bars represent the less parsimonious hypothesis of three independent origins of the implosion mechanism. (e) Same reconstruction under the alternative pipid phylogeny suggested by morphology.

Mentions: In contrast to previous non-documented observations [20], we provide compelling behavioral data on Pseudhymenochirus merlini showing that this species, while calling, moves a column of atmospheric air from the lungs through the glottis (Additional file 2: Movie). We conclude that this movement of air almost certainly is causal for sound production in this species. Unlike all other extant pipid genera, all of which show a motionless calling, vocalizations in Pseudhymenochirus are clearly associated with intermittent constrictions of the posterior flanks and extension of the throat (Figure 2). The observed sequence of movements further suggests that sounds are produced during expiration, i.e., movement of the air from the lungs (Figure 2). Moreover, males produce release calls, showing also regular contractions of flanks and extension of throat.


Reversal to air-driven sound production revealed by a molecular phylogeny of tongueless frogs, family Pipidae.

Irisarri I, Vences M, San Mauro D, Glaw F, Zardoya R - BMC Evol. Biol. (2011)

Sound production in Pseudhymenochirus merlini. (a) Time series of emission of one note in a male, showing movement of throat and flanks indicative of movement of an air column (also see Aditional file 2: Movie). (b) Spectrogram and oscillogram of a male advertisement call with five notes. (c) Reconstruction under ML of ancestral character states of sound production mechanism (red without, and blue, with movement of air column) using BayesMultistate. (d) Preferred ancestral character state reconstruction of origin (red bar) and reversal (blue bar) of sound production mechanism; white bars represent the less parsimonious hypothesis of three independent origins of the implosion mechanism. (e) Same reconstruction under the alternative pipid phylogeny suggested by morphology.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3111386&req=5

Figure 2: Sound production in Pseudhymenochirus merlini. (a) Time series of emission of one note in a male, showing movement of throat and flanks indicative of movement of an air column (also see Aditional file 2: Movie). (b) Spectrogram and oscillogram of a male advertisement call with five notes. (c) Reconstruction under ML of ancestral character states of sound production mechanism (red without, and blue, with movement of air column) using BayesMultistate. (d) Preferred ancestral character state reconstruction of origin (red bar) and reversal (blue bar) of sound production mechanism; white bars represent the less parsimonious hypothesis of three independent origins of the implosion mechanism. (e) Same reconstruction under the alternative pipid phylogeny suggested by morphology.
Mentions: In contrast to previous non-documented observations [20], we provide compelling behavioral data on Pseudhymenochirus merlini showing that this species, while calling, moves a column of atmospheric air from the lungs through the glottis (Additional file 2: Movie). We conclude that this movement of air almost certainly is causal for sound production in this species. Unlike all other extant pipid genera, all of which show a motionless calling, vocalizations in Pseudhymenochirus are clearly associated with intermittent constrictions of the posterior flanks and extension of the throat (Figure 2). The observed sequence of movements further suggests that sounds are produced during expiration, i.e., movement of the air from the lungs (Figure 2). Moreover, males produce release calls, showing also regular contractions of flanks and extension of throat.

Bottom Line: To place this paradoxical pattern into an evolutionary framework, we reconstructed robust molecular phylogenies of pipids based on complete mitochondrial genomes and nine nuclear protein-coding genes that coincided in placing Pseudhymenochirus nested among other pipids.We conclude that although Pseudhymenochirus probably has evolved a reversal to the ancestral non-pipid condition of air-driven sound production, the mechanism through which it occurs is an evolutionary innovation based on the derived larynx of pipids.This strengthens the idea that evolutionary solutions to functional problems often emerge based on previous structures, and for this reason, innovations largely depend on possibilities and constraints predefined by the particular history of each lineage.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biodiversity and Evolutionary Biology, Museo Nacional de Ciencias Naturales, CSIC, Madrid, Spain.

ABSTRACT

Background: Evolutionary novelties often appear by conferring completely new functions to pre-existing structures or by innovating the mechanism through which a particular function is performed. Sound production plays a central role in the behavior of frogs, which use their calls to delimit territories and attract mates. Therefore, frogs have evolved complex vocal structures capable of producing a wide variety of advertising sounds. It is generally acknowledged that most frogs call by moving an air column from the lungs through the glottis with the remarkable exception of the family Pipidae, whose members share a highly specialized sound production mechanism independent of air movement.

Results: Here, we performed behavioral observations in the poorly known African pipid genus Pseudhymenochirus and document that the sound production in this aquatic frog is almost certainly air-driven. However, morphological comparisons revealed an indisputable pipid nature of Pseudhymenochirus larynx. To place this paradoxical pattern into an evolutionary framework, we reconstructed robust molecular phylogenies of pipids based on complete mitochondrial genomes and nine nuclear protein-coding genes that coincided in placing Pseudhymenochirus nested among other pipids.

Conclusions: We conclude that although Pseudhymenochirus probably has evolved a reversal to the ancestral non-pipid condition of air-driven sound production, the mechanism through which it occurs is an evolutionary innovation based on the derived larynx of pipids. This strengthens the idea that evolutionary solutions to functional problems often emerge based on previous structures, and for this reason, innovations largely depend on possibilities and constraints predefined by the particular history of each lineage.

Show MeSH
Related in: MedlinePlus