Precopulatory acoustic interactions of the New World malaria vector Anopheles albimanus (Diptera: Culicidae)
Abstract Background Anopheles albimanus is a malaria vector in Central America, northern South America and the Caribbean. Although a public health threat, An. albimanus precopulatory mating behaviors are unknown. Acoustics play important roles in mosquito communication, where flight tones allow male...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2019-08-01
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| Series: | Parasites & Vectors |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s13071-019-3648-8 |
| _version_ | 1818306960119824384 |
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| author | Hoover Pantoja-Sánchez Sebastián Gomez Viviana Velez Frank W. Avila Catalina Alfonso-Parra |
| author_facet | Hoover Pantoja-Sánchez Sebastián Gomez Viviana Velez Frank W. Avila Catalina Alfonso-Parra |
| author_sort | Hoover Pantoja-Sánchez |
| collection | DOAJ |
| description | Abstract Background Anopheles albimanus is a malaria vector in Central America, northern South America and the Caribbean. Although a public health threat, An. albimanus precopulatory mating behaviors are unknown. Acoustics play important roles in mosquito communication, where flight tones allow males to detect and attract potential mates. The importance of sound in precopulatory interactions has been demonstrated in Toxorhynchites brevipalpis, Aedes aegypti, Culex quinquefasciatus and Anopheles gambiae; convergence in a shared harmonic of the wing beat frequency (WBF) during courtship is thought to increase the chance of copulation. To our knowledge, An. albimanus precopulatory acoustic behaviors have not been described to date. Here, we characterized An. albimanus (i) male and female flight tones; (ii) male–female precopulatory acoustic interactions under tethered and free flight conditions; and (iii) male-male acoustic interactions during free flight. Results We found significant increases in the WBFs of both sexes in free flight compared to when tethered. We observed harmonic convergence between 79% of tethered couples. In free flight, we identified a female-specific behavior that predicts mate rejection during male mating attempts: females increase their WBFs significantly faster during mate rejection compared to a successful copulation. This behavior consistently occurred during mate rejection regardless of prior mating attempts (from the same or differing male). During group flight, males of An. albimanus displayed two distinct flying behaviors: random flight and a swarm-like, patterned flight, each associated with distinct acoustic characteristics. In the transition from random to patterned flight, males converged their WBFs and significantly decreased flight area, male-male proximity and the periodicity of their trajectories. Conclusions We show that tethering of An. albimanus results in major acoustic differences compared to free flight. We identify a female-specific behavior that predicts mate rejection during male mating attempts in this species and show that male groups in free flight display distinct flying patterns with unique audio and visual characteristics. This study shows that An. albimanus display acoustic features identified in other mosquito species, further suggesting that acoustic interactions provide worthwhile targets for mosquito intervention strategies. Our results provide compelling evidence for swarming in this species and suggests that acoustic signaling is important for this behavior. |
| first_indexed | 2024-12-13T06:50:47Z |
| format | Article |
| id | doaj.art-fd010a2f5fca47d7bb3dd23d09532c42 |
| institution | Directory Open Access Journal |
| issn | 1756-3305 |
| language | English |
| last_indexed | 2024-12-13T06:50:47Z |
| publishDate | 2019-08-01 |
| publisher | BMC |
| record_format | Article |
| series | Parasites & Vectors |
| spelling | doaj.art-fd010a2f5fca47d7bb3dd23d09532c422022-12-21T23:56:09ZengBMCParasites & Vectors1756-33052019-08-0112111210.1186/s13071-019-3648-8Precopulatory acoustic interactions of the New World malaria vector Anopheles albimanus (Diptera: Culicidae)Hoover Pantoja-Sánchez0Sebastián Gomez1Viviana Velez2Frank W. Avila3Catalina Alfonso-Parra4Departamento de Ingeniería Electrónica, SISTEMIC, Universidad de AntioquiaDepartamento de Ingeniería Electrónica, SISTEMIC, Universidad de AntioquiaPrograma de Estudio y Control de Enfermedades Tropicales, PECET, Universidad de AntioquiaMax Planck Tandem Group in Mosquito Reproductive Biology, Universidad de AntioquiaInstituto Colombiano de Medicina Tropical, Universidad CESAbstract Background Anopheles albimanus is a malaria vector in Central America, northern South America and the Caribbean. Although a public health threat, An. albimanus precopulatory mating behaviors are unknown. Acoustics play important roles in mosquito communication, where flight tones allow males to detect and attract potential mates. The importance of sound in precopulatory interactions has been demonstrated in Toxorhynchites brevipalpis, Aedes aegypti, Culex quinquefasciatus and Anopheles gambiae; convergence in a shared harmonic of the wing beat frequency (WBF) during courtship is thought to increase the chance of copulation. To our knowledge, An. albimanus precopulatory acoustic behaviors have not been described to date. Here, we characterized An. albimanus (i) male and female flight tones; (ii) male–female precopulatory acoustic interactions under tethered and free flight conditions; and (iii) male-male acoustic interactions during free flight. Results We found significant increases in the WBFs of both sexes in free flight compared to when tethered. We observed harmonic convergence between 79% of tethered couples. In free flight, we identified a female-specific behavior that predicts mate rejection during male mating attempts: females increase their WBFs significantly faster during mate rejection compared to a successful copulation. This behavior consistently occurred during mate rejection regardless of prior mating attempts (from the same or differing male). During group flight, males of An. albimanus displayed two distinct flying behaviors: random flight and a swarm-like, patterned flight, each associated with distinct acoustic characteristics. In the transition from random to patterned flight, males converged their WBFs and significantly decreased flight area, male-male proximity and the periodicity of their trajectories. Conclusions We show that tethering of An. albimanus results in major acoustic differences compared to free flight. We identify a female-specific behavior that predicts mate rejection during male mating attempts in this species and show that male groups in free flight display distinct flying patterns with unique audio and visual characteristics. This study shows that An. albimanus display acoustic features identified in other mosquito species, further suggesting that acoustic interactions provide worthwhile targets for mosquito intervention strategies. Our results provide compelling evidence for swarming in this species and suggests that acoustic signaling is important for this behavior.http://link.springer.com/article/10.1186/s13071-019-3648-8MosquitoMalariaHarmonic convergenceSwarmingMating |
| spellingShingle | Hoover Pantoja-Sánchez Sebastián Gomez Viviana Velez Frank W. Avila Catalina Alfonso-Parra Precopulatory acoustic interactions of the New World malaria vector Anopheles albimanus (Diptera: Culicidae) Parasites & Vectors Mosquito Malaria Harmonic convergence Swarming Mating |
| title | Precopulatory acoustic interactions of the New World malaria vector Anopheles albimanus (Diptera: Culicidae) |
| title_full | Precopulatory acoustic interactions of the New World malaria vector Anopheles albimanus (Diptera: Culicidae) |
| title_fullStr | Precopulatory acoustic interactions of the New World malaria vector Anopheles albimanus (Diptera: Culicidae) |
| title_full_unstemmed | Precopulatory acoustic interactions of the New World malaria vector Anopheles albimanus (Diptera: Culicidae) |
| title_short | Precopulatory acoustic interactions of the New World malaria vector Anopheles albimanus (Diptera: Culicidae) |
| title_sort | precopulatory acoustic interactions of the new world malaria vector anopheles albimanus diptera culicidae |
| topic | Mosquito Malaria Harmonic convergence Swarming Mating |
| url | http://link.springer.com/article/10.1186/s13071-019-3648-8 |
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