Quantitative and Discrete Evolutionary Changes in the Egg-Laying Behavior of Single Drosophila Females
How a nervous system assembles and coordinates a suite of elementary behavioral steps into a complex behavior is not well understood. While often presented as a stereotyped sequence of events, even extensively studied behaviors such as fly courtship are rarely a strict repetition of the same steps i...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-05-01
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| Series: | Frontiers in Behavioral Neuroscience |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fnbeh.2019.00118/full |
| _version_ | 1818485914513440768 |
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| author | Lasse B. Bräcker Christian A. Schmid Verena A. Bolini Claudia A. Holz Benjamin Prud’homme Anton Sirota Nicolas Gompel |
| author_facet | Lasse B. Bräcker Christian A. Schmid Verena A. Bolini Claudia A. Holz Benjamin Prud’homme Anton Sirota Nicolas Gompel |
| author_sort | Lasse B. Bräcker |
| collection | DOAJ |
| description | How a nervous system assembles and coordinates a suite of elementary behavioral steps into a complex behavior is not well understood. While often presented as a stereotyped sequence of events, even extensively studied behaviors such as fly courtship are rarely a strict repetition of the same steps in a predetermined sequence in time. We are focusing on oviposition, the act of laying an egg, in flies of the genus Drosophila to describe the elementary behavioral steps or microbehaviors that a single female fly undertakes prior to and during egg laying. We have analyzed the hierarchy and relationships in time of these microbehaviors in three closely related Drosophila species with divergent egg-laying preferences and uncovered cryptic differences in their behavioral patterns. Using high-speed imaging, we quantified in depth the oviposition behavior of single females of Drosophila suzukii, Drosophila biarmipes and Drosophila melanogaster in a novel behavioral assay. By computing transitions between microbehaviors, we identified a common ethogram structure underlying oviposition of all three species. Quantifying parameters such as relative time spent on a microbehavior and its average duration, however, revealed clear differences between species. In addition, we examined the temporal dynamics and probability of transitions to different microbehaviors relative to a central event of oviposition, ovipositor contact. Although the quantitative analysis highlights behavioral variability across flies, it reveals some interesting trends for each species in the mode of substrate sampling, as well as possible evolutionary differences. Larger datasets derived from automated video annotation will overcome this paucity of data in the future, and use the same framework to reappraise these observed differences. Our study reveals a common architecture to the oviposition ethogram of three Drosophila species, indicating its ancestral state. It also indicates that Drosophila suzukii’s behavior departs quantitatively and qualitatively from that of the outgroup species, in line with its known divergent ethology. Together, our results illustrate how a global shift in ethology breaks down in the quantitative reorganization of the elementary steps underlying a complex behavior. |
| first_indexed | 2024-12-10T16:15:47Z |
| format | Article |
| id | doaj.art-4724e26ed0a34d6fbf3b477f1bfea9f4 |
| institution | Directory Open Access Journal |
| issn | 1662-5153 |
| language | English |
| last_indexed | 2024-12-10T16:15:47Z |
| publishDate | 2019-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Behavioral Neuroscience |
| spelling | doaj.art-4724e26ed0a34d6fbf3b477f1bfea9f42022-12-22T01:41:58ZengFrontiers Media S.A.Frontiers in Behavioral Neuroscience1662-51532019-05-011310.3389/fnbeh.2019.00118453796Quantitative and Discrete Evolutionary Changes in the Egg-Laying Behavior of Single Drosophila FemalesLasse B. Bräcker0Christian A. Schmid1Verena A. Bolini2Claudia A. Holz3Benjamin Prud’homme4Anton Sirota5Nicolas Gompel6Fakultät für Biologie, Biozentrum, Ludwig-Maximilians Universität München, Munich, GermanyFakultät für Biologie, Biozentrum, Ludwig-Maximilians Universität München, Munich, GermanyFakultät für Biologie, Biozentrum, Ludwig-Maximilians Universität München, Munich, GermanyFakultät für Biologie, Biozentrum, Ludwig-Maximilians Universität München, Munich, GermanyAix-Marseille Université, CNRS, IBDM, Institut de Biologie du Développement de Marseille, Campus de Luminy Case 907, Marseille, FranceBernstein Center for Computational Neuroscience Munich, Faculty of Medicine, Ludwig-Maximilians-Universität München, Planegg-Martinsried, GermanyFakultät für Biologie, Biozentrum, Ludwig-Maximilians Universität München, Munich, GermanyHow a nervous system assembles and coordinates a suite of elementary behavioral steps into a complex behavior is not well understood. While often presented as a stereotyped sequence of events, even extensively studied behaviors such as fly courtship are rarely a strict repetition of the same steps in a predetermined sequence in time. We are focusing on oviposition, the act of laying an egg, in flies of the genus Drosophila to describe the elementary behavioral steps or microbehaviors that a single female fly undertakes prior to and during egg laying. We have analyzed the hierarchy and relationships in time of these microbehaviors in three closely related Drosophila species with divergent egg-laying preferences and uncovered cryptic differences in their behavioral patterns. Using high-speed imaging, we quantified in depth the oviposition behavior of single females of Drosophila suzukii, Drosophila biarmipes and Drosophila melanogaster in a novel behavioral assay. By computing transitions between microbehaviors, we identified a common ethogram structure underlying oviposition of all three species. Quantifying parameters such as relative time spent on a microbehavior and its average duration, however, revealed clear differences between species. In addition, we examined the temporal dynamics and probability of transitions to different microbehaviors relative to a central event of oviposition, ovipositor contact. Although the quantitative analysis highlights behavioral variability across flies, it reveals some interesting trends for each species in the mode of substrate sampling, as well as possible evolutionary differences. Larger datasets derived from automated video annotation will overcome this paucity of data in the future, and use the same framework to reappraise these observed differences. Our study reveals a common architecture to the oviposition ethogram of three Drosophila species, indicating its ancestral state. It also indicates that Drosophila suzukii’s behavior departs quantitatively and qualitatively from that of the outgroup species, in line with its known divergent ethology. Together, our results illustrate how a global shift in ethology breaks down in the quantitative reorganization of the elementary steps underlying a complex behavior.https://www.frontiersin.org/article/10.3389/fnbeh.2019.00118/fullDrosophilabehaviorethogramevolutionovipositiondecision making |
| spellingShingle | Lasse B. Bräcker Christian A. Schmid Verena A. Bolini Claudia A. Holz Benjamin Prud’homme Anton Sirota Nicolas Gompel Quantitative and Discrete Evolutionary Changes in the Egg-Laying Behavior of Single Drosophila Females Frontiers in Behavioral Neuroscience Drosophila behavior ethogram evolution oviposition decision making |
| title | Quantitative and Discrete Evolutionary Changes in the Egg-Laying Behavior of Single Drosophila Females |
| title_full | Quantitative and Discrete Evolutionary Changes in the Egg-Laying Behavior of Single Drosophila Females |
| title_fullStr | Quantitative and Discrete Evolutionary Changes in the Egg-Laying Behavior of Single Drosophila Females |
| title_full_unstemmed | Quantitative and Discrete Evolutionary Changes in the Egg-Laying Behavior of Single Drosophila Females |
| title_short | Quantitative and Discrete Evolutionary Changes in the Egg-Laying Behavior of Single Drosophila Females |
| title_sort | quantitative and discrete evolutionary changes in the egg laying behavior of single drosophila females |
| topic | Drosophila behavior ethogram evolution oviposition decision making |
| url | https://www.frontiersin.org/article/10.3389/fnbeh.2019.00118/full |
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