Neural Evolution of Context-Dependent Fly Song

Ding, Yun; Lillvis, Joshua L.; Cande, Jessica; Berman, Gordon J; Arthur, Ben J.; Long, Xi; Xu, Min; Dickson, Barry J.; Stern, David L.

doi:10.1016/j.cub.2019.02.019

Cited by 85 publications

(132 citation statements)

References 77 publications

(101 reference statements)

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“…Evidently, P1 neurons activate this circuit in parallel with a “command” network, including pIP10 descending interneurons 7, 49 , that triggers rapid-onset courtship behavior. These results illustrate how acute and enduring responses to sensory cues may be segregated into parallel neural pathways, allowing behavioral control on different time scales, with different degrees of flexibility (Fig.…”

Section: Discussionmentioning

confidence: 99%

Neurons that Function within an Integrator to Promote A Persistent Behavioral State in Drosophila

Jung

Kennedy

Chiu

et al. 2019

Preprint

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23Innate behaviors involve both reflexive motor programs and internal states. In 24 Drosophila, optogenetic activation of male-specific P1 interneurons triggers courtship song, 25 as well as a persistent behavioral state that prolongs courtship and enhances aggressiveness. 26 Here we identify pCd neurons as persistently activated by repeated P1 stimulation. pCd 27 neurons are required for P1-evoked persistent courtship and aggression, as well as for 28 normal social behavior. Activation of pCd neurons alone is inefficacious, but enhances and 29 prolongs courtship or aggression promoted by female cues. Transient female exposure 30 induced persistent increases in male aggressiveness, an effect suppressed by transiently 31 silencing pCd neurons. Transient silencing of pCd also disrupted P1-induced persistent 32 physiological activity, implying a requisite role in persistence. Finally, P1 activation of pCd 33 neurons enhanced their responsiveness to cVA, an aggression-promoting pheromone. Thus, 34 pCd neurons function within a circuit that integrates P1 input, to promote a persistent 35 internal state that enhances multiple social behaviors. 36 Fig. 1b) sensitized PPF1 neurons (ED Fig. 3).87 Gal4 line R41A01 labels a cell cluster called pCd, previously reported to play an important 88 role in female sexual receptivity 27 . Analysis of marker expression indicated that pCd cells are 89 5 cholinergic neurons that express both Fru and Dsx (ED Fig. 2f-i), two sex-determination factors 90that label neurons involved in male courtship and aggression 3,8,[28][29][30][31] . pCd neurons project densely 91 to the superior-medial protocerebrum (SMP), while extending an additional long fiber bundle 92 ventrally to innervate the dorsal region of the subesophageal zone (SEZ; Fig. 1d). Double labeling 93 of pCd neurons with somatodendritic (Denmark-RFP 32 ) and pre-synaptic (Syt-GFP 33 ) markers 94 revealed that their SMP projections are mostly dendritic, while their pre-synaptic terminals are 95 located in the SMP and the SEZ (ED Fig. 4d-f). Registration of P1 pre-synaptic labeling with pCd 96 somatodendritic labeling in a common brain template failed to reveal clear overlap (ED Fig. 4g-i), 97 and application of the GFP Reconstitution Across Synaptic Partner (GRASP 34 ) technique failed to 98 detect close proximity between P1 and pCd neurons (ED Fig. 4j-r), suggesting that functional 99 connectivity between these cells is unlikely to be monosynaptic. 100 pCd neuronal activity is required for P1-induced persistent social behaviors 101To test whether P1-evoked persistent social behaviors require pCd activity, we silenced the 102 latter using R41A01-LexA>LexAop-Kir2.1 while activating P1 a -split GAL4 neurons using UAS-103 Chrimson. In solitary males ( Fig. 2a), silencing pCd neurons dramatically reduced persistent wing 104 extension evoked by Chrimson activation of P1 cells ( Fig. 2b vs. 2c, green shading; 2d). 105Importantly, time-locked wing-extension during photostimulation was unaffected ( Fig. 2b-d, gray 106 shading). Pe...

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Section: Discussionmentioning

confidence: 99%

Neurons that Function within an Integrator to Promote A Persistent Behavioral State in Drosophila

Jung

Kennedy

Chiu

et al. 2019

Preprint

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“…[13][14][15][16][17] These findings led to the proposition that the P1 cluster functions as the center that makes the decision of whether or not to mate ( Figure 2F). 15,21,22 These interneurons connecting with P1 neurons turned out to be fru-positive, reinforcing the idea that the core portion of the courtship neural circuit is built up by connections among fru-positive neurons. The neurons that convey inputs reporting sensory cues to the P1 cluster as well as putative pathways operating downstream of the P1 cluster for motor control have been identified: e.g., inhibitory mAL and excitatory vAB3 and PPN1 as direct presynaptic interneurons for P1, [18][19][20] and P2b and pIP10 as direct postsynaptic interneurons.…”

Section: Sexu-mentioning

confidence: 58%

“…The neurons that convey inputs reporting sensory cues to the P1 cluster as well as putative pathways operating downstream of the P1 cluster for motor control have been identified: e.g., inhibitory mAL and excitatory vAB3 and PPN1 as direct presynaptic interneurons for P1, [18][19][20] and P2b and pIP10 as direct postsynaptic interneurons. 15,21,22 These interneurons connecting with P1 neurons turned out to be fru-positive, reinforcing the idea that the core portion of the courtship neural circuit is built up by connections among fru-positive neurons. 23 The question arises as to how fru orchestrates the formation of mutual connections between a specific set of fru-positive neurons to organize the entire courtship circuit.…”

Section: Fruitless As the Primary Organizer Of Male Courtship Circuitsmentioning

confidence: 58%

The mode of action of Fruitless: Is it an easy matter to switch the sex?

Sato

Yamamoto

2019

Genes Brain and Behavior

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The fruitless (fru) locus was originally defined by a male sterile mutation that promotes male‐to‐male courtship while suppressing male‐to‐female courtship in Drosophila melanogaster. The fru promoter‐1 pre‐RNA generates a set of BTB‐zinc finger family FruM proteins expressed exclusively in the male neurons, leading to the formation of sexual dimorphisms in neurons via male‐specific neuroblast proliferation, male‐specific neural survival, male‐specific neuritegenesis or male‐specific arbor patterning. Such a wide spectrum of phenotypic effects seems to result from chromatin modifications, in which FruBM recruits Bonus, Histone deacetylase 1 (HDAC1) and/or Heterochromatin protein 1a (HP1a) to ~130 target sites. One established FruBM transcriptional target is the axon guidance protein gene robo1. Multiple transcriptional regulator‐binding sites are nested around the FruBM‐binding site, and mediate sophisticated modulation of the repressor activity of FruBM. FruBM also binds to the Lola‐Q transcriptional repressor to protect it from proteasome‐dependent degradation in male but not female neurons as FruBM exists only in male neurons, leading to the formation of sexually dimorphic neural structures. These findings shed light on the multilayered network of transcription regulation orchestrated by the master regulator FruBM.

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“…Inhibition of the descending pIP10 neurons by tetanus toxin results in loss of the clack component of the song, and optogenetic activation of the pIP10 neuron results in the production of clack song. Production of the clack song is dependent on the level of light intensity (Ding et al 2019). In D. yakuba, under low light only clacks are produced, but under high light intensity, clacks followed by a pulse song are observed, indicating that pIP10 neurons can access both pulse and clack song circuits in an environment-dependent manner.…”

Section: Courtship Songmentioning

confidence: 99%

“…In D. yakuba, under low light only clacks are produced, but under high light intensity, clacks followed by a pulse song are observed, indicating that pIP10 neurons can access both pulse and clack song circuits in an environment-dependent manner. Whereas electrophysiological properties of the pIP10 neurons are conserved between D. yakuba and D. melanogaster, a neuroanatomical comparison between these species showed significant quantifiable differences in the song circuit, with about a twofold increase in the mesothoracic triangle of D. yakuba compared to D. melanogaster (Ding et al 2019). The mesothoracic triangle is a triangular-shaped structure between the dorsal pro-and mesothoracic ganglia in the ventral nerve cord, which represents a neural circuit associated with courtship behavior (Yu et al 2010).…”

Section: Courtship Songmentioning

confidence: 99%

Evolution of Reproductive Behavior

et al. 2020

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Behaviors associated with reproduction are major contributors to the evolutionary success of organisms and are subject to many evolutionary forces, including natural and sexual selection, and sexual conflict. Successful reproduction involves a range of behaviors, from finding an appropriate mate, courting, and copulation, to the successful production and (in oviparous animals) deposition of eggs following mating. As a consequence, behaviors and genes associated with reproduction are often under strong selection and evolve rapidly. Courtship rituals in flies follow a multimodal pattern, mediated through visual, chemical, tactile, and auditory signals. Premating behaviors allow males and females to assess the species identity, reproductive state, and condition of their partners. Conflicts between the "interests" of individual males, and/or between the reproductive strategies of males and females, often drive the evolution of reproductive behaviors. For example, seminal proteins transmitted by males often show evidence of rapid evolution, mediated by positive selection. Postmating behaviors, including the selection of oviposition sites, are highly variable and Drosophila species span the spectrum from generalists to obligate specialists. Chemical recognition features prominently in adaptation to host plants for feeding and oviposition. Selection acting on variation in pre-, peri-, and postmating behaviors can lead to reproductive isolation and incipient speciation. Response to selection at the genetic level can include the expansion of gene families, such as those for detecting pheromonal cues for mating, or changes in the expression of genes leading to visual cues such as wing spots that are assessed during mating. Here, we consider the evolution of reproductive behavior in Drosophila at two distinct, yet complementary, scales. Some studies take a microevolutionary approach, identifying genes and networks involved in reproduction, and then dissecting the genetics underlying complex behaviors in D. melanogaster. Other studies take a macroevolutionary approach, comparing reproductive behaviors across the genus Drosophila and how these might correlate with environmental cues. A full synthesis of this field will require unification across these levels.

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Neural Evolution of Context-Dependent Fly Song

Cited by 85 publications

References 77 publications

Neurons that Function within an Integrator to Promote A Persistent Behavioral State in Drosophila

Neurons that Function within an Integrator to Promote A Persistent Behavioral State in Drosophila

The mode of action of Fruitless: Is it an easy matter to switch the sex?

Evolution of Reproductive Behavior

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