Pheromones mediating copulation and attraction in Drosophila

Intraspecific olfactory signals known as pheromones play important roles in insect mating systems. In the model Drosophila melanogaster, a key part of the pheromone-detecting system has remained enigmatic through many years of research in terms of both its behavioral significance and its activating ligands. Here we show that Or47b-and Or88a-expressing olfactory sensory neurons (OSNs) detect the fly-produced odorants methyl laurate (ML), methyl myristate, and methyl palmitate. Fruitless (fruM)-positive Or47b-expressing OSNs detect ML exclusively, and Or47b- and Or47b-expressing OSNs are required for optimal male copulation behavior. In addition, activation of Or47b-expressing OSNs in the male is sufficient to provide a competitive mating advantage. We further find that the vigorous male courtship displayed toward oenocyte-less flies is attributed to an oenocyte-independent sustained production of the Or47b ligand, ML. In addition, we reveal that Or88a-expressing OSNs respond to all three compounds, and that these neurons are necessary and sufficient for attraction behavior in both males and females. Beyond the OSN level, information regarding the three fly odorants is transferred from the antennal lobe to higher brain centers in two dedicated neural lines. Finally, we find that both Or47b- and Or88a-based systems and their ligands are remarkably conserved over a number of drosophilid species. Taken together, our results close a significant gap in the understanding of the olfactory background to Drosophila mating and attraction behavior; while reproductive isolation barriers between species are created mainly by species-specific signals, the mating enhancing signal in several Drosophila species is conserved.

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Changes in splicing and neuromodulatory gene expression programs in sensory neurons with pheromone signaling and social experience

10.1101/2021.06.18.449021 ◽

2021 ◽

Author(s):

Pelin C Volkan ◽

Bryson Deanhardt ◽

Qichen Duan ◽

Chengcheng Du ◽

Charles Soeder ◽

...

Keyword(s):

Sensory Neurons ◽

Molecular Mechanisms ◽

Social Experience ◽

Rna Seq ◽

Male Courtship ◽

Wild Type ◽

Pheromone Signaling ◽

Courtship Behaviors ◽

Necessary And Sufficient ◽

Splicing Patterns

Social experience and pheromone signaling in ORNs affect pheromone responses and male courtship behaviors in Drosophila, however, the molecular mechanisms underlying this circuit-level neuromodulation remain less clear. Previous studies identified social experience and pheromone signaling-dependent modulation of chromatin around behavioral switch gene fruitless, which encodes a transcription factor necessary and sufficient for male behaviors. To identify the molecular mechanisms driving social experience-dependent neuromodulation, we performed RNA-seq from antennal samples of mutant fruit flies in pheromone receptors and fruitless, as well as grouped or isolated wild-type males. We found that loss of pheromone detection differentially alters the levels of fruitless exons suggesting changes in splicing patterns. In addition, many Fruitless target neuromodulatory genes, such as neurotransmitter receptors, ion channels, and ion transporters, are differentially regulated by social context and pheromone signaling. Our results suggest that modulation of circuit activity and behaviors in response to social experience and pheromone signaling arise due to changes in transcriptional programs for neuromodulators downstream of behavioral switch gene function.

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Reproductive behavior

10.1093/oso/9780198797500.003.0013 ◽

2018 ◽

Cited By ~ 1

Author(s):

Rachel Olzer ◽

Rebecca L. Ehrlich ◽

Justa L. Heinen-Kay ◽

Jessie Tanner ◽

Marlene Zuk

Keyword(s):

Sexual Selection ◽

Sexual Conflict ◽

Female Choice ◽

Reproductive Behavior ◽

Mating Systems ◽

Insect Behavior ◽

Sequential Approach ◽

Evolutionary Mechanisms ◽

Anatomy And Physiology ◽

Males And Females

Sex and reproduction lie at the heart of studies of insect behavior. We begin by providing a brief overview of insect anatomy and physiology, followed by an introduction to the overarching themes of parental investment, sexual selection, and mating systems. We then take a sequential approach to illustrate the diversity of phenomena and concepts behind insect reproductive behavior from pre-copulatory mate signalling through copulatory sperm transfer, mating positions, and sexual conflict, to post-copulatory sperm competition, and cryptic female choice. We provide an overview of the evolutionary mechanisms driving reproductive behavior. These events are linked by the economic defendability of mates or resources, and how these are allocated in each sex. Under the framework of economic defendability, the reader can better understand how sexual antagonistic behaviors arise as the result of competing optimal fitness strategies between males and females.

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Localization of genes affecting species differences in male courtship song between Drosophila virilis and D. littoralis

Genetics Research ◽

10.1017/s0016672399004097 ◽

2000 ◽

Vol 75 (1) ◽

pp. 37-45 ◽

Cited By ~ 24

Author(s):

ANNELI HOIKKALA ◽

SELIINA PÄÄLLYSAHO ◽

JOUNI ASPI ◽

JAAKKO LUMME

Keyword(s):

Species Differences ◽

Courtship Song ◽

Drosophila Virilis ◽

Marker Genes ◽

Sound Pulse ◽

Male Courtship ◽

Chromosomal Genes ◽

Pause Length ◽

Species Specific ◽

Sound Pulses

The males of six species of the Drosophila virilis group (including D. virilis) keep their wings extended while producing a train of sound pulses, where the pulses follow each other without any pause. The males of the remaining five species of the group produce only one sound pulse during each wing extension/vibration, which results in species-specific songs with long pauses (in D. littoralis about 300 ms) between successive sound pulses. Genetic analyses of the differences between the songs of D. virilis and D. littoralis showed that species-specific song traits are affected by genes on the X chromosome, and for the length of pause, also by genes on chromosomes 3 and 4. The X chromosomal genes having a major impact on pulse and pause length were tightly linked with white, apricot and notched marker genes located at the proximal third of the chromosome. A large inversion in D. littoralis, marked by notched, prevents more precise localization of these genes by classical crossing methods.

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Nocturnal mating behaviour and dynamic male investment of copulation time in the southern blue-ringed octopus, Hapalochlaena maculosa (Cephalopoda: Octopodidae)

Behaviour ◽

10.1163/1568539x-00003321 ◽

2015 ◽

Vol 152 (14) ◽

pp. 1883-1910 ◽

Cited By ~ 5

Author(s):

Peter Morse ◽

Kyall R. Zenger ◽

Mark I. McCormick ◽

Mark G. Meekan ◽

Christine L. Huffard

Keyword(s):

Mating Systems ◽

Mating Behaviour ◽

Female Size ◽

Male Size ◽

Male Preference ◽

Video Footage ◽

Mating History ◽

Males And Females ◽

Strategic Allocation ◽

Do So

The southern blue-ringed octopus,Hapalochlaena maculosaHoyle (1883), is a nocturnal species that exhibits a mating system in which females hold sperm from multiple males over a one to two month breeding window before laying a single egg clutch. Contrary to most studied animal mating systems where anisogamy exists, gamete package production is limited for both males and females of this species (approx. 50 spermatophores/eggs). This presents an animal model for studying aspects of sperm competition and dynamic mate choice behaviours. The present study reports on the mating behaviour ofH. maculosaobserved under laboratory conditions using infrared closed-circuit television video footage. Rates of male copulation attempts increased with male size, while female receptivity to mating attempts increased with female size, resulting in larger animals of both sexes gaining more copulations and spending more time per day in copulation. There was some evidence of female preference of larger males, but no male preference of females based on measured morphological traits. Both sexes terminated copulations in equal frequencies but male-terminated copulations were significantly shorter in duration. Males were more likely to terminate copulation early with females they had previously mated with, however were less likely to do so if the female had recently mated with a different male. Among male-terminated copulations, males mated for longer with females that had previously mated with other males in the trial. Male–male mounts were as common as male–female mounts, suggesting that maleH. maculosaare not able to discriminate the sex of conspecifics. These findings suggest male strategic allocation of spermatophores based female mating history is an important factor influencing mating behaviours of this species.

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2. Mating systems, or who goes with whom, and for how long

Sexual Selection: A Very Short Introduction ◽

10.1093/actrade/9780198778752.003.0002 ◽

2018 ◽

pp. 16-33

Author(s):

Leigh W. Simmons

Keyword(s):

Sexual Selection ◽

Mating System ◽

Social Relationships ◽

Breeding Season ◽

Mating Systems ◽

Practical Applications ◽

Multiple Partners ◽

Monogamous Species ◽

Genetic Techniques ◽

Males And Females

‘Mating systems, or who goes with whom, and for how long’ examines the variation in how males and females associate during the breeding season, ranging from brief couplings with multiple partners to lifelong monogamy. It also shows how the discovery that females mate with many partners, even in supposedly monogamous species such as songbirds, was made possible by modern genetic techniques. Variation in mating systems holds considerable implications for the operation of sexual selection. The way that animal mating systems have been explained historically is outlined before considering how a more contemporary understanding of genetic and social relationships has reshaped our thinking and how understanding a species’ mating system can have practical applications.

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The effects of naloxone on courtship and pairing behaviour in male and female zebra finches: the importance of testing mechanisms using multiple paradigms

Behaviour ◽

10.1163/1568539x-00003234 ◽

2015 ◽

Vol 152 (1) ◽

pp. 107-126 ◽

Cited By ~ 4

Author(s):

Michelle L. Tomaszycki ◽

Joanna H. Schnelker ◽

Brendon P. Zatirka

Keyword(s):

Repeated Measures ◽

Forced Choice ◽

Opioid Antagonist ◽

Zebra Finches ◽

Partner Preference ◽

Male Courtship ◽

Partner Preferences ◽

Pair Bonds ◽

Males And Females ◽

Pairing Behaviour

Opioids are implicated in social attachments, but their role in avian pair bonds is not well understood. The present study tested the effects of naloxone, an opioid antagonist, on pairing using both a forced-choice and a mixed-sex aviary paradigm. First, three doses of naloxone were systemically administered in males using a repeated measures forced-choice design, partner preference formation was tested on the second day. Males treated with 20 mg/kg sang less undirected song. Males treated with 10 mg/kg of naloxone sang less to the familiar partner than when treated with saline and were less likely to form a partner preference than were other treatments. In females, 10 mg/kg of naloxone in a forced-choice paradigm increased preference for the unfamiliar over the familiar male. Finally, males and females were administered either naloxone (10 mg/kg) or saline in a mixed-sex aviary. In females, naloxone increased pairing behaviours, but had no other effects in either sex. Our findings suggest that the effects of naloxone on pairing-related behaviours are context-dependent; male–male competition may decrease the effects of naloxone on male song and a choice of mates may increase affiliation in females in a semi-naturalistic paradigm, and increase preferences for an unfamiliar partner in a forced-choice paradigm. Our findings highlight the importance of using multiple paradigms to test mechanisms of behaviour. These findings contribute to our understanding of the mechanisms of monogamous relationships and suggest that opioids play a role in male courtship, female affiliation and partner preferences in both sexes of zebra finches, but that context is important.

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Variable Rates of Simple Satellite Gains across the Drosophila Phylogeny

Molecular Biology and Evolution ◽

10.1093/molbev/msy005 ◽

2018 ◽

Vol 35 (4) ◽

pp. 925-941 ◽

Cited By ~ 31

Author(s):

Kevin H -C Wei ◽

Sarah E Lower ◽

Ian V Caldas ◽

Trevor J S Sless ◽

Daniel A Barbash ◽

...

Keyword(s):

Evolutionary Dynamics ◽

Rapid Evolution ◽

Single Mutation ◽

Closely Related Species ◽

Interspecific Differences ◽

Limited Sampling ◽

Drosophila Phylogeny ◽

Males And Females ◽

Species Specific ◽

Turn Over

Abstract Simple satellites are tandemly repeating short DNA motifs that can span megabases in eukaryotic genomes. Because they can cause genomic instability through nonallelic homologous exchange, they are primarily found in the repressive heterochromatin near centromeres and telomeres where recombination is minimal, and on the Y chromosome, where they accumulate as the chromosome degenerates. Interestingly, the types and abundances of simple satellites often vary dramatically between closely related species, suggesting that they turn over rapidly. However, limited sampling has prevented detailed understanding of their evolutionary dynamics. Here, we characterize simple satellites from whole-genome sequences generated from males and females of nine Drosophila species, spanning 40 Ma of evolution. We show that PCR-free library preparation and postsequencing GC-correction better capture satellite quantities than conventional methods. We find that over half of the 207 simple satellites identified are species-specific, consistent with previous descriptions of their rapid evolution. Based on a maximum parsimony framework, we determined that most interspecific differences are due to lineage-specific gains. Simple satellites gained within a species are typically a single mutation away from abundant existing satellites, suggesting that they likely emerge from existing satellites, especially in the genomes of satellite-rich species. Interestingly, unlike most of the other lineages which experience various degrees of gains, the lineage leading up to the satellite-poor D. pseudoobscura and D. persimilis appears to be recalcitrant to gains, providing a counterpoint to the notion that simple satellites are universally rapidly evolving.

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Auditory experience controls the maturation of song discrimination and sexual response in Drosophila

eLife ◽

10.7554/elife.34348 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 18

Author(s):

Xiaodong Li ◽

Hiroshi Ishimoto ◽

Azusa Kamikouchi

Keyword(s):

Sexual Behavior ◽

Song Learning ◽

Song Perception ◽

Auditory Experience ◽

Song Discrimination ◽

Integration Node ◽

Males And Females ◽

Acoustic Exposure ◽

Species Specific ◽

Molecular Nature

In birds and higher mammals, auditory experience during development is critical to discriminate sound patterns in adulthood. However, the neural and molecular nature of this acquired ability remains elusive. In fruit flies, acoustic perception has been thought to be innate. Here we report, surprisingly, that auditory experience of a species-specific courtship song in developing Drosophila shapes adult song perception and resultant sexual behavior. Preferences in the song-response behaviors of both males and females were tuned by social acoustic exposure during development. We examined the molecular and cellular determinants of this social acoustic learning and found that GABA signaling acting on the GABAA receptor Rdl in the pC1 neurons, the integration node for courtship stimuli, regulated auditory tuning and sexual behavior. These findings demonstrate that maturation of auditory perception in flies is unexpectedly plastic and is acquired socially, providing a model to investigate how song learning regulates mating preference in insects.

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Cuticular hydrocarbons for identifying Sarcophagidae (Diptera)

Scientific Reports ◽

10.1038/s41598-021-87221-y ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Hannah E. Moore ◽

Martin J. R. Hall ◽

Falko P. Drijfhout ◽

Robert B. Cody ◽

Daniel Whitmore

Keyword(s):

Cuticular Hydrocarbons ◽

Gas Chromatography Mass Spectrometry ◽

Sexually Dimorphic ◽

Adult Males ◽

History Museum ◽

Chemical Profiles ◽

Males And Females ◽

Species Specific ◽

Flesh Flies ◽

Eleven Species

AbstractThe composition and quantity of insect cuticular hydrocarbons (CHCs) can be species-specific as well as sexually dimorphic within species. CHC analysis has been previously used for identification and ageing purposes for several insect orders including true flies (Diptera). Here, we analysed the CHC chemical profiles of adult males and females of eleven species of flesh flies belonging to the genus Sarcophaga Meigen (Sarcophagidae), namely Sarcophaga africa (Wiedemann), S. agnata Rondani, S. argyrostoma Robineau-Desvoidy, S. carnaria (Linnaeus), S. crassipalpis Macquart, S. melanura Meigen, S. pumila Meigen, S. teretirostris Pandellé, S. subvicina Rohdendorf, S. vagans Meigen and S. variegata (Scopoli). Cuticular hydrocarbons extracted from pinned specimens from the collections of the Natural History Museum, London using a customised extraction technique were analysed using Gas Chromatography–Mass Spectrometry. Time of preservation prior to extraction ranged between a few weeks to over one hundred years. CHC profiles (1) allowed reliable identification of a large majority of specimens, (2) differed between males and females of the same species, (3) reliably associated males and females of the same species, provided sufficient replicates (up to 10) of each sex were analysed, and (4) identified specimens preserved for up to over one hundred years prior to extraction.

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SCENT MARKING IN MEADOW VOLES AND PRAIRIE VOLES: A TEST OF THREE HYPOTHESES

Behaviour ◽

10.1163/156853901317367618 ◽

2001 ◽

Vol 138 (11-12) ◽

pp. 1319-1336 ◽

Cited By ~ 16

Author(s):

S.G. Mech ◽

M.H. Ferkin ◽

Keyword(s):

Avoidance Response ◽

Mating Systems ◽

Scent Marking ◽

Scent Mark ◽

Scent Marks ◽

Prairie Voles ◽

Meadow Voles ◽

Terrestrial Mammals ◽

Males And Females ◽

Marking Behaviour

AbstractMost terrestrial mammals deposit scent marks to communicate with conspecifics. We examined the scent marking behaviour of meadow voles and prairie voles, species with different mating systems and social organizations, to determine whether voles scent mark according to the 'targeting' response, the 'avoidance' response, or the 'shotgun' response. The targeting response occurs when the second scent donor deposits more of its scent marks in an area marked by the first scent donor than in an unscented area. The avoidance response occurs when the second scent donor deposits more of its scent marks in an unscented area than in an area marked by the first scent donor. The shotgun response occurs when the second scent donor deposits a similar number of its scent marks in an area containing scent marks of a conspecific and in an area containing no conspecific scent marks. We allowed voles simultaneous access to an arena containing two arms: one of the arms was scented by a conspecific and the other arm was unscented. We recorded the number of marks deposited by the voles in each arm and the amount of time they spent investigating marks deposited previously in the scented arm. Our data provide no support for the avoidance response, but provide support for the shotgun response and the target response. Species and sex differences in the scent marking behaviours of voles when they encounter the scent marks of conspecifics are discussed within the framework that scent marking responses depend on the voles' social organization and mating system, and that these responses may reflect the tactics males and females use to attract mates and compete with same-sex conspecifics.

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