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Genome-Wide Responses of Female Fruit Flies Subjected to Divergent Mating Regimes.

ABSTRACT: Elevated rates of mating and reproduction cause decreased female survival and lifetime reproductive success across a wide range of taxa from flies to humans. These costs are fundamentally important to the evolution of life histories. Here we investigate the potential mechanistic basis of this classic life history component. We conducted 4 independent replicated experiments in which female Drosophila melanogaster were subjected to 'high' and 'low' mating regimes, resulting in highly significant differences in lifespan. We sampled females for transcriptomic analysis at day 10 of life, before the visible onset of ageing, and used Tiling expression arrays to detect differential gene expression in two body parts (abdomen versus head+thorax). The divergent mating regimes were associated with significant differential expression in a network of genes showing evidence for interactions with ecdysone receptor. Preliminary experimental manipulation of two genes in that network with roles in post-transcriptional modification (CG11486, eyegone) tended to enhance sensitivity to mating costs. However, the subtle nature of those effects suggests substantial functional redundancy or parallelism in this gene network, which could buffer females against excessive responses. There was also evidence for differential expression in genes involved in germline maintenance, cell proliferation and in gustation / odorant reception. Interestingly, we detected differential expression in three specific genes (EcR, keap1, lbk1) and one class of genes (gustation / odorant receptors) with previously reported roles in determining lifespan. Our results suggest that high and low mating regimes that lead to divergence in lifespan are associated with changes in the expression of genes such as reproductive hormones, that influence resource allocation to the germ line, and that may modify post-translational gene expression. This predicts that the correct signalling of nutrient levels to the reproductive system is important for maintaining organismal integrity.

SUBMITTER: Gerrard DT

PROVIDER: S-EPMC3694895 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Genome-Wide Responses of Female Fruit Flies Subjected to Divergent Mating Regimes.

Gerrard Dave T DT Fricke Claudia C Edward Dominic A DA Edwards Dylan R DR Chapman Tracey T

PloS one 20130627 6

Elevated rates of mating and reproduction cause decreased female survival and lifetime reproductive success across a wide range of taxa from flies to humans. These costs are fundamentally important to the evolution of life histories. Here we investigate the potential mechanistic basis of this classic life history component. We conducted 4 independent replicated experiments in which female Drosophila melanogaster were subjected to 'high' and 'low' mating regimes, resulting in highly significant d ...[more]

PMID: 23826372

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Project description:Many animals use acoustic signals to attract a potential mating partner. In fruit flies (Drosophila melanogaster), the courtship pulse song has a species-specific interpulse interval (IPI) that activates mating. Although a series of auditory neurons in the fly brain exhibit different tuning patterns to IPIs, it is unclear how the response of each neuron is tuned. Here, we studied the neural circuitry regulating the activity of antennal mechanosensory and motor center (AMMC)-B1 neurons, key secondary auditory neurons in the excitatory neural pathway that relay song information. By performing Ca2+ imaging in female flies, we found that the IPI selectivity observed in AMMC-B1 neurons differs from that of upstream auditory sensory neurons [Johnston's organ (JO)-B]. Selective knock-down of a GABAA receptor subunit in AMMC-B1 neurons increased their response to short IPIs, suggesting that GABA suppresses AMMC-B1 activity at these IPIs. Connection mapping identified two GABAergic local interneurons that synapse with AMMC-B1 and JO-B. Ca2+ imaging combined with neuronal silencing revealed that these local interneurons, AMMC-LN and AMMC-B2, shape the response pattern of AMMC-B1 neurons at a 15 ms IPI. Neuronal silencing studies further suggested that both GABAergic local interneurons suppress the behavioral response to artificial pulse songs in flies, particularly those with a 15 ms IPI. Altogether, we identified a circuit containing two GABAergic local interneurons that affects the temporal tuning of AMMC-B1 neurons in the song relay pathway and the behavioral response to the courtship song. Our findings suggest that feedforward inhibitory pathways adjust the behavioral response to courtship pulse songs in female flies.SIGNIFICANCE STATEMENT To understand how the brain detects time intervals between sound elements, we studied the neural pathway that relays species-specific courtship song information in female Drosophila melanogaster We demonstrate that the signal transmission from auditory sensory neurons to key secondary auditory neurons antennal mechanosensory and motor center (AMMC)-B1 is the first-step to generate time interval selectivity of neurons in the song relay pathway. Two GABAergic local interneurons are suggested to shape the interval selectivity of AMMC-B1 neurons by receiving auditory inputs and in turn providing feedforward inhibition onto AMMC-B1 neurons. Furthermore, these GABAergic local interneurons suppress the song response behavior in an interval-dependent manner. Our results provide new insights into the neural circuit basis to adjust neuronal and behavioral responses to a species-specific communication sound.

Project description:BACKGROUND: Interlocus conflict predicts (a) evolution of traits, beneficial to males but detrimental to females and (b) evolution of aging and life-span under the influence of the cost of bearing these traits. However, there are very few empirical investigations shedding light on these predictions. Those that do address these issues, mostly reported response of male reproductive traits or the lack of it and do not address the life-history consequence of such evolution. Here, we test both the above mentioned predictions using experimental evolution on replicate populations of Drosophila melanogaster. We present responses observed after >45 generations of altered levels of interlocus conflict (generated by varying the operational sex ratio). RESULTS: Males from the male biased (high conflict, M-regime) regime evolved higher spontaneous locomotor activity and courtship frequency. Females exposed to these males were found to have higher mortality rate. Males from the female biased regime (low conflict, F-regime) did not evolve altered courtship frequency and activity. However, progeny production of females continuously exposed to F-males was significantly higher than the progeny production of females exposed to M-males indicating that the F-males are relatively benign towards their mates. We found that males from male biased regime lived shorter compared to males from the female biased regime. CONCLUSION: F-males (evolving under lower levels of sexual conflict) evolved decreased mate harming ability indicating the cost of maintenance of the suit of traits that cause mate-harm. The M-males (evolving under higher levels sexual conflict) caused higher female mortality indicating that they had evolved increased mate harming ability, possibly as a by product of increased reproduction related activity. There was a correlated evolution of life-history of the M and F-males. M-regime males lived shorter compared to the males from F-regime, possibly due to the cost of investing more in reproductive traits. In combination, these results suggest that male reproductive traits and life-history traits can evolve in response to the altered levels of interlocus sexual conflict.

Dataset Information

Genome-Wide Responses of Female Fruit Flies Subjected to Divergent Mating Regimes.

Publications

Genome-Wide Responses of Female Fruit Flies Subjected to Divergent Mating Regimes.

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