Genomic responses to the socio-sexual environment in male <i>Drosophila melanogaster</i> exposed to conspecific rivals

Mohorianu, Irina; Bretman, Amanda; Smith, Damian T.; Fowler, Emily K.; Dalmay, Tamás; Chapman, Tracey

doi:10.1261/rna.059246.116

Cited by 51 publications

(71 citation statements)

References 71 publications

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“…Additionally, the expression of dnc is altered by exposure to a rival male [23]. We used a dnc knockout, and rut and amn knockdown driven in the whole brain by elav-Gal4, to investigate the importance of ASM in extended mating duration (Supplementary figure S1).…”

Section: Assessment Of Genetic Controlmentioning

confidence: 99%

Flexible memory controls sperm competition responses in male Drosophila melanogaster

Rouse¹,

Watkinson²,

Bretman³

2018

Proc. R. Soc. B.

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Article:Rouse, J orcid.org/0000-0001-8457-4623, Watkinson, K and Bretman, A orcid.org/0000-0002- 4421-3337 (2018) AbstractMales of many species use social cues to predict sperm competition and tailor their reproductive strategies, such as ejaculate or behavioural investment, accordingly. Whilst these plastic strategies are widespread, the underlying mechanisms remain largely unknown. Plastic behaviour requires individuals to learn and memorise cues associated with environmental change before using this experience to modify behaviour. Drosophila melanogaster respond to an increase in sperm competition threat by extending mating duration after exposure to a rival male. This behaviour shows lag times between environmental change and behavioural response suggestive of acquisition and loss of memory. Considering olfaction is important for a male's ability to assess the sperm competition environment, we hypothesised that an olfactory learning and memory pathway may play a key role in controlling this plastic behaviour. We assessed the role of genes and brain structures known to be involved in learning and memory. We show that sperm competition responses depend on anaesthesia sensitive memory, specifically the genes rut and amn. We also show that the lobes of the mushroom bodies are integral to the control of plastic mating behaviour. These results reveal the genetic and neural properties required for reacting to changes in the sperm competition environment.

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Section: Assessment Of Genetic Controlmentioning

confidence: 99%

Flexible memory controls sperm competition responses in male Drosophila melanogaster

Rouse¹,

Watkinson²,

Bretman³

2018

Proc. R. Soc. B.

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“…The effects of same-sex social contact on male behaviour, ejaculate and gene expression can be observed on a timescale of hours to a few days (12, 23, 24). However, we observed no effect on the microbiome of young flies, but rather only at older ages, in line with declines in functions such as mating success (37) and climbing ability (4).…”

Section: Resultsmentioning

confidence: 99%

“…However, there is a great deal of interaction between the microbiome and host immune pathways, hormones and neurotransmitters known as the ‘microbiota-gut-brain axis’ (11). Therefore host social environments that impact stress and immune responses (1, 2, 12) could indirectly alter the microbiome. This could have profound consequences for host health given the microbiomes influence on development and behaviour (13), susceptibility to pathogens (14), ageing (15, 16) and fitness trade-offs (17).…”

Section: Introductionmentioning

confidence: 99%

“…Larvae gain gut microbes through ingestion of their egg casing and from their food, and this environmental replenishment continues during adulthood (30), so extrinsic effects of the social environment are likely. Additionally, fly gene expression is socially sensitive, including immune, stress and lifespan related genes (1, 12), so there is potential for intrinsic effects of social environments acting through the microbiota-gut-brain axis.…”

Section: Introductionmentioning

confidence: 99%

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Social environment drives sex and age-specific variation in Drosophila melanogaster microbiome composition and predicted function

Leech

McDowall

Hopkins

et al. 2020

Preprint

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Social environments influence multiple traits of individuals including immunity, stress and ageing, often in sex-specific ways. The composition of the microbiome (the assemblage of symbiotic microorganisms within a host) is determined by environmental factors and the host’s immune, endocrine and neural systems. The social environment could alter host microbiomes extrinsically by affecting transmission between individuals, likely promoting homogeneity in the microbiome of social partners. Alternatively, intrinsic effects arising from interactions between the microbiome and host physiology (the microbiota-gut-brain axis) could translate social stress into dysbiotic microbiomes, with consequences for host health. We investigated how manipulating social environments during larval and adult life-stages altered the microbiome composition of Drosophila melanogaster fruit flies. We used social contexts that particularly alter the development and lifespan of males, predicting that any intrinsic social effects on the microbiome would therefore be sex-specific. The presence of adult males during the larval stage significantly altered the microbiome of pupae of both sexes. In adults, same-sex grouping increased bacterial diversity in both sexes. Importantly, the microbiome community structure of males was more sensitive to social contact at older ages, an effect partially mitigated by housing focal males with young rather than co-aged groups. Functional analyses suggest that these microbiome changes impact ageing and immune responses. This is consistent with the hypothesis that the substantial effects of the social environment on individual health are mediated through intrinsic effects on the microbiome, and provides a model for understanding the mechanistic basis of the microbiota-gut-brain axis.Significance statementThe social environment has pervasive, multifaceted effects on individual health and fitness. If a host’s microbiome is sensitive to the social environment then it could be an important mediator of social effects, as the reciprocal relationships between hosts and their microbiomes have substantial implications for host health. Using a Drosophila melanogaster fruit fly model we show that the fly microbiome is sensitive to the social environment in a sex, age and life-stage dependent manner. In particular, older adult male microbiome communities are altered by same-sex social contact, but this depends on the age of the social partners. These changes have functional effects on fly immunity and lifespan, evidence that indeed this is an influential mediator of social effects on health.

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“…Yet phenotypic studies that have manipulated social environments to manipulate sperm competition have revealed considerable plasticity for seminal fluid expression according to the presence/absence of rival males (e.g. Harris & Moore, 2005; Fedorka et al , 2011; Ramm et al , 2015; Mohorianu et al , 2017; Sloan et al , 2018). Here, we argue that variation in social environment and thus the extent of GEIs may arise from heterogeneity in social conditions and could maintain genetic variation in seminal fluid expression.…”

Section: Discussionmentioning

confidence: 99%

Genotype-by-environment interactions for seminal fluid expression and sperm competitive ability

Patlar

Ramm

2019

Preprint

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Sperm competition commonly occurs whenever females mate multiply, leading to variation in male paternity success. This can be due to variation in the various traits that might affect sperm competitive ability, which itself depends on both genetic and environmental factors, as well as on genotype‐by‐environment interactions (GEI). Seminal fluid is a major component of the male ejaculate that is often expected to mediate sperm competition, where different genotypes can differ in their seminal fluid expression as a response to different levels of sperm competition (i.e. exhibit GEI). We therefore here focussed on testing for GEI in expression of two recently identified seminal fluid transcripts, suckless‐1 and suckless‐2, which potentially modulate sperm competitive ability in the simultaneously hermaphroditic flatworm Macrostomum lignano via their effects on manipulating post‐mating partner behaviour and ultimately the fate of transferred ejaculates. In addition, we sought to test for GEI in sperm competitive ability in a standardized sperm competition (P1 and P2) assay, to investigate the relationship between natural variation in the expression of these seminal fluid transcripts generated through GEI and relative paternity success. We found GEI for the expression level of suckless‐1 and suckless‐2, as well as for sperm competitive ability. Moreover, we found a positive relation between the expression of suckless‐1 and relative paternity success (P1). This suggests that natural variation in the expression of this seminal fluid transcript indeed can influence sperm competition outcomes in M. lignano.

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Genomic responses to the socio-sexual environment in male Drosophila melanogaster exposed to conspecific rivals

Cited by 51 publications

References 71 publications

Flexible memory controls sperm competition responses in male Drosophila melanogaster

Flexible memory controls sperm competition responses in male Drosophila melanogaster

Social environment drives sex and age-specific variation in Drosophila melanogaster microbiome composition and predicted function

Genotype-by-environment interactions for seminal fluid expression and sperm competitive ability

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