Social behavior and aging: A fly model

Brenman-Suttner, Dova B; Yost, Ryley T.; Frame, Ariel K.; Robinson, John Wesley; Moehring, Amanda J.; Simon, Anne F.

doi:10.1111/gbb.12598

Cited by 21 publications

(24 citation statements)

References 281 publications

(583 reference statements)

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“…Thus, lifespan assays confirm that males live significantly shorter than females, consistent with multiple studies on sex‐specific lifespan in Drosophila [25, 26]. Note however that other factors besides sex (such as male‐male aggression) may contribute to differences in longevity between males and females [27]. Longevity patterns are thus consistent with the notion that the repeat‐rich Y chromosome reduces survivorship in the heterogametic sex [3, 4].…”

Section: Resultssupporting

confidence: 85%

Toxic Y chromosome: increased repeat expression and age-associated heterochromatin loss in male Drosophila with a young Y chromosome

Nguyen

Bachtrog

2020

Preprint

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Sex‐specific differences in lifespan are prevalent across the tree of life and influenced by heteromorphic sex chromosomes. In species with XY sex chromosomes, females often outlive males. Males and females can differ in their overall repeat content due to the repetitive Y chromosome, and repeats on the Y might lower survival of the heterogametic sex (toxic Y effect). Here, we take advantage of the well‐assembled young Y chromosome of Drosophila miranda to study the sex‐specific dynamics of chromatin structure and repeat expression during aging in male and female flies. Male D. miranda have about twice as much repetitive DNA compared to females, and live shorter than females. Heterochromatin is crucial for silencing of repetitive elements, yet old D. miranda flies lose H3K9me3 modifications in their pericentromere, with heterochromatin loss being more severe during aging in males than females. Satellite DNA becomes de‐repressed more rapidly in old vs. young male flies relative to females. In contrast to what is observed in D. melanogaster, we find that transposable elements (TEs) are expressed at higher levels in male D. miranda throughout their life. We show that epigenetic silencing via heterochromatin formation is ineffective on the large TE‐ rich neo‐Y chromosome, resulting in up‐regulation of Y‐linked TEs already in young males. This is consistent with an interaction between the age of the Y chromosome and the genomic effects of aging. Our data support growing evidence that “toxic Y chromosomes” can diminish male fitness and a reduction in heterochromatin can contribute to sex‐specific aging.

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Section: Resultssupporting

confidence: 85%

Toxic Y chromosome: increased repeat expression and age-associated heterochromatin loss in male Drosophila with a young Y chromosome

Nguyen

Bachtrog

2020

Preprint

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“…Hence, we wanted to confirm previous findings and validate our loss-of-function mutant. Using a climbing assay to investigate startle-induced activity, we observed age-related reductions in climbing in Cs, as well as in UAS- nlg3/+ flies, as expected [ 2 ], in both males and females ( Figure 3 A–D).…”

Section: Resultssupporting

confidence: 79%

“…An individual’s ability to respond to others relies on the perception of social cues and their subsequent integration in the nervous system [ 1 ]. We are only beginning to understand how the neural circuitry, or the brain’s ability to process signals from others, facilitates this integration and allows for a response to other individuals [ 2 ]. The inability to properly integrate social cues can result in abnormal social interactions, as seen in individuals with autism spectrum disorders [ 3 , 4 ].…”

Section: Introductionmentioning

confidence: 99%

“…Recently, social space has been used as an effective assay to study social interactions with others in a group to identify neural circuitry, underlying mechanisms, and functional changes within the fly brain that modulate these interactions [ 2 ]. Other social behaviors, including courtship, aggression, sociability, and Drosophila Stress Odorant (dSO) avoidance, are also used to examine the underlying mechanisms of social behavior in Drosophila [ 9 , 10 , 11 , 12 , 13 ].…”

Section: Introductionmentioning

confidence: 99%

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Abnormal Social Interactions in a Drosophila Mutant of an Autism Candidate Gene: Neuroligin 3

Yost

Robinson

Baxter

et al. 2020

IJMS

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Social interactions are typically impaired in neuropsychiatric disorders such as autism, for which the genetic underpinnings are very complex. Social interactions can be modeled by analysis of behaviors, including social spacing, sociability, and aggression, in simpler organisms such as Drosophila melanogaster. Here, we examined the effects of mutants of the autism-related gene neuroligin 3 (nlg3) on fly social and non-social behaviors. Startled-induced negative geotaxis is affected by a loss of function nlg3 mutation. Social space and aggression are also altered in a sex- and social-experience-specific manner in nlg3 mutant flies. In light of the conserved roles that neuroligins play in social behavior, our results offer insight into the regulation of social behavior in other organisms, including humans.

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“…Rounding out the issue is a comprehensive review by Brenman‐Suttner et al, who explore the complex interactions between genetics, physiology, and time that orchestrate age‐related changes in social behaviors. Using D. melanogaster as a model system, the authors discuss a broad range of sex‐dependent behaviors, such as courtship, aggression, or egg‐laying conditioning, as well as those expressed by both males and females, like social spacing and circadian rhythm entrainment.…”

mentioning

confidence: 99%

Sex differences in 3D: Differentiation, dimorphism, or dependence?

Shansky

2020

Genes Brain and Behavior

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Across neuroscience research, the expression "sex differences" has become a catchall term for any phenomenon that we might observe in one sex but not the other-or even a phenomenon observed in both sexes subgroups of males that exhibit distinct patterns of gene expression in the ventral tegmental area (VTA). Intriguingly, these divisions were most tightly predictive of the behavior of the male's female partner, even more so than the behavior of the male himself.Of course, not all social behavior is related to mating, and as three of this issue's research articles demonstrate, genetic modifications can produce sex-dependent effects in a wide range of social outcomes.First, haploinsufficiency of the CACNA1C gene resulted in increased rough-and-tumble play in adolescent female rats, but not males. 6 In contrast, heterozygous males, but not females exhibited altered prosocial ultrasonic vocalizations (USVs). Because CACNA1C is implicated with several mental illnesses that differentially affect men and women (eg, major depressive disorder and schizophrenia), these data may shed light onto a potential mechanism of sex-dependent pathophysiologies. USVs also play a key role in pup-mother communication, and Nolan et al 7 find that male and female Fmr1 (a gene linked to fragile X syndrome) knockout or heterozygous mice exhibit discrete patterns of altered vocalizations compared with their wildtype, same-sex littermates. Finally, in a mutant mouse model of amyotrophic lateral sclerosis (ALS), Kreilaus et al 8 report that prior to the onset of expected motor deficits, mutant males, but not females exhibited reduced sociability, pointing to a potential sex-specific early marker of the disease.Rounding out the issue is a comprehensive review by Brenman-Suttner et al, 9 who explore the complex interactions between genetics, physiology, and time that orchestrate age-related changes in social behaviors. Using D. melanogaster as a model system, the authors discuss a broad range of sex-dependent behaviors, such as courtship, aggression, or egg-laying conditioning, as well as those expressed by both males and females, like social spacing and circadian rhythm entrainment.Together with those in the upcoming companion Special Issue, the articles here comprise a rich sampling of the many ways in which biological sex can contribute to behavioral outcomes in a host of species ranging from fruit flies to humans. The diverse perspectives offered in both issues should serve as food for thought to GB2's readers as they attempt to consider sex as a biological variable in their own research.

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Social behavior and aging: A fly model

Cited by 21 publications

References 281 publications

Toxic Y chromosome: increased repeat expression and age-associated heterochromatin loss in male Drosophila with a young Y chromosome

Toxic Y chromosome: increased repeat expression and age-associated heterochromatin loss in male Drosophila with a young Y chromosome

Abnormal Social Interactions in a Drosophila Mutant of an Autism Candidate Gene: Neuroligin 3

Sex differences in 3D: Differentiation, dimorphism, or dependence?

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