Modular Genetic Control of Sexually Dimorphic Behaviors

Xu, Xiaohong; Coats, Jennifer K.; Yang, Cindy F.; Wang, Amy; Ahmed, Osama M.; Alvarado, Maricruz; Izumi, Tetsuro; Shah, Nirao M.

doi:10.1016/j.cell.2011.12.018

Cited by 243 publications

(284 citation statements)

References 125 publications

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“…c) Relationship between average gene expression level and differential expression between species. In both b and c , genes that have been associated with parental care in previous studies (by physiological/pharmacological studies or induced mutations) 64–66 are labelled; the gene is also boxed if located inside parental behaviour QTLs identified in this study.…”

Section: Extended Datamentioning

confidence: 99%

The genetic basis of parental care evolution in monogamous mice

Bendesky

Kwon

Lassance

et al. 2017

Nature

222

202

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Summary Parental care is essential for the survival of mammals, yet the mechanisms underlying its evolution remain largely unknown. Here we show that two sister species of mice, Peromyscus polionotus and P. maniculatus, have large and heritable differences in parental behaviour. Using quantitative genetics, we identify 12 genomic regions that affect parental care, eight of which have sex-specific effects, suggesting that parental care can evolve independently in males and females. Furthermore, some regions affect parental care broadly, whereas others affect specific behaviours, such as nest building. Of the genes linked to differences in nest-building behaviour, vasopressin is differentially expressed in the hypothalamus of the two species, with increased levels associated with less nest building. Using pharmacology in Peromyscus and chemogenetics in Mus, we show that vasopressin inhibits nest building but not other parental behaviours. Together, our results indicate that variation in an ancient neuropeptide contributes to interspecific differences in parental care.

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Section: Extended Datamentioning

confidence: 99%

The genetic basis of parental care evolution in monogamous mice

Bendesky

Kwon

Lassance

et al. 2017

Nature

222

202

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“…Notably, this masculinization of the number of aromatase-expressing neurons is accompanied by a masculinization of aggression behaviour in females even in the absence of adult supplementation of testosterone. Numerous, novel sex differences in gene expression patterns within the MeA, mPOA, VMH and BNST have been identified [10]. Using genome-wide expression profiling in conjunction with in situ hybridization, we discovered that the regulation of sexually dimorphic gene expression patterns is complex as many individual genes are upregulated in different brain regions in the two sexes [10].…”

Section: (B) Sex Differences In Gene Expressionmentioning

confidence: 99%

“…As discussed above, these receptors can regulate gene expression, and many hormone-dependent sex differences in gene expression have been identified, including in the sex hormone receptors themselves and the enzyme aromatase that converts testosterone into 17b-oestradiol [10][11][12][13][14][15][16][17][18][36][37]40]. For example, we have used genetic strategies to visualize the expression pattern of aromatase in the brain and discovered that it is expressed in a few discrete areas, including the posterodorsal MeA (MeApd) and the posteromedial part of medial division of the BNST (BNSTmpm).…”

Section: (B) Sex Differences In Gene Expressionmentioning

confidence: 99%

“…The MeA, VMH, BNST and mPOA exhibit sex differences such that the number of neurons or innervation within these regions are different in males and females [10,[36][37]40,[99][100][101], and with few exceptions, subsets of adult neurons within these regions express one or more sex hormone receptors [10,[36][37]40,[102][103][104]. As discussed above, these receptors can regulate gene expression, and many hormone-dependent sex differences in gene expression have been identified, including in the sex hormone receptors themselves and the enzyme aromatase that converts testosterone into 17b-oestradiol [10][11][12][13][14][15][16][17][18][36][37]40].…”

Section: (B) Sex Differences In Gene Expressionmentioning

confidence: 99%

“…With traditional approaches, it is not possible to prospectively identify or manipulate the relevant subpopulations within the BNST that control sex-typical social behaviours. Hormone-dependent gene expression patterns define specific pools of neurons in the BNST as well as other heterogeneous brain regions that control sex-typical social behaviours [10,[36][37][38][39][40]. The use of genetic strategies to selectively study and manipulate such molecularly defined neuronal subpopulations within the BNST and elsewhere will be essential in the attempt to untangle and understand the neural circuits underlying sexually dimorphic behaviour.…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Genetic dissection of neural circuits underlying sexually dimorphic social behaviours

Bayless

Shah²

2016

Phil. Trans. R. Soc. B

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The unique hormonal, genetic and epigenetic environments of males and females during development and adulthood shape the neural circuitry of the brain. These differences in neural circuitry result in sex-typical displays of social behaviours such as mating and aggression. Like other neural circuits, those underlying sex-typical social behaviours weave through complex brain regions that control a variety of diverse behaviours. For this reason, the functional dissection of neural circuits underlying sex-typical social behaviours has proved to be difficult. However, molecularly discrete neuronal subpopulations can be identified in the heterogeneous brain regions that control sex-typical social behaviours. In addition, the actions of oestrogens and androgens produce sex differences in gene expression within these brain regions, thereby highlighting the neuronal subpopulations most likely to control sexually dimorphic social behaviours. These conditions permit the implementation of innovative genetic approaches that, in mammals, are most highly advanced in the laboratory mouse. Such approaches have greatly advanced our understanding of the functional significance of sexually dimorphic neural circuits in the brain. In this review, we discuss the neural circuitry of sex-typical social behaviours in mice while highlighting the genetic technical innovations that have advanced the field.

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Clinical Advances in Sex- and Gender-Informed Medicine to Improve the Health of All

et al. 2020

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IMPORTANCE Biological sex and sociocultural gender represent major sources of diversity among patients, and recent research has shown the association of sex and gender with health. A growing body of literature describes widespread associations of sex and gender with cells, organs, and the manner in which individual patients interact with health care systems. Sex-and gender-informed medicine is a young paradigm of clinical practice and medical research founded on this literature that considers the association of sex and gender with each element of the disease process from risk, to presentation, to response to therapy. OBSERVATIONS Characteristics that underlie sex and gender involve both endogenous and exogenous factors that change throughout the life course. This review details clinical examples with broad applicability that highlight sex and gender differences in the key domains of genetics, epigenomic modifiers, hormonal milieu, immune function, neurocognitive aging process, vascular health, response to therapeutics, and interaction with health care systems. These domains interact with one another in multidimensional associations, contributing to the diversity of the sex and gender spectra. Novel research has identified differences of clinical relevance with the potential to improve care for all patients.CONCLUSIONS AND RELEVANCE Clinicians should consider incorporating sex and gender in their decision-making to practice precision medicine that integrates fundamental components of patient individuality. Recognizing the biological and environmental factors that affect the disease course is imperative to optimizing care for each patient. Research highlights the myriad ways sex and gender play a role in health and disease. However, these clinically relevant insights have yet to be systematically incorporated into care. The framework described in this review serves as a guide to help clinicians consider sex and gender as they practice precision medicine.

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Modular Genetic Control of Sexually Dimorphic Behaviors

Cited by 243 publications

References 125 publications

The genetic basis of parental care evolution in monogamous mice

The genetic basis of parental care evolution in monogamous mice

Genetic dissection of neural circuits underlying sexually dimorphic social behaviours

Clinical Advances in Sex- and Gender-Informed Medicine to Improve the Health of All

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