Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Review
. 2012;53(3-4):253-69.
doi: 10.1093/ilar.53.3-4.253.

Sexually selected traits: a fundamental framework for studies on behavioral epigenetics

Eldin Jašarević  1 , David C Geary, Cheryl S Rosenfeld
Affiliations
Review

Sexually selected traits: a fundamental framework for studies on behavioral epigenetics

Eldin Jašarević et al. ILAR J. 2012.

Abstract

Emerging evidence suggests that epigenetic-based mechanisms contribute to various aspects of sex differences in brain and behavior. The major obstacle in establishing and fully understanding this linkage is identifying the traits that are most susceptible to epigenetic modification. We have proposed that sexual selection provides a conceptual framework for identifying such traits. These are traits involved in intrasexual competition for mates and intersexual choice of mating partners and generally entail a combination of male-male competition and female choice. These behaviors are programmed during early embryonic and postnatal development, particularly during the transition from the juvenile to adult periods, by exposure of the brain to steroid hormones, including estradiol and testosterone. We evaluate the evidence that endocrine-disrupting compounds, including bisphenol A, can interfere with the vital epigenetic and gene expression pathways and with the elaboration of sexually selected traits with epigenetic mechanisms presumably governing the expression of these traits. Finally, we review the evidence to suggest that these steroid hormones can induce a variety of epigenetic changes in the brain, including the extent of DNA methylation, histone protein alterations, and even alterations of noncoding RNA, and that many of the changes differ between males and females. Although much previous attention has focused on primary sex differences in reproductive behaviors, such as male mounting and female lordosis, we outline why secondary sex differences related to competition and mate choice might also trace their origins back to steroid-induced epigenetic programming in disparate regions of the brain.

Keywords: DNA methylation; histone proteins; neurodevelopment; sex dimorphism; steroid hormones.

PubMed Disclaimer

Figures

Figure 1
Figure 1
The inflated gular pouch of the great and magnificent frigatebirds (Fregata minor and Fregata magnificens, respectively) is a sexually selected trait and likely to be a direct indicator of the male's health to a prospective female partner. Photo taken by Cheryl S. Rosenfeld on North Seymour Island in the Galápagos Archipelago.
Figure 2
Figure 2
Example of skypointing with beak pointing upward and wings spread out by male blue-footed booby (Sula nebouxii) on right side of the photo, as female on left side observes this behavior, which is part of an elaborate courtship behavioral pattern that has evolved in this species. Photo taken by Cheryl S. Rosenfeld on North Seymour Island in the Galápagos Archipelago.
Figure 3
Figure 3
Picture of bighorn sheep ram (Ovis canadensis ). Two males compete by kneeling in front of each other and then trying to maneuver the points of their horns under the body of their competitor. Photo taken by Cheryl S. Rosenfeld in Yellowstone National Park, Wyoming.
Figure 4
Figure 4
Parental behaviors of California mice (Peromyscus californicus). While the female nurses the pups, the male engages in anogenital licking and grooming of them. Photo taken by Cheryl S. Rosenfeld.
Figure 5
Figure 5
Working hypothetical model of how endocrine disrupting compounds (EDC) such as bisphenol A (BPA) might disrupt sexually selected traits. Steroid hormones, including estrogen and testosterone, can underpin various epigenetic changes, including changes in DNA methylation patterns and histone protein modification. These epigenetic changes can lead to sex-dependent alteration in the neural architecture. Consequently, these epigenetic and morphologic differences underpin sexual differentiation of the brain and synchronization of adult behaviors. Given the sensitivity of these traits to developmental steroid hormone concentrations, exposure to EDCs that disrupt hormone signaling during these critical life history stages has the potential to disrupt the full expression of sexually selected traits. These traits thus might be employed as biomarkers for endocrine disruption and serve as the framework for experiments designed to test the effects of EDCs on brain, cognitive, and behavioral development in males and females.
Figure 6
Figure 6
Effects of early developmental exposure to bisphenol A (BPA) and ethinyl estradiol (EE) on spatial learning and memory of adult male and female deer mice (Peromyscus maniculatus) in the Barnes maze. Latency (i.e., time required to escape the maze) across days of training for males (A) and females (C) (Mean ± SEM). Number of escape errors across days of training for males (B) and females (D) (Mean ± SEM, *p < 0.01). Adapted from Jašarević and colleagues (2011).
Figure 7
Figure 7
Effects of early developmental exposure to bisphenol A (BPA) and ethinyl estradiol on spatial search strategy of adult male and female deer mice (Peromyscus maniculatus) in the Barnes maze. (A) Examples of composite images from single animals tracked from entry to escape illustrating different spatial strategies used to exit the maze. (B) Distribution of different spatial strategies according to sex, diet exposure, and day of training. During the initial training period (day 1), most animals navigated by using a random strategy (black), followed by a serial search strategy (white). The most efficient spatial search strategy (gray) emerged when the animals began to use direction and position intra-maze cues. By day 3 of training, control males used more efficient strategies than control females and ethinyl estradiol– and BPA-exposed males, who in turn did not differ on any day (p < 0.0002). Ethinyl estradiol–exposed females used more efficient strategies than control and BPA-exposed females on all days except day 2. Adapted from Jašarević and colleagues (2011).
Figure 8
Figure 8
Female choice of control versus bisphenol A (BPA)–exposed males. Control and BPA-exposed females exhibited longer duration of nose-to-nose contact (Mean ± SEM) with control males than with BPA-exposed males. *p < 0.05. Adapted from Jašarević and colleagues (2011).
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Adkins-Regan E. 2005. Hormones and Animal Social Behavior. Princeton NJ: Princeton University Press
    1. Alter MD, Rubin DB, Ramsey K, Halpern R, Stephan DA, Abbott LF, Hen R. 2008. Variation in the large-scale organization of gene expression levels in the hippocampus relates to stable epigenetic variability in behavior. PLoS One 3:e3344. - PMC - PubMed
    1. Amaral PP, Dinger ME, Mercer TR, Mattick JS. 2008. The eukaryotic genome as an RNA machine. Science 319:1787–1789. - PubMed
    1. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY. 1999. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 23:185–188. - PubMed
    1. Amundsen T. 2000. Why are female birds ornamented? Trends Ecol Evol 15:149–155. - PubMed

Publication types