Sexually antagonistic epigenetic marks that canalize sexually dimorphic development

Abstract

The sexes share the same autosomal genomes yet sexual dimorphism is common due to sex-specific gene expression. When present, XX and XY karyotypes trigger alternate regulatory cascades that determine sex-specific gene expression profiles. In mammals, secretion of testosterone (T) by the testes during fetal development is the master switch influencing the gene expression pathways (male vs. female) that will be followed, but many genes have sex-specific expression prior to T secretion. Environmental factors, like endocrine disruptors and mimics, can interfere with sexual development. However, sex-specific ontogeny can be canalized by the production of epigenetic marks (epimarks) generated during early ontogeny that increase sensitivity of XY embryos to T and decrease sensitivity of XX embryos. Here we integrate and synthesize the evidence indicating that canalizing epimarks are produced during early ontogeny. We will also describe the evidence that such epimarks sometimes carry over across generations and produce mosaicism in which some traits are discordant with the gonad. Such carryover epimarks are sexually antagonistic because they benefit the individual in which they were formed (via canalization) but harm opposite-sex offspring when they fail to erase across generations and produce gonad-trait discordances. SA-epimarks have the potential to: i) magnify phenotypic variation for many sexually selected traits, ii) generate overlap along many dimensions of the masculinity/femininity spectrum, and iii) influence medically important gonad-trait discordances like cryptorchidism, hypospadias, and idiopathic hirsutism.

A Genomic Imprinting Model of Termite Caste Determination: Not Genetic but Epigenetic Inheritance Influences Offspring Caste Fate

“…The basic idea of our genomic imprinting model, that maternal and paternal imprinting act on the offspring's sexual development in different directions, is in accordance with the sexual antagonism theory of genomic imprinting (Day and Bonduriansky 2004;Rice et al 2016). An example of the sexual antagonism of parental imprinting can be seen in the genomic imprinting sex determination mechanism in some haplodiploid insects (Dobson and Tanouye 1998;Gadagkar 2000).…”

“…Sex-specific epimarks would contribute to king-and queen-specific gene expression and thus increase reproductive output. Incomplete erasure of these epimarks in the germ line would lead to transgenerational carryover of the sexspecific epimarks, which could act antagonistically in the offspring influencing their sexual development (Rice et al 2016).…”

“…We developed a novel genomic imprinting model for caste predisposition in R. speratus and other Reticulitermes termites that closely matches empirical data from both lab and field studies. Sex-specific epigenetic marks (hereafter called "epimarks") of the parents can influence the phenotype of the offspring through incomplete erasure of the epimarks in the germ line (Rice et al 2016). Our genomic imprinting model assumes that heritable epimarks (i.e., imprinting) in-crease in strength with the sexual maturation of the parents (fig.…”

Epigenetics in ecology and evolution: what we know and what we need to know

“…One striking idea about the phenotypic effects of epigenetic variation that is developed by Rice et al . () and that requires further empirical testing is that occasional failure to erase epigenetic marks that canalize sex‐specific development can lead to gonad–trait mismatches in a subsequent generation. Such mismatches might, for instance, explain overlap in the masculinity/femininity phenotype spectrum.…”

The De-Scent of Sexuality: Should We Smell a Rat?

“…Before discussing the evidence for a potential link between the TRPC2 gene and SSSB in primates, and indeed all mammals, it is essential to clarify that any such link ought not to be interpreted as promoting a single "gay gene" theory of homosexuality (i.e., same-sex sexual partner preferences) and SSSB. Firstly, there is already a growing body of evidence for an epigenetic and polygenic underpinning of homosexuality and SSSB (Ratnu, Emami, & Bredy, 2017;Rice, Friberg, & Gavrilets, 2016;Sanders et al, 2017). Secondly, since it is the absence of functional TRPC2 that appears to facilitate heightened SSSB, it seems that the gene is not itself driving SSSB, but instead that it is perhaps underpinning same-sex aversion, which is inversely related but not inherently antithetical to SSSB.…”