Conflict on the Sex Chromosomes: Cause,Effect, and Complexity

Intralocus sexual conflict and intragenomic conflict both affect sex chromosome evolution and can in extreme cases even cause the complete turnover of sex chromosomes. Additionally, established sex chromosomes often become the focus of heightened conflict. This creates a tangled relationship between sex chromosomes and conflict with respect to cause and effect. To further complicate matters, sexual and intragenomic conflict may exacerbate one another and thereby further fuel sex chromosome change. Different magnitudes and foci of conflict offer potential explanations for lineage-specific variation in sex chromosome evolution and answer long-standing questions as to why some sex chromosomes are remarkably stable, whereas others show rapid rates of evolutionary change.Compared to the autosomes, the unique inheritance pattern of the sex chromosomes is often thought to intensify evolutionary conflict (Rice 1984; Frank 1991; Jaenike 2001). Sex chromosomes are therefore hot spots for two specific types of conflict: intralocus conflict, in which an allele confers different fitness effects depending on the sex in which it is found, and intragenomic conflict, in which selfish genetic elements (SGEs) promote their own transmission at the expense of unlinked regions of the genome. These conflicts act in distinct but complementary ways. Not only do they shape sex chromosome and genome evolution, but in some cases, they also have the power to cause complete turnover of sex chromosomes.Unlike the autosomes, because the sex chromosomes are unevenly transmitted between males and females and are also unevenly distributed between the sexes (Fig. 1), the relative effect of male- and female-specific selection acting on them is unbalanced. The inherent differences in sex-specific selection on the sex chromosomes themselves, and between the sex chromosomes and the autosomes, form the basis of a large and often compelling body of evolutionary theory that predicts the ways that intralocus sexual conflict will arise, play out, and in some cases potentially be resolved. This theory predicts that, under some conditions, the sex chromosomes are hot spots of intralocus sexual conflict (Rice 1984; Albert and Otto 2005; Connallon and Clark 2010), and in some cases alleles that harm one sex more than they benefit the other can still reach high frequencies if they are sex-linked (Rice 1984; Dean et al. 2012). All this theory predicts that although the sex chromosomes generally represent a small proportion of the genome, they should play a disproportionately large role in sexual conflict, sexual dimorphism, and sexual selection. There is substantial empirical evidence supporting at least some of this theory (Dean and Mank 2014).Open in a separate windowFigure 1.Transmission of the sex chromosomes. Females are shown in red, males in blue. In male heterogamety (A), the Y chromosome is passed through the patriline and limited to males. The maternal X chromosome is passed from mother to both sons and daughters, but the paternal X can only be transmitted to daughters. Additionally, the X is present two-thirds of the time in females. In female heterogamety (B), the W chromosome is limited to females and passed solely from mother to daughter. The paternal Z chromosome can be passed from father to both daughters and sons; however, the maternal Z chromosome is only passed to sons. Converse to the X chromosome, the Z chromosome is resident in males two-thirds of the time.

Table 1.

Studies showing a disproportionate role of the sex chromosomes in sexual dimorphism, fitness, or fertility

	Male heterogamety		Female heterogamety
	X chromosome	Y chromosome	Z chromosome	W chromosome
Associations with sexually dimorphic phenotypic traits	Size dimorphism in red deer (Foerster et al. 2007) Sexually antagonistic fitness variation in Drosophila (Gibson et al. 2002; Innocenti and Morrow 2010) Variation in stalk-eyed fly eye span (Wolfenbarger and Wilkinson 2001)	Male coloration in guppies (Winge 1927; Postma et al. 2011) Male mating behavior in sticklebacks (Kitano et al. 2009; although see Natri et al. 2013)	Female mating preference in moths (Iyengar et al. 2002) Female mate choice in flycatchers (Saether et al. 2007) Male plumage traits in flycatchers (Saetre et al. 2003)	Female benefit coloration in cichlids (Roberts et al. 2009)
Associations with reproduction and fertility	Male reproductive genes in mice (Mueller et al. 2008)	Male fertility genes in mammals (Lange et al. 2009) Male fitness in Drosophila (Lemos et al. 2010; Sackton et al. 2011)	Genes related to male reproductive function in silk moth (Arunkumar et al. 2009)	Genes related to female fecundity and fertility in chickens (Moghadam et al. 2012)

Open in a separate windowIn addition to their role in sexual conflict, the sex chromosomes also experience high levels of intragenomic conflict resulting from SGEs that promote their own transmission at the expense of the rest of the genome (Burt and Trivers 2006). Of particular importance are sex-linked segregation distorters, as these generate strong selection favoring genes that suppress their action. Theory predicts that intragenomic conflict should be particularly intense when involving the sex chromosomes (Hurst and Pomiankowski 1991). This is because sex chromosomes can generate antagonistic coevolution between sex-linked segregation distorters and their suppressors (Partridge and Hurst 1998).In addition to shaping the evolutionary properties of existing sex chromosomes, in some situations sexual and intragenomic conflict may also actually catalyze the formation of sex chromosomes (Fisher 1931; Charlesworth and Charlesworth 1980; Rice 1987; Werren and Beukeboom 1998). Conflict may also explain the rate of degradation of the sex-limited Y and W chromosomes (Bachtrog et al. 2011) and turnover of sex chromosomes (Hall 2004; van Doorn and Kirkpatrick 2007, 2010), suggesting that conflict plays a causal role in sex chromosome evolution.There is also growing evidence of a direct relationship between SGEs and sexual conflict involving the sex chromosomes. Many SGEs increase their transmission advantage by targeting sperm, which can reduce male fertility owing to reduced overall sperm production. Lower sperm production can in turn result in reduced siring success during sperm competition (Price and Wedell 2008) and potentially favor polyandry as a female strategy to bias paternity against SGE-carrying males (Wedell 2013). As a consequence, SGEs may also influence the potential for sexual conflict as they can favor increased female mating rates, which increases the potential for conflict between the sexes.Sexual and intragenomic conflict are therefore critical for sex chromosome evolution and, once sex chromosomes are established, can further shape their evolutionary and genomic properties. Disentangling cause and effect is difficult but crucial to understanding the role of sex chromosomes in sexual and intragenomic conflict and vice versa.