Sex Determination, Sex Ratios and Genetic Conflict

Genetic mechanisms of sex determination are unexpectedly diverse and change rapidly during evolution. We review the role of genetic conflict as the driving force behind this diversity and turnover. Genetic conflict occurs when different components of a genetic system are subject to selection in opposite directions. Conflict may occur between genomes (including paternal-maternal and parentalzygotic conflicts) or within genomes (between cytoplasmic and nuclear genes or sex chromosomes and autosomes). The sex-determining system consists of parental sex-ratio genes, parental-effect sex determiners, and zygotic sex determiners, which are subject to different selection pressures because of differences in their modes of inheritance and expression. Genetic conflict theory is used to explain the evolution of several sex-determining mechanisms, including sex chromosome drive, cytoplasmic sex-ratio distortion, and cytoplasmic male sterility in plants. Although still limited, there is growing evidence that genetic conflict could be important in the evolution of sex-determining mechanisms. PERSPECTIVES AND OVERVIEW Sex-determining mechanisms in plants and animals are remarkably diverse. A brief synopsis illustrates the point. In hermaphroditic species, both male (microgamete) and female (macrogamete) function reside within the same 233 0066-4162/98/1120-0233$08.00 P1: PSA/spd P2: ARK/ary QC: ARK October 16, 1998 18:53 Annual Reviews AR067-09 234 WERREN & BEUKEBOOM individual, whereas dioecious (or gonochoristic) species have separate sexes. Within these broad categories there is further diversity in the phenotypic and genetic mechanisms of sex determination. In dioecious species, various mechanisms exist, including haplodiploidy (males derived from haploid eggs, females from diploid eggs), paternal genome loss (sex determined by loss of paternal chromosomes after fertilization), male heterogamety (males with heteromorphic XY sex chromosomes and females with homomorphic XX), female heterogamety (ZW females and ZZ males), polygenic sex determination, environmental sex determination, and a variety of other mechanisms (reviewed in 17, 175). Sex determination can even differ markedly within a species and between closely related species. For example, platyfish (Xiphophorus maculatus) can have either male heterogamety or female heterogamety (104). In addition, mechanisms that appear to be the same can differ markedly in the underlying genetics. For example, male heterogametic systems can be based on dominant male determiners on the Y (e.g. in mammals) or on a genic balance between factors on the X and autosomes (e.g. in Drosophila). Molecular studies have shown that genes involved in primary sex determination evolve rapidly (48, 111, 166, 169, 170, 176) and that sex-determining genes in one species may not be involved in sex determination in related species (67, 100). In this diversity lies a quandary. Although one would assume that such a basic aspect of development as sex determination would be highly stable in evolution, the opposite is the case. This observation leads to two important evolutionary questions: “Why are sex-determining mechanisms so diverse, and how do sexdetermining mechanisms change, i.e. how do transitions occur from one sexdetermining mechanism to another?” Presumably, sex-determining systems change when some factor (or factors) destabilizes an existing sex-determining mechanism, leading to the evolution of a new mechanism. Therefore, the focus should be on factors that potentially destabilize sex-determining mechanisms and whether some features of sex determination make it inherently unstable over evolutionary time. In this review, we consider the role of genetic conflict in the evolution of sexdetermining systems. Genetic conflict occurs when different genetic elements within a genome are selected to “push” a phenotype in different directions. There are two basic forms of genetic conflict. Intragenomic conflict involves conflicting selective pressures between different genetic elements within an individual organism (e.g. between cytoplasmic genes and autosomal genes). Intergenomic conflict occurs between genetic elements in different individuals that interact over a particular phenotype. Genetic conflict is an inherent feature of sex-determining systems. For example, cytoplasmically inherited genetic elements (e.g. mitochondria, cytoplasmic microorganisms, plastids) are typically inherited through the egg cytoplasm P1: PSA/spd P2: ARK/ary QC: ARK October 16, 1998 18:53 Annual Reviews AR067-09 SEX DETERMINATION EVOLUTION 235 but not through sperm. As a result, these elements are selected to produce strongly female-biased sex ratios, which increases their transmission to future generations (42, 55). In contrast, autosomal genes (those residing on non-sex chromosomes) are generally selected to produce a balance in the sex ratio (57). As a result, cytoplasmic and autosomal genes are selected to push sex determination in different directions. There is considerable evidence that conflict between autosomal and cytoplasmic genes is widespread (86, 170). Genetic conflict over sex determination can also occur between sex chromosome and autosomal genes and between parentaland offspring-expressed genes. Coevolutionary interactions among these conflicting selective components may provide a “motor” for evolutionary change in sex determination. We discuss various models for the evolution of sex determination, focusing on the potential role of genetic conflict. We argue that genetic conflict is the most likely general explanation for the diversity of sex-determining mechanisms. However, although the evidence for its role in sex determination is mounting, unequivocal examples of genetic conflict causing evolutionary transitions in sex determination have yet to be made. In light of this, possible directions for future research are discussed. The reader is also referred to reviews on the diversity of sex-determining mechanisms (17, 175), sex-ratio evolution (3, 31, 171), the evolution of heteromorphic sex chromosomes (27, 142), and somatic and germline sex determination in fruitflies (35, 137, 156), vinegar worms (36, 80), mammals (64, 82, 100), and plants (66). BRIEF HISTORICAL SKETCH