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Maternal-Offspring Conflict Leads to the Evolution of Dominant Zygotic Sex

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Maternal-Offspring Conflict Leads to the Evolution of Dominant Zygotic Sex Heredity (2002) 88, 102–111 2002 Nature Publishing Group All rights reserved 0018-067X/02 $25.00 www.nature.com/hdy Maternal-offspring conflict leads to the evolution of dominant zygotic sex determination JH Werren1, MJ Hatcher2 and HCJ Godfray3 1Department of Biology, University of Rochester, Rochester NY 14627, USA; 2School of Biology , University of Leeds, Leeds LS2 9JT, UK; 3NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, SL5 7PY, UK Sex determination in many species involves interactions males more negatively effect fitness within the family, a male among maternally expressed genes (eg, mRNA’s and pro- heterogametic (XY male) sex determining system evolves, teins placed into the egg) and zygotically expressed genes. whereas when females more negatively effect fitness in the Recent studies have proposed that conflicting selective family, a female heterogametic (ZW female) system evolves. pressures can occur between maternally and zygotically Individuals with the dominant sex allele are one sex, and the expressed sex determining loci and that these may play a opposite sex is determined by maternally-expressed genes role in shaping the evolution of sex determining systems. in individuals without the dominant sex allele. Results there- Here we show that such genetic conflict occurs under very fore suggest that maternal-zygotic conflict could play a role general circumstances. Whenever sex ratio among progeny in the early evolution of chromosomal sex determining sys- in a family affects the fitness of either progeny in that family tems. Predictions are made concerning the patterns of or maternal fitness, then maternal-zygotic genetic conflict expression of maternal and zygotic sex determining genes occurs. Furthermore, we show that this conflict typically expected to result from conflict over sex determination. results in a ‘positive feedback loop’ that leads to the evol- Heredity (2002) 88, 102–111. DOI: 10.1038/sj/hdy/6800015 ution of a dominant zygotic sex determining locus. When Keywords: sex determination; parent-offspring conflict; heterogamety Introduction basal genes involved in sex determination may be con- served, the upstream regulators of sex determination are Animals and plants display an extraordinary variety of variable between species (Wilkins, 1995; Sievert et al, mechanisms for sex determination (White, 1973; Bull, 1997; Raymond et al, 1998; Meise et al, 1998; Marin and 1983). This variety is surprising because we might reason Baker, 1998). that such an important developmental pathway would Why are sex determining mechanisms so diverse? It be highly conserved. However, even within orders and has long been recognized that conflicting selective press- genera, sex determination varies and evolutionary tran- ures over sex determination exist between autosomal sitions between mechanisms are thought to be frequent. genes and non-Mendelian factors (eg, cytoplasmic For instance, reptiles exhibit male heterogamety (XY elements, meiotic driving sex chromosomes; Lewis, 1941; males with heteromorphic sex chromosomes, XX females Howard, 1942; Hamilton, 1967). Various authors have with homomorphic sex chromosomes), female hetero- proposed that such ‘genetic conflict’ may cause evol- gamety, homomorphy with dominant male or female- utionary change in sex determination mechanisms determining alleles, environmental sex determination, (Eberhard, 1980; Cosmides and Tooby, 1981; Werren et and mixed genetic/environmental systems (Janzen and al, 1988; Hurst et al, 1996; Werren and Beukeboom, 1998). Paukstis, 1991; Girondot et al, 1994; Viets et al, 1994). Simi- The basic reasoning behind this idea is that the distor- larly, the Diptera show a diversity of genetic mech- tions in sex ratio caused by such non-Mendelian elements anisms, including X:Autosomal balance (eg, Drosophila), creates strong selection for alterations in sex determi- dominant male determining loci with heteromorphic or nation that increase production of the rarer sex, because homomorphic sex chromosomes, dominant female such genotypes have increased fitness. For instance, determining loci, and maternal sex determination theoretical models suggest that coevolutionary feedback (Ullerich, 1984; Marin and Baker, 1998). The housefly between cytoplasmic and autosomal factors may lead to (Musca domestica) shows a variety of sex determining the evolution of monogeny (Werren, 1987) and evolution- alleles, including maternal effect and zygotically ary transition from female heterogamety to male hetero- expressed genes (Du¨ ebendorfer et al, 1992; Schmidt et al, gamety (Rigaud et al, 1997; Caubet et al, 2000). Similarly, 1997). Molecular studies indicate that, although certain sex chromosome meiotic drive has been proposed as a possible mechanism causing the evolution of novel sex determining mechanisms in mammals, such as X*Y Correspondence: JH Werren, Department of Biology, University of Roch- females in lemmings (Bull and Bulmer, 1981) and XY* ester, Rochester NY 14627, USA females in Akodon rodents (Hoekstra and Hoekstra, 2001). Genetic conflict and sex determination JH Werren et al 103 A more subtle form of sex determination conflict can maternal effect genes), by the individual’s genotype occur between maternal effect genes (eg, genes producing (zygotic effect genes), or by some interaction between maternal products such as mRNA or proteins that are these two components. Further, assume that the fitness placed in the egg and effect zygotic development) and of the progeny in a family is a function of the family sex zygotically expressed genes (Werren and Beukeboom, ratio (ie, the proportion of males among the progeny of 1998; Werren and Hatcher, 2000). There is growing evi- the female parent). For simplicity, we assume that the dence that maternal effect genes influence sex determi- family sex ratio has an equal effect on the fitness of male nation in a wide range of organisms. Maternal effect sex or female progeny. As will be seen later, this model can determining genes have been described in Drosophila mel- also be used to study situations where family sex ratio anogaster (Steinemann-Zwicky et al, 1990; Cline, 1993), influences maternal fitness or family size. To examine the Musca domestica (Schmidt et al, 1997; Du¨ ebendorfer and potential for conflicting selective pressures between sex- Hediger, 1998), Caenorhabditis elegans (Ahringer et al, determination genes that are expressed in the mother and 1992) and Chrysomia rufescens (Ullerich, 1984). In many zygote, we start by comparing the optimal sex ratios for coccids (Nur, 1989), sex of the progeny is determined by each. We demonstrate that these optima are different and the maternal genotype, almost certainly due to maternal that there is a potential for conflict. We then go on to effect products placed into the egg. As the genetic details demonstrate that this conflict can lead to the evolution of of more systems are discovered, maternal effects on sex diverging sex determining systems, by analysing the joint determination are likely to be found to be a common fea- dynamics of maternal and zygotically expressed sex ture. determination genes. Werren and Beukeboom (1998) suggested a number of There are two mathematical strategies for analyzing scenarios under which maternal effect-zygotic gene con- problems such as these, one employing the machinery of flict might arise over sex determination, including (a) par- inclusive fitness (eg, Charnov, 1982), the other using tial inbreeding or local mate competition, and (b) more explicit population genetic approaches. The inclus- maternal or offspring fitness varying with family sex ive fitness approach is used to determine evolutionary ratio. The former scenarios were examined by Werren optima and is versatile in that it can be applied to a rela- and Hatcher (2000), who found that maternal and zygotic tively diverse set of biological conditions (Taylor, 1994; optima for sex determination did indeed differ under Taylor and Frank, 1996). However, it assumes weak selec- partial sib-mating and local mate competition (Hamilton, tion and only small additive genetic deviations from the 1967). As predicted, the maternal optima in both cases optimal phenotype. The population genetic approach were more strongly skewed towards females. Although makes more explicit assumptions about the genetic archi- the zygotic optima were also female-biased, they were tecture of a trait, and therefore can be applied to some less biased than the maternal ESS. Despite rather small of the conditions we plan to explore below (eg, invasion differences in the optima, under many circumstances of a dominant masculinizing sex determining allele). genes producing extreme sex ratios had large initial rates However, the latter approach is less versatile because of increase against the alternative strategy, suggesting very specific assumptions concerning the genetic archi- that slight differences in optima could lead to extremes tecture and population structure are required. We use the in sex determining strategies. inclusive fitness approach to determine the optimal sex Trivers (1974) first realized that maternal and offspring ratio for maternally and zygotically expressed genes. sex ratio optima can diverge, and derived the optimal Explicit genetic models are then employed to confirm the solutions for the situation where the costs of producing results of the inclusive fitness approach and to explore a male and female offspring differ to the parent. How- the dynamics of major effect alleles. Finally, simulations
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