Maternal-offspring conflict leads to the evolution of dominant zygotic sex determination

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 1 Department 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 among maternally expressed genes (eg, mRNA’s and proteins placed into the egg) and zygotically expressed genes. Recent studies have proposed that conflicting selective pressures can occur between maternally and zygotically expressed sex determining loci and that these may play a role in shaping the evolution of sex determining systems. Here we show that such genetic conflict occurs under very general circumstances. Whenever sex ratio among progeny in a family affects the fitness of either progeny in that family or maternal fitness, then maternal-zygotic genetic conflict occurs. Furthermore, we show that this conflict typically results in a ‘positive feedback loop’ that leads to the evolution of a dominant zygotic sex determining locus. When males more negatively effect fitness within the family, a male heterogametic (XY male) sex determining system evolves, whereas when females more negatively effect fitness in the family, a female heterogametic (ZW female) system evolves. Individuals with the dominant sex allele are one sex, and the opposite sex is determined by maternally-expressed genes in individuals without the dominant sex allele. Results therefore suggest that maternal-zygotic conflict could play a role in the early evolution of chromosomal sex determining systems. Predictions are made concerning the patterns of expression of maternal and zygotic sex determining genes expected to result from conflict over sex determination. Heredity (2002) 88, 102–111. DOI: 10.1038/sj/hdy/6800015 Keywords: sex determination; parent-offspring conflict; heterogamety Introduction Animals and plants display an extraordinary variety of mechanisms for sex determination (White, 1973; Bull, 1983). This variety is surprising because we might reason that such an important developmental pathway would be highly conserved. However, even within orders and genera, sex determination varies and evolutionary transitions between mechanisms are thought to be frequent. For instance, reptiles exhibit male heterogamety (XY males with heteromorphic sex chromosomes, XX females with homomorphic sex chromosomes), female heterogamety, homomorphy with dominant male or femaledetermining alleles, environmental sex determination, and mixed genetic/environmental systems (Janzen and Paukstis, 1991; Girondot et al, 1994; Viets et al, 1994). Similarly, the Diptera show a diversity of genetic mechanisms, including X:Autosomal balance (eg, Drosophila), dominant male determining loci with heteromorphic or homomorphic sex chromosomes, dominant female determining loci, and maternal sex determination (Ullerich, 1984; Marin and Baker, 1998). The housefly (Musca domestica) shows a variety of sex determining alleles, including maternal effect and zygotically expressed genes (Düebendorfer et al, 1992; Schmidt et al, 1997). Molecular studies indicate that, although certain Correspondence: JH Werren, Department of Biology, University of Rochester, Rochester NY 14627, USA basal genes involved in sex determination may be conserved, the upstream regulators of sex determination are variable between species (Wilkins, 1995; Sievert et al, 1997; Raymond et al, 1998; Meise et al, 1998; Marin and Baker, 1998). Why are sex determining mechanisms so diverse? It has long been recognized that conflicting selective pressures over sex determination exist between autosomal genes and non-Mendelian factors (eg, cytoplasmic elements, meiotic driving sex chromosomes; Lewis, 1941; Howard, 1942; Hamilton, 1967). Various authors have proposed that such ‘genetic conflict’ may cause evolutionary change in sex determination mechanisms (Eberhard, 1980; Cosmides and Tooby, 1981; Werren et al, 1988; Hurst et al, 1996; Werren and Beukeboom, 1998). The basic reasoning behind this idea is that the distortions in sex ratio caused by such non-Mendelian elements creates strong selection for alterations in sex determination that increase production of the rarer sex, because such genotypes have increased fitness. For instance, theoretical models suggest that coevolutionary feedback between cytoplasmic and autosomal factors may lead to the evolution of monogeny (Werren, 1987) and evolutionary transition from female heterogamety to male heterogamety (Rigaud et al, 1997; Caubet et al, 2000). Similarly, 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 females in lemmings (Bull and Bulmer, 1981) and XY* females in Akodon rodents (Hoekstra and Hoekstra, 2001). Genetic conflict and sex determination JH Werren et al A more subtle form of sex determination conflict can occur between maternal effect genes (eg, genes producing maternal products such as mRNA or proteins that are placed in the egg and effect zygotic development) and zygotically expressed genes (Werren and Beukeboom, 1998; Werren and Hatcher, 2000). There is growing evidence that maternal effect genes influence sex determination in a wide range of organisms. Maternal effect sex determining genes have been described in Drosophila melanogaster (Steinemann-Zwicky et al, 1990; Cline, 1993), Musca domestica (Schmidt et al, 1997; Düebendorfer and Hediger, 1998), Caenorhabditis elegans (Ahringer et al, 1992) and Chrysomia rufescens (Ullerich, 1984). In many coccids (Nur, 1989), sex of the progeny is determined by the maternal genotype, almost certainly due to maternal effect products placed into the egg. As the genetic details of more systems are discovered, maternal effects on sex determination are likely to be found to be a common feature. Werren and Beukeboom (1998) suggested a number of scenarios under which maternal effect-zygotic gene conflict might arise over sex determination, including (a) partial inbreeding or local mate competition, and (b) maternal or offspring fitness varying with family sex ratio. The former scenarios were examined by Werren and Hatcher (2000), who found that maternal and zygotic optima for sex determination did indeed differ under partial sib-mating and local mate competition (Hamilton, 1967). As predicted, the maternal optima in both cases were more strongly skewed towards females. Although the zygotic optima were also female-biased, they were less biased than the maternal ESS. Despite rather small differences in the optima, under many circumstances genes producing extreme sex ratios had large initial rates of increase against the alternative strat (...truncated)