Heredity (2002) 88, 102–111

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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 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 (Düebendorfer 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; Düebendorfer 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
ever, this result has been largely ignored, and its impli- are used to confirm results from the genetic and inclusive
cations for the evolution of sex determination have not fitness models.
been explored. Here, we consider modifications of Triv-
ers’ original approach, and consider their implications for Optimal sex ratios for maternal and zygotic genes
the evolution of sex determining systems. We show that For both analytical approaches, we consider the dynam-
whenever the sex ratio in a family affects the fitness of ics of a rare mutant whose sex ratio strategy deviates
either the progeny within that family or the maternal fit- from that of the rest of the population. The following
ness, then selection acting upon maternal-effect and terms are defined: x is the mutant sex ratio (proportion
zygotic sex determination genes will diverge. Further- males), x̂ is the sex ratio of the common genotype and
more, we show that coevolution of the maternal-effect the resident sex ratio strategy, ␻(x̄) is the fitness of all
and zygotic sex determining genes can lead to the evol- members of the family (both males and females), which
ution of single zygotic locus sex determination, a likely is a function of the average proportion of males in the
primitive precursor to male heterogametic (XY) or female family, x̄. For much of our analysis, we will use a simple
heterogametic (ZW) sex determination (Rice, 1987; Char- linear function, ␻(x̄) ⫽ ␣ ⫹ ␤x̄ where ␣ and ␤ are con-
lesworth, 1996). We also show that such coevolution can, stants. If ␤ ⬎ 0, individuals in male-biased broods have
in different circumstances, lead to monogeny (production higher fitness and other things being equal we expect a
of all-male or all-female families based on maternal male-biased sex ratio to evolve. If ␤ ⬍ 0 female-biased
genotype). These models may be relevant to a variety of broods have higher fitness and a female-biased sex ratio
biological systems. The applicability of the models to real should evolve.
biological systems is discussed. First, the inclusive fitness approach is used to deter-
mine the optimum sex ratio for a maternally-expressed
The basic model gene where offspring fitness is influenced by family sex
Consider a species in which the sex of an individual is ratio. Consider a female producing a brood of sex ratio
determined either by the genotype of the mother (ie, by x in a population where the vast majority of others

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JH Werren et al

104
produce a sex ratio x̄. The mutant’s fitness, Wm is given from equation 4, if n ⫽ 1 (there are no brood mates for
by a weighted form of the Shaw–Mohler equation the parent and offspring to treat differently). The opti-
(Charnov, 1982) that takes into account the effect of the mum sex ratio in the case of full sibs (r ⫽ .) is
␤ ⫺ ␣ ⫹ 冑␣(␣ ⫹ ␤) ⫹ ␤2
mutant’s sex ratio on brood fitness,

Wm ⫽ 冉
␻(x) 1 ⫺ x x
⫹ .
␻(x̂) 1 ⫺ x̂ x̂ 冊 (1)
x*z ⫽
3␤
.

Both equations 2 and 6 are also obtained using an

(6)

⭸Wm
The ESS sex ratio is found by solving
⭸x |x⫽x̂
(eg, Char-
explicitly population genetic approach (see Appendix).
Figure 1 shows the optimal sex ratio for the parent, for
the zygote in a family of full siblings, and for the zygote
nov, 1982) and with the linear fitness relationship
in a family of half siblings. Except when ␤ ⫽ 0 (no sex
described above is
ratio effect on family fitness) the maternal and zygotic
3␤ ⫺ 2␣ ⫹ 冑4␣2 ⫹ 4␣␤ ⫹ 9␤2 optima are different. If individuals in male-biased broods
x*m ⫽ , (2) have higher fitness (␤ ⬎ 0), then more male-biased sex
8␤ ratios are favoured. However, maternally-expressed
where the asterisk and subscript m denote the maternal genes are selected to produce a more male-biased sex
optimum. ratio than are zygotically-expressed genes. As relatedness
Now consider a zygotically-expressed factor, and among zygotes in the family decreases (eg, half-sibs; r ⫽
specifically a rare mutant which when expressed in the 1), the zygotic optimum becomes less male biased and
zygote causes its bearer to become male with probability potential conflict between maternal and zygotic genes
x. If there are n other individuals in the brood then the increases. When female-biased families have higher fit-
1 ness, then the reverse pattern results.
average brood sex ratio is (x ⫹ (n ⫺ 1)x̂). In the inclus- The conflict arises because sex ratio selection is affected
n
ive fitness approach we tally the effect of this single by two factors: (i) the Fisherian advantage of producing
mutant’s behaviour on its own fitness, and on that of its the rarer sex which tends to result in a sex ratio of equal-
siblings weighted by their coefficient of relatedness, r ity at equilibrium, and (ii) the family-level advantage of
(Hamilton, 1964). The mutant’s inclusive fitness, Wz, can producing a greater proportion of the less damaging (or
be expressed in Shaw–Mohler form less costly) sex. Parents and young weight these effects
slightly differently, with selection acting on a zygotically-

Wz ⫽
␻ 冉
1
n
(x ⫹ (n ⫺ 1)x̂) 冊 (3)
expressed gene emphasizing (i) over (ii) relative to a
maternally expressed gene, hence leading to a sex ratio
nearer equality. There is thus a potential for conflict and
␻(x̂)
this will be greater in species with multiply mating
1 1 females where sibling relatedness is lower.

冢 冣
((1 ⫺ x) ⫹ r(n ⫺ 1) (1 ⫺ x)) (x ⫹ r(n ⫺ 1)x)
n n
⫹ , Coevolution of maternal sex ratio and a dominant
(1 ⫺ x̂) x̂
zygotic masculinizer
The above solutions demonstrate the potential for con-
where the two terms in parentheses are the relative fit- flict, but they do not address the evolutionary dynamics
ness gains through female and male function (both via of such conflict. We investigate this in the following
self and siblings) respectively. The optimum zygotic sex
ratio, x*z, is found as before,

x ⫽
*
␤␾ ⫺ 2␣n ⫹ 冪4␣n 2
(␣ ⫹ ␤) ⫹ ␤2␾2
(4)
z
2␤(n ⫹ ␾)
where ␾ ⫽ n ⫹ 2(1 ⫹ (n ⫺ 1)r).
We digress slightly to discuss exactly what we mean
by brood size, n. In the mutant offspring fitness equation,
the unilateral change in sex ratio by the mutant affects
the fitness of n other offspring. It does not actually matter
whether these other offspring are contemporaneous or
are part of the parent’s future reproductive success so
long as the offspring’s sex ratio decision affects its own
and their fitness. As optimum offspring sex ratio asymp-
totes quite fast with increasing n we shall henceforth Figure 1 Maternal and zygotic optimal sex ratios in relationship to
assume n → ⬁ in which case relative cost of male production (␤). When ␤ ⬍ 0, males reduce
brood fitness more than daughters, and a female-biased sex ratio
␤(1 ⫹ 2r) ⫺ 2␣ ⫹ 冑4␣(␣ ⫹ ␤) ⫹ ␤2(1 ⫹ 2r)2 is favoured for both maternal and zygotic genes. Similarly, when
x*z ⫽ . (5) daughters are the more detrimental sex (␤ ⬎ 0), a male-biased sex
4␤(1 ⫹ r) ratio is selected. Maternally-expressed genes favour a more skewed
sex ratio (solid line) than zygotic genes. The zygotic optimum
Note that we re-obtain the parental optimum (Equation depends on relatedness within broods: genes expressed in full-sib-
2) if r ⫽ 1 (which implies that the offspring, like the par- ships (crossed line) are selected to bias the sex ratio more than
ent, values brood mates identically to itself) and also genes in half-sibships (dashed line).

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105
sections, where the co-dynamics of maternal and zygotic where ⑀i is the sex-specific frequency of one of the three
genes are analyzed using a population genetic approach. genotype/sex combinations containing the A allele
Specifically, we first investigate the co-dynamics of an (Aamm females, i ⫽ 1; Aamm males, i ⫽ 2; AaMm males,
allele that causes male development (a dominant i ⫽ 3). To obtain relative gene frequencies we divide by
masculinizer) at a zygotic sex determination locus, and Tf or Tm, the total number of females and males produced
alleles at a maternal effect locus. We are particularly that generation

冉 冊
interested here in whether conflict can lead to an XX
female, XY male sex determination system. 1⫺x̂ x̂⫹1
Tf ⫽ (1 ⫺ q) (1 ⫺ x̂) ␻(x̂) ⫹ q ␻ (10)
Consider two loci, the first coding for a maternally- 2 2
expressed factor that determines brood sex ratio. aa is the
common genotype and such females produce a brood sex
ratio of x̂ (though this may be overridden by a zygotically
Tm ⫽ (1 ⫺ q) x̂␻(x̂) ⫹ q
x̂⫹1
2
␻冉 冊
x̂⫹1
2
(11)

expressed factor). Aa is a mutant genotype where the Whether the rare allele spreads depends on the value of
dominant A allele causes the mother to produce a sex the dominant eigenvalue (␭) of the matrix G. The optimal
ratio of x. The second locus is expressed in the zygote; ⭸␭
individuals with the mm genotype become male with
probability x or x̂ depending on their mother’s genotype,
maternal sex ratio x*m is found by calculating
⭸x
⫽0
|
x⫽x̂

while the mutant Mm genotype causes its bearer to and checking that ␭ is at a maximum rather than a mini-
become male, regardless of maternal genotype. The M mum (eg, Charnov, 1982).
allele is thus a dominant masculinizer. Because Mm males Analytical solution of the maternal optimum is poss-
can only mate with mm females the MM genotype never ible if the function ␻ is specified but even with the sim-
occurs. Let the fraction of males with the Mm genotype plest linear form the result is too complicated to be
be q. informative. We thus proceed by numerical solutions,
How will maternal sex ratio, x, and the frequency of though note two special cases. First, if ␻ is a constant (ie,
the zygotically-determined males, q, coevolve? We inves- no effect of brood composition on fitness) then xm *
⫽
tigate this by first calculating equilibrium q* given x, and (1 ⫺ q)/(2 ⫺ q) and the overall population sex ratio is ..
then the optimal maternal sex ratio x*m given q. As has long been appreciated, the Fisherian sex ratio can
be achieved by all females producing half sons and half
Frequency of Mm males: If the frequency of Mm among daughters, or half the females producing sons and the
males in the current generation is q then the frequency in other half daughters, or, as here, a combination of the
the next (q⬘) will be the number of Mm progeny produced two. Second, if Mm males are absent (q ⫽ 0) then the pure
divided by the total number of male progeny, taking into effect of brood composition on sex ratio can be studied,
account the fitness effect of brood sex ratio on all off- 1
for example if ␻ ⫽ ␣ ⫹ ␤x then x*m ⫽ (3␤ ⫺ 2␣ ⫹
spring as before. Thus 8␤
冑4␣ ⫹ 4␣␤ ⫹ 9␤ ) which is exactly the same result as
冉 冊
2 2

x⫹1 that derived earlier for the maternal optimum using the
q.␻
2 inclusive fitness approach (Equation 2).

冉 冊
q⬘ ⫽ , (7)
x⫹1 x⫹1
q ␻ ⫹ (1 ⫺ q)x␻(x) Co-dynamics of Mm and maternal sex ratio: Given the
2 2 frequency of Mm males as a function of maternal sex
and at equilibrium, q* ratio, and the optimum sex ratio of maternally-expressed

冉 冊
genes to different frequencies of Mm, the co-dynamics of
x⫹1 the system can be explored. The dynamics of the system
.␻ ⫺ x␻(x)
2 are quite interesting. Basically, when males have a nega-

冉 冊
q* ⫽ . (8) tive effect on family fitness (␤ ⬍ 0), a positive feedback
x⫹1 x⫹1
␻ ⫺ x␻(x) between the maternal effect sex ratio and the frequency
2 2 of Mm occurs. This positive feedback results in the evol-
ution of dominant male zygotic sex determination. Figure
Optimal maternal sex ratio: We now consider the optimal 2a illustrates the case where males have a mild negative
maternal sex ratio in a population containing Mm males effect on family fitness (␤ ⫽ ⫺0.1). In the absence of Mm
at frequency q among males. With random mating and males, this leads to a slightly female-biased maternal sex
assuming A is sufficiently rare such that AA genotypes ratio (in this particular case x*m ⫽ 0.474). However, this
and Aa ⫻ Aa matings can be ignored, the transmission female-biased sex ratio allows the M allele to invade and
dynamics of the A allele in a population of aa individuals to equilibrate at a frequency of 0.051. M spreads for the
can be represented in matrix format by ⑀⬘i ⫽ G⑀i, or reasons described in the first section: it is a zygotically-
(1 ⫺ q)
1⫺x
2
␻(x) ⫹ q
1⫺x
4
␻ 冉 冊
x⫹1
2
1⫺x̂
␻(x̂)
1⫺x̂
4
␻ 冉 冊
x̂⫹1
2
expressed gene and compared with maternally-expressed
genes it experiences stronger Fisherian frequency-depen-

冢 冣冢 冣
2
Tf Tf Tf dent selection, and weaker selection to produce less of
x x
冉 冊
x⫹1 x̂ x̂
冉 冊
x̂⫹1 the sex that reduces family-level fitness. Given that the

冢冣
⑀⬘1 (1 ⫺ q) ␻(x) ⫹ q ␻ ␻(x̂) ␻ ⑀1
2 4 2 2 4 2 frequency of Mm males is 0.051 a lower maternal sex ratio
⑀⬘
= ⑀2 ,
2
Tm Tm Tm is selected (0.461) and this leads to a greater value of q
冉 冊 冉 冊
⑀⬘3 ⑀3 and so on. As is plotted in Figure 2a, the system evolves
1 x⫹1 1 x̂⫹1
q ␻ ␻ until q ⫽ 1 and all males are Mm and x*m ⫽ 0 and all
4 2 4 2
0
Tm Tm females are mm. This shows that the system can evolve
(9) to a dominant male zygotic sex determination (Mm male,

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106

Figure 3 Evolution to monogeny: a maternal feminizer overrides

a zygotic male determining locus (␤ = −0.1). Complete monogeny
evolves, with the population being composed of Ff mothers that
produce all daughters and ff mothers that produce all sons (x*z = 1).
As above, the population sex ratio thus evolves to 50:50 (q* = 0.5).
Arrows indicate the trajectory of evolutionary change.

chromosomes. The evolution of heteromorphic sex chro-

mosomes from undifferentiated precursors has been
demonstrated theoretically and results from selection for
reduced recombination, which can occur for a variety of
reasons (Charlesworth, 1978, 1996; Charlesworth and
Charlesworth, 1980; Rice, 1987, 1994).
An interesting and counter-intuitive outcome of
maternal-effect zygotic conflict is that the population sex
ratio evolves to 50% males. This occurs even though the
‘optimal’ sex ratio for both maternal effect and zygotic
genes is female-biased (Figure 1). The reason for this is
Figure 2 (a) Maternal effect optima and proportion Mm zygotes that the presence of the conflict over sex ratio allows the
among males when males reduce brood fitness more than females successive invasion of increasingly biased maternally-
(␤ = −0.1). A positive feedback between the dominant male allele
and maternal feminizing alleles leads to male heterogamety (Mm
and zygotically-expressed factors that ultimately reach a
males and mm females). The population starts at the maternal sex hard constraint (the frequency of Mm males cannot
ratio optimum and 0% Mm males. It evolves along the line of evol- exceed one, and maternal sex ratio cannot be smaller than
utionary trajectory indicated by the arrows, by a ‘positive feedback’ zero) that results in the equal sex ratio. We have explored
between maternal and zygotic sex determining loci, reaching the the co-dynamics of the two loci for different values of ␤
end-point where 100% of males are Mm and the maternal locus ⬍ 0 and for different forms of the function ␻ and believe
produces 0% males (mm females). (b) Maternal effect optima and
proportion Ff zygotes among females when females reduce brood
our results are robust whenever there is conflict of this
fitness more than males (␤ = 0.2). When females are the more type with males having a greater negative effect on fam-
‘costly’ sex, the system evolves to female heterogamety (Ff females ily fitness than females. The analysis presented here relies
and ff males; arrows as above). on invasion analysis for the maternal allele, A, but we
have also simulated the complete dynamics of the system
to check that invasion by A implies it achieves fixation.
mm female) as a result of the maternal-zygotic genetic The analysis above assumes that the maternal effect
conflict. Such dominant single locus male sex determi- locus evolves incrementally by replacement of alleles of
nation occurs in many organisms, including a number of small effect relative to resident alleles, in response to the
systems with cytologically heteromorphic sex chromo- dominant zygotic masculinizing allele. Is the positive
somes (XY male XX females), where a dominant male feedback dependent upon small incremental changes at
determiner occurs on the Y. Degenerate Y chromosomes the maternal effect locus? We investigated this by looking
are believed to evolve from dominant single locus sex at the dynamics of a major maternal effect locus with a
determination by a number of mechanisms dominant masculinizer. In this situation Fmfm females pro-
(Charlesworth, 1978; Rice, 1994). Such a system can be duce all-females among the mm progeny (Mm progeny
considered analogous to a primitive (cytologically develop into males) and fmfm females produce x ⫽ 1/2
undifferentiated) sex chromosome system with male het- sons among mm progeny (Mm develop into males). Here,
erogamety, where a dominant male determiner occurs on the all-female producing Fmfm genotype invades the
the analogue to the Y chromosome (Bull, 1983). Such population whenever ␤ ⬎ 0, and positive feedback
dominant single locus male sex determination occurs in evolves the system to dominant zygotic masculinizer as
many organisms, including systems with (XY male XX before (FmFmMm males and FmFmmm females). Therefore,
females) but without cytologically heteromorphic sex the result is not dependent upon incremental changes at

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JH Werren et al

107
the maternal effect locus. The same conclusions result for A more complete treatment of the dynamics leading
evolution of ZW females when ␤ ⬎ 0 (see below). to monogeny will be presented elsewhere, and here we
present only the basic results. When males negatively
Evolution of incipient female heterogamety and affect family fitness, maternal-effect loci are selected to
monogeny produce a female-biased sex ratio. Above we have shown
Here it is shown that the same type of positive feedback how this can lead to XY-type sex determination when
between maternally- and zygotically-expressed sex deter- there is a zygotic, dominant masculinizer that overrides
mination loci in the presence of conflict over the sex ratio the action of a maternal sex determining locus. However,
can give rise to incipient female heterogamety (primitive now consider a maternally-expressed allele (Fm) that
ZW female/ZZ male systems) and monogeny (females causes its bearer (Fmfm) to produce all-female broods, and
that produce 100% males or 100% females), depending that overrides the action of a zygotic locus; the progeny
upon the circumstances. of fmfm mothers develop into the sex based upon their
genotype at the zygotic locus (aa or Aa), whereas Fmfm
Evolution of female heterogametic sex determination mothers produce all-female progeny. Following the same
(primitive ZW females): The analysis of the evolution of approaches as before, the equilibrium frequency (q*) of
incipient female heterogamety (again, to the primitive . ␻(0) ⫺ (1 ⫺ x)␻(x)
stage with sex chromosomes undifferentiated except at a Fmfm females is q* ⫽ , and the zygotic
single sex determining locus) uses the same basic ␻(0) ⫺ (1 ⫺ x)␻(x)
approach as above. Female heterogamety evolves when optimum in the presence of such females can be found
female progeny are more costly to family fitness (␤ ⬎ 0). from analysis of the matrix:
Here we consider a zygotic locus which when ff causes
its bearer to become male with a probability, x or x̂, dic- (1 ⫺ x) ␻ 冉 冊
x⫹x̂
1 q␻(0) ⫹ . (1 ⫺ q) (1 ⫺ x) ␻冉 冊x⫹x̂

冢 冣冢 冣
2 2 ␻(0)
tated by maternal genotype, but which when Ff always 2Tf Tf 4Tf
develops as a female (a dominant feminizer). As Ff indi-
viduals are always females they inevitably mate with ff
males and no FF genotypes are ever produced. Proceed- 冢冣
⑀⬘1
⑀21
⬘
=
x␻ 冉 冊
x⫹x̂
2
(1 ⫺ q)x␻ 冉 冊
x⫹x̂
2
0
⑀1
⑀2
⑀31
⬘ 2Tm 2Tm ⑀31
ing exactly as before we can derive the equilibrium fre-
q␻(0) ␻(0)
quency of Ff as a function of maternal sex ratio, and then 0
4Tf 4Tf
derive the optimum maternal sex ratio as a function of
the Ff frequency. It is easy to show that the dominant (12)
feminizer will not invade when ␤ ⬍ 0 (ie, when males
are the costlier sex to family fitness). However, it does with: Tm ⫽ (1 ⫺ q)x̂␻(x̂), Tf ⫽ q␻(0) ⫹ (1 ⫺ q) (1 ⫺ x̂)␻(x̂),
readily invade when ␤ ⬎ 0, as described below. and ⑀i the frequencies of Aafmfm females (i ⫽ 1), Aafmfm
In Figure 2b we illustrate the co-dynamics in the same males (i ⫽ 2) and AaFmfm females (i ⫽ 3).
way as in the analysis of the dominant masculinizer, We can show that under some circumstances, the Fmfm
except that now we assume that females have a slightly genotype will spread through the population to a fre-
greater negative effect on offspring fitness (␤ ⫽ 0.2). This quency of 0.5, while the zygotic sex locus optimum
effect results in a slightly male-biased maternal sex ratio, declines to 0% males (x*z ⫽ 0; Fig. 3). The result is mon-
which allows Ff to spread and equilibriate at a low fre- ogeny; a population of females producing either 100%
quency. This initiates the same type of positive feedback daughters (Fmfm) or 0% daughters (fmfm). Our analysis of
observed before, except that now it results in 100% of the co-dynamics indicates that monogeny will not neces-
females being Ff and 100% of males being ff (because the sarily evolve; for ␤ ⬍ ⫺0.5 an internal equilibrium exists
maternal effect locus evolves to 100% male production, such that the frequency of Fmfm ⬍ 0.5 and x*z ⬍ 1. Simi-
x*m ⫽ 1). We thus have incipient female heterogamety, larly, when females are more costly to family fitness (␤
potentially a precursor to the ZW female/ZZ male sys- ⬎ 0), then a dominant all-male maternal effect allele spre-
tems found in birds, some reptiles and fish and invert- ads and zygotic alleles evolve towards more female pro-
ebrates (White, 1973; Bull, 1983). Note that the positive duction.
feedback does not require small incremental changes at Given that family sex ratio effects on family fitness can
the maternal locus; simulations indicate that female het- evolve either dominant zygotic sex determination (XY
erogamety will also evolve from a positive feedback males and ZW females) or dominant maternal effect
between a dominant maternal allele that produces 100% alleles and monogeny, the question is which should
males and a dominant zygotic feminizer (that overrides occur? Based on these models, we conclude that this
the action of the maternal locus). As before, despite both depends upon whether maternal effect or zygotic genes
optima being male biased, the end result of coevolution- are ‘epistatically’ dominant. That is, if a zygotic gene can
ary feedback is a 1:1 population sex ratio. override the maternal effect contribution, then XY or ZW
systems result. If a maternal effect locus overrides zygotic
Evolution of monogeny: In some sex determination sys- sex loci, then monogeny can occur. Our analysis indicates
tems, sex ratio is apparently determined completely by that conditions for the evolution of monogeny may be
the genotype of the mother. In these systems, some more stringent than those for dominant zygotic sex deter-
mothers produce 100% males whereas others produce
mination. However, we suspect that other selective
100% females (White, 1973; Bull, 1983). These are presum-
effects (eg, inbreeding depression) may also predispose
ably cases where sex is controlled by maternal effect
systems to monogeny versus zygotic sex determination
genes. Examples include the fly Chrysomya rufifacies
(Bull, 1983).
(Ullerich, 1984), some coccid insects (Nur, 1989), midges
and cynipid wasps (White, 1973).

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JH Werren et al

108
Discussion dio et al, 1990). Gomendio et al (1990) discuss examples
where son suckling frequency is higher than that of
Trivers (1974) first pointed out the potential for genetic daughters in red deer, goats, bison and African elephants.
conflict between parents and offspring over repro- There is evidence for sex-biased resource allocation in
duction. It is widely known that he considered conflict primates (reviewed in van Hoof (1997)) and some human
over resource allocation to progeny (parental populations (Bereczkei and Dunbar, 1997). Examples and
investment), and concluded that progeny are generally scenarios for biased provisioning in birds are reviewed in
selected to seek more resources from a parent than the Stamps (1990) and Sheldon (1998). In several bird species,
parent is selected to provide, assuming that providing the there is now substantial evidence that fledging sex ratios
extra resource imposes a future reproductive cost to the may be determined by maternal-offspring conflict over
parent. He also extended this thinking to sex ratio evol- sex ratio and resource allocation (Dhondt and Hoch-
ution (Trivers, 1974) showing that the optimum sex ratio achka, 2001). In the great tit, Parus major, male chicks are
differs for the offspring versus the mother when one sex stronger competitors than their female siblings, resulting
costs more to produce than does the other. However, the in more male-biased fledging sex ratios particularly when
implications of this result to the evolution of sex determi- resources are scarce, the opposite pattern to that favoured
nation have not been widely considered. by maternal sex ratio genes (Oddie, 2000). Many potential
Here we show that even relatively slight effects of fam- examples of sex ratio dependent maternal fitness may
ily sex ratio on offspring fitness results in genetic conflict occur when offspring fitness is sex-differentially depen-
over sex determination, between maternally expressed dent on maternal condition (Trivers and Willard, 1973)
and zygotically expressed genes. This conflict, via a ‘posi- as this model implicitly assumes sex-differential costs of
tive feedback’ between zygotic and maternal effect genes, rearing (average) offspring. These circumstances are also
can lead to the evolution of dominant single locus zygotic likely to be common in insects and do not require exten-
sex determination. When male progeny reduce family sive parental care to occur. For example, Nunney (1983)
fitness, a dominant Mm male mm female system evolves; found that the size and fecundity of male and female
when female progeny reduce family fitness, a dominant Drosophila are differentially affected by food availability,
Ff female ff male system evolves. Although the outcome suggesting that family sex ratio could influence offspring
can be zygotic ‘control’ over sex determination, the fitness under some circumstances. Another key point is
underlying structure of sex determination should still that the fitness effects can be very slight, and still catalyze
reveal the conflict. In Mm male systems, maternally the evolution of maternally expressed genes that favor
expressed genes are predicted to push sex determination one sex and a dominant sex determining allele that favors
towards female development, and it is for this reason the opposite sex. For this reason, the conditions favoring
that, in the absence of the dominant M male determiner, the positive feedback that leads to dominant zygotic sex
the default sex of mm individuals is female. Similarly, in determination are likely to be widespread.
Ff female systems, maternally expressed genes are pre- Dominant zygotic sex determination is likely to be a
dicted to push sex determination towards males, and the precursor to the evolution of heteromorphic sex chromo-
default sex in the absence of F (due to the action of somes in some systems; Mm male heterogamety leading
maternal effect genes) is male. In both cases, a dominant to the evolution of XY males with heteromorphic sex
single sex locus sex determination is expected to evolve chromosomes and a degenerate Y chromosome, and Ff
when the sex locus can override the influences of matern- female heterogamety leading to the evolution of ZW
ally expressed genes favoring the opposite sex. A key females with heteromorphic sex chromosomes and
point here is that even though the sex ratio in the popu- degenerate W chromosomes. The processes involved in
lation may be 50:50, with a dominant zygotic sex sex chromosome evolution have been examined exten-
determining locus, the situation can arise from genetic sively and are thought to be quite complex (Charlesworth
conflict between zygotic and maternal sex determining and Charlesworth, 1980; Bull, 1983; Rice, 1987, 1994;
factors and the signature of this conflict will be apparent Charlesworth, 1996). Once an incipient sex chromosome
in the expression patterns of zygotic and maternal sex system (eg, single locus sex determination) has evolved,
determining genes. selection can favor reduced recombination between sex
The structure of our model is general enough to be chromosomes for a variety of reasons (Rice, 1987; Charle-
applicable to three different situations: (a) sex ratio in a sworth, 1996). As a result, further heterogeneity charac-
family affects the fitness (eg, size, survival) of offspring in teristic of advanced sex chromosome systems can evolve,
the family, (b) male and female offspring ‘cost’ different including loss of gene function and eventual degener-
amounts of resources for the mother to produce, and ation of the Y. Less work has concentrated on the pro-
therefore her family size is influenced by her family sex cesses involved in the initial evolution of dominant single
ratio (in this case the fitness term is family size, which is locus sex determining systems.
a function of the sex ratio), and (c) the sex ratio in the XY male/XX female sex determination occurs in mam-
family affects longevity or future fecundity of the mother, mals and is common in vertebrates and some insect
and therefore her lifetime fitness. How likely are these groups. ZW female/ZZ male systems occur in birds,
conditions to exist in nature? Most relevant data come snakes, lepidopterans (butterflies and moths), some fish
from mammals and birds. Males of many polygynous and isopods, and other organisms (Bull, 1983). It is not
mammals are thought to be more costly than females, uncommon in the literature for dominant Mm male sex
although appropriate cost measurements are rare determination to be described as XY male sex determi-
(Clutton-Brock, 1982; Clutton-Brock and Iason, 1986). nation (and dominant Ff female sex determination as ZW
Mothers allocate more resources to sons than daughters female sex determination), even in systems without het-
in red deer, and are less likely to calf having reared a son eromorphic sex chromosomes. Further, many systems
in the previous winter (Clutton-Brock et al, 1981; Gomen- with heteromorphic sex chromosomes may involve a

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JH Werren et al

109
dominant zygotically-acting sex locus on the heteromor- Both theoretical and empirical studies present growing
phic sex chromosome. evidence that genetic conflict can play a role in sex deter-
In mammals, sex determination is likely to have arisen mination evolution (Bull and Charnov, 1977; Juchault and
originally from dominant male sex determination, with Rigaud, 1995; Carvalho et al, 1998; Werren and Beuke-
the dominant sex locus SrY now occurring on the other- boom, 1998; Caubet et al, 2000; Werren and Hatcher,
wise largely degenerate Y chromosome (Goodfellow and 2000). The existence of divergent selection between
Lovell-Badge, 1993). In Diptera, sex determination ranges nuclear genes and inherited cytoplasmic factors (eg, mito-
from single locus dominant male (Mm males), to XY sys- chondria, chloroplasts, inherited microorganisms) is well
tems containing a dominant sex locus, to X:Autosomal established and can lead to polymorphisms in sex deter-
balance, to monogeny (dominant maternal sex mination within populations, such as CMS in plants
determination) (Marin and Baker, 1998). In systems with (Koelewijn and van Damme, 1995; Frank, 2000) and cyto-
X:Autosomal balance sex determination, such as Droso- plasmic sex ratio distorters in animals (Juchault et al,
phila melanogaster, it is less obvious whether dominant 1993; Kelly et al, 2001). Conflict between driving sex chro-
single locus sex determination was the ancestral state. mosomes and autosomal genes may similarly shape sex
However, given the abundance of dominant sex locus sex determining systems (Hamilton, 1967; Carvalho et al,
determination in other dipterans (Marin and Baker, 1998), 1998; Jaenike, 1999).
it is possible that X:autosome balance systems were also Added to these more obvious sources of conflicting
derived ancestrally from dominant Mm male sex determi- selective pressures over sex determination, is maternal-
nation. One explanation for the evolution of X:Autosomal zygotic gene conflict. Such conflict can result under par-
balance is selection for coupling of dosage compensation tial inbreeding (Werren and Hatcher, 2000) or as shown
with sex determination. Dosage compensation is a prob- here when fitness of offspring correlates with family sex
lem which arises once one sex chromosome has under- ratio. The potential consequences of maternal-zygotic sex
gone degeneration or gene silencing, such that the hetero- determination conflict have not been fully explored. For
gametic sex has an unbalanced number of example, more explicit models are needed to investigate
transcriptionally active genes on the sex chromosome. the effects of multiple mating, maternal fitness effects,
There are a number of theories proposed to explain the and differential fitness costs to male and female progeny
evolution of Y (or W) degeneration (Charlesworth, 1978; on maternal and zygotic conflict. Also unexplored is
Rice, 1994). potential maternal-paternal conflict over zygotic sex
The results presented here show that likely precursors determination. Such conflict could be mediated by
of XY:XX and ZW:ZZ heteromorphic sex chromosome paternal and maternal imprinting of sex determining loci;
systems, dominant Mm male and dominant Ff female sex such as proposed for genes involved in offspring accrual
determination, readily evolve as a consequence of of resources during pregnancy (Haig, 1993). As a general
maternal-zygotic genetic conflict over sex determination. pattern, we expect that paternally expressed sex
To our knowledge, this is one of the few formal models determining genes will be selected to push sex determi-
accounting for the evolution of dominant single locus sex nation more towards a balanced sex ratio (as is the case
determination. Charlesworth and Charlesworth (1978) for zygotic sex determining genes); differential selection
have investigated analytically the evolution of two- on paternal versus maternal sex determiners will increase
zygotic locus systems (involving separate loci for male with multiple mating by the female, either within a single
and female function) for the evolution of separate sexes brood or over successive broods, because the ‘genetic
from a hermaphroditic plant progenitor. Bull (1983: pp interests’ of maternal and paternal genes diverge more
135–137) and Kraak and DeLooze (1993) have suggested greatly under these circumstances.
other routes to the evolution of single locus sex determi- We hope that researchers investigating the mechanics
nation; their theories invoke fluctuations in the popu- of sex determination will consider the possible role of
lation sex ratio for major genes to become established. conflicting selective pressures between different genetic
A second possible outcome of maternal zygotic gene elements, particularly between zygotic and maternal sex
conflict is the evolution of maternal control over zygotic determining loci, in shaping the underlying structure of
sex determination. When a dominant maternal locus sex determination systems.
exists, this will lead to monogeny, where some females
produce all-female families and others produce all-male
families. Our results show that monogeny can evolve Acknowledgements
when the maternal locus overrides the action of zygotic The work of JHW was supported by funds from the US
sex loci, and when the fitness of the family is affected by NSF. MJH was supported by the Royal Society (Dorothy
sex ratio in the family. Monogeny occurs in a number of Hodgkin Research Fellowship 502008) and NERC
dipterans, including some midges and sciarid and calli- (GR3/11880). We would like to thank Deborah Charles-
phorid flies (Ullerich, 1984; Gerbi, 1986; Rocha and Peron- worth, Brian Charlesworth, and Leo Beukeboom for help-
dini, 2000). It is unclear to us what circumstances will ful discussions on sex determination.
lead to a maternal locus being able to override the action
of a zygotic locus, versus the reverse. It would seem that
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