tive differential investment. For example, Post et al. (1999)
and Forchhammer (2000) proposed that biased sex ratios
in dimorphic species may arise as a consequence of sex-
differential viability of fetuses resulting from differences in
growth rates and susceptibility to environmentally induced
changes in maternal condition (the extrinsic modification
hypothesis). Supporting data for nonfacultative alteration
of sex ratios are also available from literature on mouse
development at neurulation (Seller and Perkins-Cole 1987)
and timing of mating since lights out in Norway rats (Rat-
tus norvegicusHornig and McClintock 1994).
Predictions of the extrinsic modification hypothesis are
not necessarily mutually exclusive with any of the other
hypotheses discussed, as its authors point out, and all may
produce similar results (table 11.2). The key difference be-
tween the extrinsic modification hypothesis and all others is
that alteration of sex ratios or levels of parental investment
does not occur because of facultative adjustment by the par-
ents, but rather because of differential susceptibility of the
sexes to extrinsic influences. Further, even though Post et al.
(1999) proposed the model as a possibility for dimorphic
species, the level of dimorphism required to elicit differences
in fetal viability may be subtle and may not require differ-
ences in size at all. In fact, it is entirely possible that many
of the data used to support the FCA hypothesis, as well as
many further studies that show seasonal differences in sex
ratios at birth or weaning, but where the authors have found
correlations with climatic variables rather than cohort ad-
vantage (e.g., Myers et al. 1985; Goundie and Vessey 1986;
Havelka and Millar 1997) may be explained equally well
by this extrinsic modification hypothesis, without invoking
parental manipulation.
Proximate Mechanisms for Adjustment
Because maternal investment in each offspring increases
dramatically throughout gestation and lactation, elimina-
tion of developing young to alter sex ratios would appear
increasingly expensive in terms of fitness, unless litter re-
duction is necessary to tailor maternal output to environ-
mental conditions (Hornig and McClintock 1996). Conse-
quently, the earlier in the investment sequence sex ratios
can be adjusted, the lower the cost for the mother. Evidence
exists that timing of mating relative to ovulation can influ-
ence the probability that ova are fertilized by an X- or Y-
bearing sperm (reviewed by Roberts 1978; Clutton-Brock
and Iason 1986; James 1996). Specific mechanisms for these
differences have not been conclusively identified, but may
include differential facilitation or inhibition of X- or Y-
bearing sperm in the female’s reproductive tract, or pref-
erential fertilization by one or the other (Krackow 1995;
Rorie 1999). Further, data indicate that Y-bearing sperm
may swim faster than X spermatozoa, but are not as long-
lived (Roberts 1978; Soede et al. 2000).
Even if equal numbers of ova are fertilized by X and
Y spermatozoa, it does not follow that the sex ratio will
remain even at implantation. There is a growing body of
literature showing that male preimplantation embryos de-
velop faster than females, and that there are temporal limi-
tations to uterine receptivity to implantation (summarized
by Krackow and Burgoyne 1998). As a consequence, an
interaction between the asynchronous development of the
embryos and uterine receptivity can produce biased sex ra-
tios of implanted embryos (Krackow 1995; Krackow and
Burgoyne 1998). Still, even if equal numbers of males and
females implant, sex ratios after implantation may become
skewed by male and female embryos being differentially
susceptible to maternal dietary deficiencies (Rivers and
Crawford 1974), or through differential fetal resorption
(Krackow 1992). Cameron (2004) cited recent studies link-
ing circulating levels of glucose and differential responses of
male and female embryos to glucose as a potential mech-
anism for altering sex ratios. Importantly, none of these
potential causes of bias described here necessarily requires
parental manipulation, and hence may not constitute fac-
ultative manipulation of sex ratios. But neither do they ex-
clude that possibility. Even if they are not facultative they
may still be adaptive, depending on the environmental
context.Missing LinksKrackow (2002) argued persuasively that we should focus
our efforts on identifying mechanisms for distortion of sex
ratios that will prove parental manipulation and hence fac-
ultative adjustment. His conclusion underscores the fact
that a key assumption of sex ratio hypotheses other than
the extrinsic modification hypothesis is that observed biases
arise becauseof differential investment, rather than dif-
ferential investment being a result of differential offspring
mortality. While differential investment in the sexes can in-
deed produce skews at any stage of development —up to
independence — is a skewed ratio at the end of parental
investment necessarily indicative of differential investment?
Conversely, does differential investment necessarily alter the
sex ratio? The answer to both of these questions clearly
must be “NO,”as distorted sex ratios may come about by
differential mortality without differential investment, as per
the foregoing section (see also Clutton-Brock et al. 1985;
Clutton-Brock 1991). While such mortality does not neces-
sarily constitute facultative manipulation, few studies have
tested for differential investment explicitly; they simply as-Facultative Sex Ratio Adjustment 137