nections during postnatal life (Alberts 1984; see also Gott-
lieb 1981). Thus nongenetic maternal influences begin pre-
natally through a variety of sensory experiences, such as
when fetuses shift positions as the mother grooms, travels
or sleeps, ‘smell’ what the mother eats, and experience acute
changes in glucocorticoids when the mother is stressed by
an agonistic social interaction or a predator encounter (see
also Boonstra et al. chap. 12, this volume). Because percep-
tual development begins early, learning via some modalities
can also begin before birth. For instance, fetuses can learn
odors in the amniotic fluid that may later influence food
preferences or social recognition of kin (Hepper 1987; Terry
and Johanson 1996; Galef chap. 18, this volume). Thus pre-
natal sensory experiences can influence later behaviors, in-
cluding kin recognition, mate choice, learning, filial prefer-
ences, and mother-infant interactions (Ronca and Alberts
1995).
Circulating hormones during gestation can influence
later morphology, physiology, and behavior. For example,
in some polytocous species (litter size 1) prenatal expo-
sure to gonadal steroid hormones can profoundly alter re-
productive life histories. Individuals gestating between two
males (2M) experience higher androgen levels than those
between two females (2F), and these intrauterine position
(IUP) effects have consequences in adulthood. In house
mice, 2M females have delayed sexual maturation, reduced
fecundity, fewer litters, are aggressive and maintain large
territories, and are less sexually attractive to males, relative
to 2F females. 2M males have decreased sexual activity but
are more aggressive and more paternal than 2F males. In
addition, 2M female mice and Mongolian gerbils tend to
give birth to male-biased litters (and vice versa for 2F fe-
males), thus creating intergenerational transmission of IUP
effects (reviewed in Clark and Galef 1995; Ryan and Van-
denbergh 2002). Behavioral effects of IUP have been docu-
mented for only a few species of laboratory animals, al-
though some field observations have been made of lab-born
animals with known IUPs released on highway islands. Ob-
servations of these animals suggest that IUP does affect re-
productive and social behaviors and perhaps, ultimately,
fitness (Zielinski et al. 1992). However, it is not clear how
generalizable these effects are to other species, or to animals
born in the wild. Fortunately, for some species IUP can be
determined without caesarian deliveries, as the ano-genital
distance (AGD) reflects the degree of prenatal androgen ex-
posure and can be used as a proxy for IUP (e.g., Vanden-
bergh and Huggett 1995). Thus by measuring AGDs, field
researchers may be able to evaluate the consequences of
prenatal experiences for adult social behaviors and repro-
ductive success.
How might IUPs relate to a species’ particular ecology?
If the local environment favors one sex over another (short-
term sex-ratio biasing; Fisher 1930) because males, say, are
the rarer sex, or if a female in a polygynous species is in ex-
ceptionally good condition and would be favored to over-
produce sons (Trivers and Willard 1973), then daughters
would more often gestate between males and be partially
masculinized as adults. Those daughters may also overpro-
duce sons themselves (as 2M females tend to produce male-
biased litters), continuing to bias the population toward
males. If that daughter is in exceptionally good condition
herself, this would be beneficial, but if she is in moderate or
poor condition, then selection would not favor her sons
over her daughters, and she may experience a fitness loss.
Excess males would also be costly if the local population is
no longer female-biased. Thus the immediate effects of IUP
may, over time, influence secondary sexual characteristics,
sex ratios, and reproductive success, depending on original
maternal condition and local demographics.Perinatal environmental and social influences
on development
For fossorial or semifossorial animals reared in burrows,
developing young do not directlyexperience a broad range
of physical and social environments. Instead, parents can
convey environmental variation to their offspring indirectly.
A young animal can experience the effects of food short-
ages, climate changes (temperature, day length), or social
instability before venturing out of the nest. As an example,
when species inhabit a wide range geographically, photo-
periodic cues (day length) can be important indicators of
upcoming seasonal changes and signal appropriate times
for reproductive efforts. The photoperiod experienced by fe-
males during pregnancy is transmitted hormonally via mel-
atonin to young during gestation and lactation. In voles and
hamsters, maternal melatonin influences offspring growth
rate, fat deposition, pelage, and sexual maturation. Young
born in the spring or early summer mature quickly and may
start breeding that year, whereas those born in the late sum-
mer remain prepubertal often until the following spring,
decreasing energetic needs until reproduction begins again.
Thus perinatal melatonin from mothers adaptively primes
young for somatic and reproductive growth appropriate for
the time of year in which they are born (for an excellent re-
view of environmental cueing of photoperiod see Lee and
Gorman 2000; see also Nelson 1991 for reproductive prim-
ing via 6-MBOA, a secondary plant compound found in
newly grown vegetation).
Without ever seeing daylight a young animal can appor-
tion its somatic and reproductive efforts to best suit its fu-
ture fitness potential. Although photoperiod is commonly
thought to trigger breeding condition in seasonal species, so-
cial and dietary cues also influence development or regres-Ontogeny of Adaptive Behaviors 197