Abstract:
INTRODUCTION: Mammalian reproductive and somatic development is regulated
by steroid hormones, growth hormone (GH), and insulin-like growth factor-1
(IGF-1). Based largely on information from humans, model organisms, and
domesticated animals, testosterone (T) and the GH/IGF-1 system activate
sexually differentiated development, promoting male-biased growth, often at a
cost to health and survivorship. To test if augmented prenatal androgen exposure
in females produces similar developmental patterns and trade-offs, we examine
maternal effects in wild meerkats (Suricata suricatta), a non-model species in
which adult females naturally, albeit differentially by status, express exceptionally
high androgen concentrations, particularly during pregnancy. In this cooperative
breeder, the early growth of daughters predicts future breeding status and
reproductive success.
METHODS: We examine effects of normative and experimentally induced variation
in maternal androgens on the ontogenetic patterns in offspring reproductive
hormones (androstenedione, A4; T; estradiol, E2), IGF-1, growth from pup
emergence at 1 month to puberty at 1 year, and survivorship. Specifically, we
compare the male and female offspring of dominant control (DC or high-T),
subordinate control (SC or lower-T), and dominant treated (DT or blocked-T)
dams, the latter having experienced antiandrogen treatment in late gestation.
RESULTS: Meerkat offspring showed sex differences in absolute T and IGF-1
concentrations, developmental rates of A4 and E2 expression, and survivorship
— effects that were sometimes socially or environmentally modulated. Atypical
for mammals were the early male bias in T that disappeared by puberty, the
absence of sex differences in A4 and E2, and the female bias in IGF-1. Food
availability was linked to steroid concentrations in females and to IGF-1,
potentially growth, and survival in both sexes. Maternal treatment significantly
affected rates of T, E2, and IGF-1 expression, and weight, with marginal effects on survivorship; offspring of DT dams showed peak IGF-1 concentrations and the
best survivorship.
DISCUSSION: Maternal effects thus impact offspring development in meerkats,
with associated trade-offs: Whereas prenatal androgens modify postnatal
reproductive and somatic physiology, benefits associated with enhanced
competitiveness in DC lineages may have initial costs of reduced IGF-1, delay
in weight gain, and decreased survivorship. These novel data further confirm the
different evolutionary and mechanistic pathways to cooperative breeding and call
for greater consideration of natural endocrine variation in both sexes.
