Exposure to a novel male during late pregnancy influences subsequent growth of offspring during lactation

Abstract

In mammals, allocation to reproduction can either be primed or suppressed in relation to cues from other individuals. Some conspecifics (e.g. potential mates) may enhance an individual's ability to reproduce but others may have a detrimental effect on reproductive success. One widely studied response to conspecific cues, the 'Bruce effect', occurs when pregnant females abort their pregnancies after exposure to a novel male. It has been suggested that this response has evolved as a counter-tactic to the threat of infanticide posed by novel males. In some species, like mice, pregnancy termination will only occur if females are exposed to the unfamiliar male during a brief critical period early in pregnancy, which is surprising considering that an unfamiliar male threatens infanticide whenever present, and in particular near to birth. We demonstrate that female mice experiencing novel males during late pregnancy also alter their investment in progeny, but in a more subtle manner than previously observed. Females exposed to an unfamiliar male during late pregnancy give birth to offspring of a comparable weight to those produced by females exposed to the paternal male, but these offspring grow more slowly over lactation. As a consequence, offspring from these females weigh less at weaning. Modification of their growth trajectory, however, allows these offspring to catch up to normal weights by adulthood. Thus, cues of unfamiliar males, and possibly their associated threat of infanticide, can produce more wide-ranging effects on maternal investment than previously recognized.

Perceived threats of infanticide reduce maternal allocation during lactation and lead to elevated oxidative damage in offspring

“…Our results support the prediction that the “late Bruce effect,” in which female mice exposed to a novel male late in pregnancy weaned at lower weights (Gale et al., ), may be due to a strategic reduction in maternal investment in lactation. It is notable that females exposed to a novel male's scent spent less time nursing pups than females exposed to the scent of their mate.…”

“…As in our previous study (Gale et al., ), the offspring of the females that were exposed to the novel male were smaller at the end of lactation, but they caught up in size by maturity. The catch‐up growth exhibited by the offspring coincides with the time after lactation when offspring begin to feed themselves on solid food.…”

“…The Bruce effect only occurs in mice if the female is exposed in early pregnancy, up to 4–5 days postmating (Bruce, ), before embryo implantation. We have shown that if female mice are exposed to an unfamiliar male in late pregnancy (approximately day 14), offspring are of comparable birthweight, but growth is slower over lactation, resulting in lighter weaning weights (Gale, Gibson, Brooks & Garratt, ) compared with controls. Following weaning however, the experimental offspring grew faster and caught up to the control offspring by the onset of adulthood.…”

Male‐mediated prenatal loss: Functions and mechanisms

“…In these species, the blastocyst is prevented from successful implantation after exposure to a nonsire male without the need for male aggression (see below). After successful implantation, however, laboratory experiments in these species have shown that exposure to a novel male no longer induces pregnancy failure, although it can cause a reduction in investment by females (e.g., smaller pups at birth) . All documented instances of male‐mediated implantation failure are more consistent with the Bruce effect than with feticide.…”

Transitions in paternal social status predict patterns of offspring growth and metabolic transcription

“…Mice are a useful organism to study transgenerational effects because development can be modified by both maternal (Mateo & Maestripieri, ) and paternal (Rando, ) inputs. Maternal and paternal effects are often detected as a modulation of offspring growth rate during and after gestation (Gale, Gibson, Brooks, & Garratt, ; Grandjean et al, ; Mashoodh, Franks, Curley, & Champagne, ; McPherson, Owens, Fullston, & Lane, ). Converging evidence suggests that these parental effects are mediated in part by reprogramming of metabolic transcription, particularly in the liver (Rando & Simmons, ).…”