The scent of senescence: sexual signalling and female preference in house mice

Abstract

Sexual signals are expected to be costly to produce and maintain, thus ensuring that only males in good condition can sustain their expression at high levels. When males reach senescence they lose physiological function and condition, which could constrain their ability to invest in costly sexual signals, decreasing their attractiveness to mates. Furthermore, females may have evolved mating preferences that cause avoidance of senesced males to enhance fertilization success and viability of offspring. Among mammals, the size of antlers and other weapons can decrease with senescence, but changes in olfactory sexual signals have been largely unexplored. We examined changes in olfactory signals with senescence in house mice (Mus musculus domesticus), where males excrete volatile and involatile molecules in scent marks that elicit behavioural and priming responses in females. Compared to middle‐aged males, the urine of senesced males contained a lower concentration of involatile signalling proteins (major urinary proteins or MUPs), and associated volatiles that bind to these proteins. The reduced intensity of male scent will affect the longevity of scent signals deposited in the environment and, accordingly, females were less attracted to urine from senesced males deposited 12 h previously. Females also discriminated against senesced males encountered behind a mesh barrier. These results reveal that investment in olfactory signalling is reduced during senescence and suggest that senesced males and their scent may be less attractive to females.

Female attraction to male scent and associative learning: the house mouse as a mammalian model

“…Investment in MUPs and associated volatile ligands declines as adult males start to age; urinary protein levels start to decline when wild-stock males (housed singly in the laboratory) are >18 months old, declining to approximately one-third of the amount excreted by younger adult males once males are aged 25e32 months (Garratt, Stockley, Armstrong, Beynon, & Hurst, 2011). This decline in urinary protein correlates strongly with the decline in epididymal sperm counts as males start to senesce.…”

“…However, in most cases scent marks are not likely to be encountered very soon after deposition. As scent marks age and the abundance of volatiles declines, the amount of 2-sec-butyl-4,5-dihydrothiazole (an androgen-dependent volatile that binds largely to darcin) in senesced male urine after 4 h is equivalent to that in younger adult male urine after 8e12 h. Given a choice between urine marks 12 h after deposition, females are significantly less attracted to investigate those from a senesced adult male where the emission of volatiles is now extremely weak (Garratt et al, 2011). As yet, we have limited understanding of the temporal dynamics of scent marks (e.g.…”

Reintroducing domesticated wild mice to sociality induces adaptive transgenerational effects on MUP expression

“…Several researchers have proposed that such expression is a result of sexual selection. This "honest-signal" model predicts that females favor males who can afford high expression despite potential costs (e.g., protein loss or attracting predators and competitors) (18)(19)(20)(21)(22). Although this hypothesis has not been explicitly tested, the observation that MUP concentration declines as mice adapt to captivity (17,23) suggests a possible role of relaxed social and sexual selection.…”

Superoxide dismutase deficiency impairs olfactory sexual signaling and alters bioenergetic function in mice

“…Urine samples were collected from males at the end of the habituation period and in the final week of the experiment. Total urinary protein levels were assessed with the Coomassie assay, which reflects total urinary MUP concentration, and were corrected for urinary dilution by measuring urinary creatinine levels (20). Scent-marking rates were assessed at the same periods, but on 2 separate days that did not coincide with urine collection, by placing a piece of benchkote (30 × 8 cm) in each male's cage for a 2-h period.…”

“…Reductions in various aspects of olfactory signaling occur with senescence, and are correlated with reduced attractiveness of old male scent. It has been tentatively suggested that oxidative stress could be linked to this reduced sexual signaling with age (20). We started by examining the ability of homozygous, fully deficient Sod1 mice (Sod1 −/− mice) to scent-mark a territory area with urine and invest in various molecular and morphological scent signaling components with established roles in female attraction.…”