Life history costs of olfactory status signalling in mice

Gosling, L. M.; Roberts, S. Craig; Thornton, Emma; Andrew, Mark

doi:10.1007/s002650000242

Cited by 97 publications

(86 citation statements)

References 31 publications

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“…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.…”

mentioning

confidence: 97%

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

Nelson

Cauceglia

Merkley

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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When brought into captivity, wild animals can adapt to domestication within 10 generations. Such adaptations may decrease fitness in natural conditions. Many selective pressures are disrupted in captivity, including social behavioral networks. Although lack of sociality in captivity appears to mediate domestication, the underlying mechanisms are not well understood. Additionally, determining the contribution of genetic inheritance vs. transgenerational effects during relaxed selection may provide insight into the flexibility of adaptation. When wild-derived mice kept under laboratory conditions for eight generations were reintroduced to sociality and promiscuity (free mate choice), they adapted within two generations. Fitness assessments between this promiscuous lineage and a monogamous laboratory lineage revealed malespecific effects. Promiscuous-line males had deficits in viability, but a striking advantage in attracting mates, and their scent marks were also more attractive to females. Here, we investigate mechanistic details underlying this olfactory signal and identify a role of major urinary protein (MUP) pheromones. Promiscuous-line males inherit higher MUP expression than monogamous-line males through transgenerational inheritance. Sociality-driven maternal and paternal effects reveal intriguing conflicts among parents and offspring over pheromone expression. MUP up-regulation is not driven by hormone-driven transduction pathways, but rather is associated with reduction in DNA methylation of a CpG dinucleotide in the promoter. This reduction in methylation could enhance transcription by promoting the binding of transcription factor USF1 (upstream stimulatory factor 1). Finally, we experimentally demonstrate that increased MUP expression is a female attractant. These results identify molecular mechanisms guiding domestication and adaptive responses to fluctuating sociality.social selection | sexy sons | epigenetics W ild animals bred in captivity have been observed to adapt to domestication within 10 generations (1-4). As a result, captive bred animals often have reduced fitness when reintroduced to natural conditions (5). Selective pressures disrupted by captivity include inbreeding avoidance, effective population size, disease exposure, predation, and sexual selection. For the latter example, evidence suggests that lack of social context for mate choice mediates adaptation to captivity (6). This context is especially relevant for social animals because the opportunity for mating success is regulated by hierarchical behavioral networks (i.e., social selection) (7), and this information is missing in captivity. The molecular mechanisms underlying phenotypes affected by lack of social selection are poorly understood. Furthermore, rapid adaptation to captivity raises questions about the roles of genetic inheritance vs. transgenerational effects (i.e., inheritance independent of genetic variation) (8). Resolving the mechanistic and hereditary basis of these transitions can provide insight into the flexibilit...

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mentioning

confidence: 97%

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

Nelson

Cauceglia

Merkley

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…This indicates that males from enlarged litters in the current study might be reaching sexual maturity at a younger age and contributing more resources toward reproductive investment than those from reduced litters. Gosling et al (2000) suggested that smaller male lab mice can maintain dominance over larger males by investing more in olfactory signalling and increased preputial gland mass. This investment appeared to come at a cost, however, because these originally small males had a slower growth rate.…”

Section: Liver Kidneysmentioning

confidence: 99%

Experimental evidence that litter size imposes an oxidative challenge to offspring

Gibson

Garratt

Brooks

2015

Journal of Experimental Biology

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The post-natal environment in which young develop can substantially impact development, adult phenotype and fitness. In wild mice, competition among litter-mates affects development rate and adult behaviour. We manipulated post-natal litter size in a cross-fostering design to investigate the effects of enlarged and reduced litter sizes on sexual signalling, oxidative stress and the links between them. Oxidative stress causes somatic damage that can limit reproductive success and lifespan, and is predicted to mediate investment in life-history traits, including sexual signals. We predicted that litter enlargement would cause an increase in potential oxidative stress, inhibit growth and reduce sexual signalling in male mice. Males reared in enlarged litters were smaller at weaning and, despite rapid growth immediately after weaning, remained smaller at 10 weeks of age than those reared in smaller litters. Females from enlarged litters were consistently smaller throughout post-weaning development and showed no increase in growth rate compared with females from reduced litters. In enlarged litters, protein thiol concentration was lower at weaning in the liver and kidneys, with this trend continuing at 10 weeks of age in the kidneys only. Aconitase enzyme activity was also lower in mice from enlarged litters at weaning and 10 weeks of age in the kidneys. Male mice from enlarged litters scent marked more frequently and had larger preputial glands than those from reduced litters, indicating greater sexual signalling investment irrespective of this increased oxidative challenge. The results of this study are the first to reveal oxidative costs of developmental stress in small mammals.

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“…In male mammals, reproductive behaviors that increase activity levels, such as mate guarding and scramble competition, often have substantial energetic costs, often more than doubling resting energy demands and sometimes exceeding the costs of lactation for females (32). It seems more likely that the elevated behavioral investment in scent-marking and patrolling of their home area for territorial males in this experiment may have been energetically costly, facilitating the reduction in body mass observed in this experiment and previously reported (30). We observed no differences between genotypes for this behavior, although we cannot exclude the possibility that SOD1 deficiency may influence scent-marking in a more subtle manner which was undetectable in our assay.…”

Section: Discussionmentioning

confidence: 46%

“…It has been suggested that the production of MUPs may be energetically costly (30), but the synthesis of these proteins actually makes up a small amount of a mouse's total energy budget. Estimates of the energy costs of protein synthesis range between 3 and 20 kj/g protein (31).…”

Section: Discussionmentioning

confidence: 99%

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

Garratt¹,

Pichaud²,

Glaros

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Oxidative stress (an overproduction of reactive oxygen species in relation to defense mechanisms) may restrict investment in life history traits, such as growth, reproduction, lifespan, and the production of sexual signals to attract mates. The constraint on sexual signaling by oxidative stress is of particular interest because it has been proposed as a mechanism ensuring that only good-quality males produce the most attractive sexual signals. Despite these predictions, evidence supporting this theory is, at best, equivocal. We used a superoxide dismutase knockout mouse to demonstrate that oxidative stress directly impairs investment in morphological (preputial glands) and molecular (major urinary proteins) components of olfactory signaling essential for mate attraction. By maintaining males in a much more competitive environment than usual for mouse laboratory experiments, we also revealed a range of phenotypes of superoxide dismutase deficiency not observed in previous studies of this mouse model. This range included impaired bioenergetic function, which was undetectable in the control environment of this study. We urge further examination of model organisms in seminatural conditions and more competitive laboratory environments, as important phenotypes can be exposed under these more demanding conditions.L ife history theory is based on the premise that physiological constraints limit investment in life history components. These constraints are expected to generate the negative correlations commonly observed between these traits on an interspecies level (1). Within species, individuals also differ in their capacity to invest in different traits (2), although the physiological causes of this variation remain largely elusive.Oxidative stress occurs as a consequence of an overproduction of reactive oxygen species (ROS) in relation to defense mechanisms (3). Because ROS are produced as a by-product of oxidative phosphorylation, investment in energetically demanding life history traits has been predicted to increase oxidative stress, which may then constrain investment in other areas (4, 5). Ecological research in wild animals has provided correlative evidence for a link between oxidative stress and investment in traits, such as growth (6), reproduction (7,8), and lifespan (7). Early evidence linking oxidative stress to variation in lifespan within (9) and between species (10) led to the development of genetically modified antioxidant enzyme knockout animals, allowing precise tests of the effects of these pathways on lifespan under controlled laboratory conditions (11). These tests concluded that oxidative stress does not play a major role in governing the lifespan of laboratory animals (11).As in the case of lifespan, sexual signals show considerable among-individual variation and can correlate with oxidative stress. Sexual signals are often condition-dependent in expression, such that only good-quality signalers express the largest or most elaborate sexual signals (12). These signaling systems only evolve and rem...

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Life history costs of olfactory status signalling in mice

Cited by 97 publications

References 31 publications

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

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

Experimental evidence that litter size imposes an oxidative challenge to offspring

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

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