I see / smell / touch / hear and therefore I am: sex differences in perception alter survival and reproduction

The more we reproduce, the shorter we live. This stark maxim is supported by evidence gathered across decades from many different animals including humans. Females are particularly sensitive to the effects of elevated reproduction and in laboratory tests using insects, varying the amount of reproduction can decrease female length of life by up to a half, and even reverse which sex lives longest.

Despite all this study, we have a surprising lack of knowledge about the details of how these dramatic effects occur. Partly this is because many laboratory studies are done in a relatively homogenous environment in which exposure to potentially confounding effects of the same or opposite sex throughout life are minimised or even absent. It is becoming increasingly clear, however, that effects of the social and sexual environment can have dramatic effects on ageing. Hence a rich source of effects on the lifespan of each sex is missing from many studies that aim to identify ageing pathways.

Coupled with this, a new body of research is showing something really surprising: the role of perception itself on lifespan. For instance, the mere perception of same or opposite sex individuals, can have significant effects on survival and reproduction in a way that completely mimics actual exposure. Similar effects are observed in relation to the effect of the smell of food, versus actually eating it!

We propose to use the powerful fruitfly model system to investigate the importance and role of the perceptual effects of the social and sexual environment on lifespan, ageing and reproduction in both sexes. We also aim to show how these effects are linked to those of nutrient sensing genes that themselves have well-documented effects on lifespan.

We will do this in two parts:

1. By measuring the effect on the survival, ageing and reproductive success of each sex of varying the exposure of focal individuals of both sexes to: (i) same, opposite and both sex individuals, (ii) social and sexual groups of varying age, (iii) direct versus no direct contacts, (iv) blocked sensory inputs (smell, sound vision, touch), (v) blocked reproduction (sterile / fertile), (vi) 'danger', i.e. the presence of dead / live individuals. In addition, we will test the effects of candidate genes highlighted as important from previous research.
2. By measuring the effect of the manipulations in 1 on the expression of genes that sense how much and what has been eaten. We already know that such genes show a very different pattern of expression in males versus females and that this is changed when they initiate reproduction. By measuring how the manipulations employed in 1 change the activity of these genes in each sex we will be able to provide a direct link between perception of the expected level of reproduction, activation of nutrient sensing and ultimate lifespan. This will be confirmed by direct tests with candidate genes, that have been highlighted as key in mediating these effects

The work aims to provide important tests of why reproduction shortens life and speeds up ageing. It will also highlight the emerging importance of perceptual effects in determining lifespan and show how this might work. The research is expected to result in a major advance in our fundamental understanding of lifespan and ageing in each sex and will have direct relevance to studies on humans, given that many of the pathways we will be studying are shared with ourselves.

A major determinant of lifespan across many taxa is the level of reproductive activity. Decades of research has sought to unpick the underlying basis of these 'survival costs' of mating and reproduction, and to understand the mechanisms of sex-specificity. Despite this important work, the precise mechanisms of reproductive costs in both sexes remains surprisingly incomplete. This research programme aims to resolve this and proposes a model linking sex-specific perception of the social and sexual environment, via nutrient sensing, to lifespan, ageing and reproductive success.

Objective 1. To test how the social and sexual environment initiates the expression of sex-specific patterns of survival, ageing and reproductive success
(i) sex-specific lifespan, ageing and reproductive success. To test whether the manipulations of inputs to focal individuals alter the effect of those interactions on the trajectory of survival and reproductive success.
(ii) manipulation of base line social and sexual environments. To expose focal individuals of each sex to variation in the same and opposite sex environment.
(iii) manipulation of perception per se - entirely perceptual effects of same, opposite and both sex groups.
(iv) manipulation of sensory inputs - visual, auditory, tactile and pheromonal information.
(v) effect of reproductive potential - using germ-line lacking males and females.
(vi) effect of 'danger' - using exposure to dead non focal individuals.
(vii) effect of candidate perceptual mechanisms.

Objective 2. To test how the social and sexual environment of each sex shapes nutrient sensing pathways.
(i) patterns of sex biased gene expression in nutrient sensing genes.
(ii) effect of candidate nutrient sensing mechanisms.

The programme supports the 3Rs (replace, reduce, refine) through the deployment of the fruitfly model system, and will provide new fundamental information, highly relevant to human studies, of ageing mechanisms in males and females.