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The role of ageing in the maintenance of variability in male reproductive success

Final Report Summary - AGEING AND RS (The role of ageing in the maintenance of variability in male reproductive success)

Sexual selection is expected to generate intense directional selection on pre- and post-copulatory traits, however such traits typically exhibit considerable variation. This presents a paradox because directional selection is expected to progressively erode genetic variation in sexually-selected traits by driving them to fixation. Understanding how variance in male reproductive success is maintained, despite persistent directional selection for certain phenotypes, constitutes one of the major challenges in evolutionary biology. An increasing body of work shows that senescence is a biologically relevant evolutionary force, but its consequences at an evolutionary level remain poorly understood as it is a surprisingly under-investigated source of variation in male reproductive success. The main aim of this project was to study the role of ageing in the maintenance of the variability in male reproductive success using an internal fertilising fish (the guppy, Poecilia reticulata) as a model species.

The experiments conducted in this project were designed to investigate the effects of (i) sperm ageing and (ii) male ageing on traits associated with male reproductive success with a specific focus on postcopulatory traits. Findings revealed that sperm ageing (the ageing of sperm inside male’s body due for example to a prolonged sexual rest or low female availability) influences both sperm performance (specifically sperm swimming speed) and competitive fertilization ability but do not affect fertilization in non-competitive conditions (i.e. in absence of sperm competition). Sperm ageing also resulted in trans-generational effects on offspring fitness, with sons produced by females fertilized by aged sperm producing sperm with slow swimming velocity, suggesting that the effects due to sperm ageing are non-transient and impact the reproductive potential of male offspring, creating the potential for an evolutionary conflict between the sexes. This latter finding is particularly interesting not only in the context of sperm ageing, but because of its significance as first evidence of paternal effect on offspring reproductive fitness mediated solely by sperm condition.
In addition, a longitudinal study looking simultaneously at male and sperm ageing has been conducted to reveal the interplay between reproduction, ageing and somatic maintenance. Preliminary results on this part or the project revealed that the interaction between ageing at organism level and at gametic level impacts male’s reproductive success contributing in maintaining variation in male’s reproductive success.

In summary, this project has achieved its objectives and extended our understanding of evolutionary consequences of senescence, revealing how ageing of both males and their sperm has deep negative impacts on multiple aspect of a male reproductive fitness.