The evolutionary ecology of pre- and post-meiotic sperm senescence Tom Pizzari 1 , Rebecca Dean 1 , Allan Pacey 2 , Harry Moore 2, 3 and Michael B. Bonsall 4 1 Edward Grey Institute, Department of Zoology, University of Oxford, Oxford, OX1 3PS, UK 2 Academic Unit of Reproductive and Developmental Medicine, University of Sheffield, Sheffield, S10 2SF, UK 3 Centre for Stem Cell Biology, Department of Molecular Biology and Biotechnology, University of Sheffield, Sheffield, S10 2TN, UK 4 Mathematical Ecology Research Group, Department of Zoology, University of Oxford, Oxford, OX1 3PS, UK Male reproductive success is an extremely variable fitness component. Understanding the maintenance of this variation is a key challenge in evolutionary biology. An often neglected source of variation in male reproduc- tive success is determined by age-dependent patterns of decline in sperm fitness. Two pathways mediate sperm senescence: pre-meiotic senescence of somatic and germ cells of the ageing male, and post-meiotic ageing of the spermatozoon. Recently, theoretical and empirical stu- dies have highlighted wide-ranging implications of both pathways. We clarify different mechanisms of sperm senescence, outlining their distinct evolutionary implica- tions for the male, the female and the zygote, and their influence on fundamental evolutionary processes, in- cluding the evolution of anisogamy, sexual conflict, sexual selection, and applied issues such as assisted conception. Introduction Reproductive ageing or senescence (see Glossary) is deter- mined by life-history trade-offs, evolutionary constraints on development and metabolism, and age-dependent selection [1–3]. Although senescence acting on individuals has been widely studied [4], growing interest has recently focused on the evolutionary and ecological repercussions that senes- cence might have for gametic performance and fitness. Different senescence mechanisms influence the probability that a sperm cell will fertilise an egg, and — if fertilisation does occur — the viability of the ensuing zygote, with drastically different implications on the fitness of individual sperm cells, the male parent, the inseminated female, and the zygote [5]. Here, we focus on these age-dependent declines in sperm fertilisation probability and offspring viability, which for simplicity we refer to as sperm senes- cence (see Glossary). Sperm senescence occurs at two levels: the organismal level, in the somatic and/or germ cells of a male before meiosis (pre-meiotic); and the gametic level, during and Review Glossary Ageing or senescence: an increase in mortality or a decline in fertility with advancing age. Theories of ageing predict that mechanisms of intrinsic damage lead to reduced somatic or reproductive function. Male reproductive senescence has attracted a number of ultimate explanations. For example, male ageing has been interpreted as an adaptation to reduce competition between fathers and offspring [69,70]. More recently, erectile dysfunction in ageing men has been interpreted as an adaptation to avoid fertilisation by old males [71]. These theories suffer two main problems. First, in most wild popu- lations, the contribution of male senescence to mortality might be limited. Second, these theories are based either on group selection arguments that are difficult to reconcile with selection at the individual level or on kin selection arguments that would apply under a very restricted set of conditions (e.g. organisms with limited or no dispersal and overlapping generations). Anisogamy: the production of discrete types of gametes of different size with small, mobile male gametes (sperm) fertilising large, nur- turing female gametes (eggs). Cryptic female choice: post-copulatory female driven mechanisms that bias the outcome of sperm competition in favour of the ejacu- lates of certain males. Glutathione S-transferases and glyoxylase detoxification systems: enzymes implicated in cellular protection against oxidative stress. Iteroparity: repeated production of offspring throughout the life cycle. Last-male sperm precedence: sperm competition dynamics in which the last male to inseminate a female enjoys a fertilising advantage over previous competitors. Pachytene: the meiotic stage at which chromosomal crossover occurs. Paternal effects: the genetic contribution of a male to its offspring. Reactive oxygen species: highly reactive molecules including oxygen ions, free radicals and peroxides, which are a natural byproduct of cellular oxygen metabolism and can damage cell structures. Sexual conflict: an evolutionary scenario in which the fitness interests of a male and a female cannot be met simultaneously. At a genetic level this can be mediated by sexually antagonistic alleles segregated at different loci (inter-locus) or at the same locus (intra-locus). Sexual selection: Darwinian selection acting on variance in mating and fertilisation success among members of the same sex, and promoting traits that confer an advantage in reproductive competition. It comprises intra- and inter-sexual selection episodes, leading to copulation (pre-copulatory) and fertilisation (post-copu- latory). Sperm competition: post-copulatory intra-sexual selection arising from the competition between the ejaculates from different males over the fertilisation of a set of eggs arising when females copulate with multiple males. Sperm senescence: in this article, we define sperm senescence as a decline in the ability of a sperm cell to fertilise an egg, and/or — when fertilisation occurs — a decline in the viability of the ensuing zygote that occurs with the advancing age of either the male (pre-meiotic sperm senescence) or of the sperm cell (post-meiotic). The reduction in fertilising efficiency can be due to changes in the morphology, metabolic performance and behaviour of the sperm cell, while the reduction in zygote viability is determined by deleterious mutations or damage to the DNA carried by the sperm. Telomerase: an enzyme that adds DNA sequence repeats to the telomeres. Corresponding author: Pizzari, T. (tommaso.pizzari@zoo.ox.ac.uk). 0169-5347/$ – see front matter ß 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2007.12.003 131