Sperm competition and the evolution of reproductive systems

Abstract

In this issue, we present four New Research Horizon Reviews on a single theme: sperm competition. I therefore first want to clarify exactly what sperm competition is, and explain why we think it is an important factor for the readership of Molecular Human Reproduction to consider. Sperm competition occurs whenever sperm from two or more males compete to fertilize a given set of ova (Parker, 1970, 1998). Because female promiscuity is a common occurrence in the animal kingdom, sperm competition is recognized by evolutionary biologists as a major force acting on many aspects of reproductive anatomy, physiology and behaviour (see for example Birkhead and Moller, 1998; Birkhead et al., 2009), including during the evolutionary history of humans (Leivers and Simmons, 2014). Males who do better in sperm competition (or do better at avoiding it) will tend to leave more offspring, and over evolutionary time the sorts of traits that increase a male’s sperm competitive ability will therefore tend to increase in frequency. Turning this around, we can expect that many of the features of male reproduction we observe today have been shaped by sperm competition, and it is this premise we explore throughout the four reviews. Why, though, should a molecular reproductive biologist care about sperm competition and related evolutionary ideas? The principal motivation for presenting this series stems from the recognition that as evolutionary biologists we are often deeply interested in reproduction (reproductive success is after all what determines an organism’s evolutionary fitness), and yet the research we pursue usually occurs in complete isolation from reproductive biologists. In part this may be due to the fact we are coming at the problem from slightly different angles: on the one hand addressing ‘ultimate’ questions of why reproductive systems are the way they are, and on the other ‘proximate’ ones about how those reproductive systems actually work. Nevertheless, a strict separation of reproductive research in this manner (our own ‘two cultures’?) represents something of a missed opportunity, since we could undoubtedly learn a lot from each other. The aim in compiling the series has therefore been to try to bridge this divide, with each author team taking one of four different aspects of reproduction that will already be familiar to the audience of MHR, but then re-examining it in the light of the latest evolutionary research and ideas in the hope of providing a fresh perspective and fostering a deeper understanding. As a starting point, an obvious feature of human reproduction— perhaps so obvious as to at first appear trivial—is that it involves the fusion of two distinct gamete types, a sperm and an egg. However, the phenomenon of gametes competing over fertilization (what would ultimately ‘become’ sperm competition) actually precedes the origin of these two different gamete types. Not only that, but the very reason we now normally have two types—that is, the evolution of anisogamy generating sperm and eggs—may to a large extent derive from just this competition over fertilization. In the first review in the series, Lehtonen and Parker (2014) therefore take us through the evolutionary steps involved in the evolution of anisogamy, and demonstrate that this fundamental transition provides the fuel for the cascade of evolutionary events that now make half of us ‘male’ and half of us ‘female’ (Lehtonen and Parker, 2014; see also Parker, 2014; Parker and Lehtonen, 2014).