Fifty years of sperm competition: the structure of a scientific revolution

Kuhn [1] recognized that scientific advances aremade through periods of ‘normal science’ and ‘revolutionary science’. During periods of normal science researchers explore their field through a series of experimental tests that challenge the central dogma of an existing paradigm. Occasionally someone might proffer a new way of thinking. Sometimes this will be countered by the findings of ‘normal science’. Rarely, it can result in a scientific revolution in which a new paradigm is established and our understanding of the natural world takes a quantum leap forward. Geoff Parker’s [2] insight into the evolutionary consequences of sperm competition 50 years ago was nothing short of a scientific revolution. For a new paradigm to become established, Kuhn [1] argued that it must preserve a large part of the accumulated knowledge that has already accrued, it must resolve some generally recognized problem that can be met in no other way, and it must have significant promise for future problem-solving. As part of his own scientific revolution, Darwin [3] had made a case for sexual selection being responsible for the evolution of exaggerated secondary sexual traits in males, because of the advantages they gave some individuals over others in competition for access to mating opportunities. Darwin saw sexual selection acting mostly on males through direct competition for access to females, and through female choice of elaborately adorned males. Darwinian sexual selection thereby acted through variation in mating success. Though Darwin may have been aware that the females of many species mate with multiple males with implications for paternity [4], he nevertheless failed to recognize that sexual selection could continue aftermating. Prior to 1970, research on poeciliid fishes [5] andDrosophila [6] had revealed how females mate with and store sperm from multiple males, and produced broods of mixed paternity. Seminal fluid peptides had been discovered and their effect on the reproductive behaviour and physiology of females documented [7–9]. Even the term ‘sperm competition’ had been coined in several reports of multiple paternity [10–12], and as far back as 1693 John Ray had asked why males should produce so many sperm [4]. Despite the knowledge accumulated on premating sexual selection, therewas a problem; contrary to Darwin, single mating by females could no longer be assumed. As a graduate student in the 1960s, Geoff Parker’s analysis of the reproductive behaviour and ecologyof theyellowdungfly [13] led him to the realization that selection arising frommultiplemating by females could explain the hitherto puzzling array of traits such as ejaculate peptides, mating plugs and extended ‘passive phases’ that occurred after mating, because these traits would promote a male’s fertilization success when in competition with the sperm of rivals. In laying down his reasoning in Sperm competition and its evolutionary consequences in the insects [2], Parker initiated a paradigm shift in our understanding of postmating sexual selection that has since developed into a mature research discipline [14].