Sperm competition and fertilization mode in fishes

Abstract

Sperm competition is a powerful selective force that has shaped sexual traits throughout animal evolution. Yet, how fertilization mode (i.e. external versus internal fertilization) influences the scope and potential for sperm competition to act on ejaculates remains unclear. Here, I examine how fertilization mode shapes ejaculatory responses to sperm competition in fishes, a diverse group that constitute the majority of vertebrate biological diversity. Fishes are an ideal group for this examination because they exhibit a wide range of reproductive behaviours and an unparalleled number of transitions in fertilization mode compared to any other vertebrate group. Drawing on data from cartilaginous and bony fishes, I first show that rates of multiple paternity are higher in internally than externally fertilizing fishes, contrary to the prevailing expectation. I then summarize how sperm competition acts on sperm number and quality in internally and externally fertilizing fishes, highlighting where theoretical predictions differ between these groups. Differences in how ejaculates respond to sperm competition between fertilization modes are most apparent when considering sperm size and swimming performance. Clarifying how fertilization mode influences evolutionary responses in ejaculates will inform our understanding of ejaculate evolution across the animal tree of life. This article is part of the theme issue ‘Fifty years of sperm competition’.

Three decades of sperm competition in birds

“…Comparative studies of birds showed similar results to those found in insects [35] and fishes [36], wherein ejaculates of species with relatively large testes (thus higher levels of sperm competition) contained fewer dead or deformed sperm, but also sperm that were longer, more consistent in size and morphology within an ejaculate and with a higher swimming velocity [37]. In the zebra finch, a species with relatively low levels of EPP, sperm length varies markedly from male to male (40-80 µm [38]).…”

Fertilization modes drive the evolution of sperm traits in Baikal sculpins

“…First, multiple paternity is evident in many viviparous teleosts (Avise & Liu, 2010, 2011), including marine copulatory sculpins (Uematsu, 2016). A recent review also shows that the rates of multiple paternity are higher in internally than externally fertilizing fish (Fitzpatrick, 2020). Second, the population of Comephorus is among the most abundant fishes in Lake Baikal (Starikov, 1977; Sideleva, 1994, 2011), and higher population densities show higher multiple paternity rates than lower population densities in internally fertilizing fishes (Soucy & Travis, 2003; Liu et al ., 2013).…”

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

“…Many of these chapters were prospective of the potential for sperm competition to operate in diverse taxonomic groups, providing ideas for the future development of research into postmating sexual selection across the animal kingdom. While many of the taxon-focused reviews in Smith were short on empirical support, the contributions to this themed issue now provide overwhelming empirical evidence that postmating sexual selection is responsible for the widespread evolution of behaviour, morphology and physiology among spiders [46], fishes [47], reptiles [48], birds [49] and mammals [50].…”