The evolutionary ecology of testicular function: size isn't everything

Abstract

Larger testes are considered the quintessential adaptation to sperm competition. However, the strong focus on testis size in evolutionary research risks ignoring other potentially adaptive features of testicular function, many of which will also be shaped by post-mating sexual selection. Here we advocate a more integrated research programme that simultaneously takes into account the developmental machinery of spermatogenesis and the various selection pressures that act on this machinery and its products. The testis is a complex organ, and so we begin by outlining how we can think about the evolution of testicular function both in terms of the composition and spatial organisation of the testis ('testicular histology'), as well as in terms of the logical organisation of cell division during spermatogenesis ('testicular architecture'). We then apply these concepts to ask which aspects of testicular function we can expect to be shaped by post-mating sexual selection. We first assess the impact of selection on those traits most strongly associated with sperm competition, namely the number and kind of sperm produced. A broad range of studies now support our contention that post-mating sexual selection affects many aspects of testicular function besides gross testis size, for example, to maximise spermatogenic efficiency or to enable the production of particular sperm morphologies. We then broaden our focus to ask how testicular function is affected by fluctuation in sperm demand. Such fluctuation can occur over an individual's lifetime (for example due to seasonality in reproduction) and may select for particular types of testicular histology and architecture depending on the particular reproductive ecology of the species in question. Fluctuation in sperm demand also occurs over evolutionary time, due to shifts in the mating system, and this may have various consequences for testicular function, for example on rates of proliferation-induced mutation and for dealing with intragenomic conflict. We end by suggesting additional approaches that could be applied to study testicular function, and conclude that simultaneously considering the machinery, products and scheduling of spermatogenesis will be crucial as we seek to understand more fully the evolution of this most fundamental of male reproductive traits.

Differences and similarities between extremely severe oligozoospermia and cryptozoospermia in intracytoplasmic sperm injection

“…A lot of comparative studies considered that relative testis size and sperm production were strongly correlated, and testis size would be a useful means of evaluating a male investment in sperm production 8. Compared to European and American people, testicular volumes of 13 ml in OA seemed to be atrophic in our study, but the testicular volumes of normal men also were 13 ml averagely (data not showed).…”

Population density and structure drive differential investment in pre- and postmating sexual traits in frogs

“…Although we cannot currently draw any firm conclusions as to the exact reasons for these positive associations, there are at least three potential and nonmutually exclusive explanations. Therefore, larger testes might be better at replenishing sperm reserves (Ramm and Schärer 2014). Because testosterone is secreted by the Leydig cells in the interstitial tissue of the testes (Jorgensen 1992), relatively large testes may be able to produce more testosterone.…”

“…However, mating success does not guarantee reproductive success: When females mate with multiple males during a reproductive period, the temporal and spatial overlap between ejaculates incites competition for fertilization among them and potentially enables females to bias fertilization success toward one or the other ejaculate, thereby extending both intra-and intersexual selection beyond copulation (Parker 1970;Eberhard 1996). Due to their intimate link to competitive fertilization success, sperm quantity and quality are particularly evident targets of postcopulatory sexual selection (Snook 2005;Gomendio et al 2006;Pizzari and Parker 2009;Simmons and Fitzpatrick 2012;Lüpold 2013;Fitzpatrick and Lüpold 2014), as are the size and efficiency of the testes that produce these sperm (Harcourt et al 1981;Byrne et al 2002;Lüpold et al 2009Lüpold et al , 2011Soulsbury 2010;Ramm and Schärer 2014;Parker 2016).…”

Altitude underlies variation in the mating system, somatic condition, and investment in reproductive traits in male Asian grass frogs (Fejervarya limnocharis)

“…In either case, the likely target of selection is the sperm-production capacity, which can be increased by enlarging testes and/or their efficiency (Parker and Pizzari 2010;Vahed and Parker 2012;Ramm and Schärer 2014).…”