Effects of nutrient limitation on sperm and seminal fluid: a systematic review and meta‐analysis

Abstract

Theory predicts that costly sexual traits should be reduced when individuals are in poor condition (i.e. traits should exhibit condition‐dependent expression). It is therefore widely expected that male ejaculate traits, such as sperm and seminal fluid, will exhibit reduced quantity and quality when dietary nutrients are limited. However, reported patterns of ejaculate condition dependence are highly variable, and there has been no comprehensive synthesis of underlying sources of such variation in condition‐dependent responses. In particular, it remains unclear whether all ejaculate traits are equally sensitive to nutrient intake, and whether such traits are particularly sensitive to certain dietary nutrients, respond more strongly to nutrients during specific life stages, or respond more strongly in some taxonomic groups. We systematically reviewed these potential sources of variation through a meta‐analysis across 50 species of arthropods and vertebrates (from 71 papers and 348 effect sizes). We found that overall, ejaculate traits are moderately reduced when dietary nutrients are limited, but we also detected substantial variation in responses. Seminal fluid quantity was strongly and consistently condition dependent, while sperm quantity was moderately condition dependent. By contrast, aspects of sperm quality (particularly sperm viability and morphology) were less consistently reduced under nutrient limitation. Ejaculate traits tended to respond in a condition‐dependent manner to a wide range of dietary manipulations, especially to caloric and protein restriction. Finally, while all major taxa for which sufficient data exist (i.e. arthropods, mammals, fish) showed condition dependence of ejaculate traits, we detected some taxonomic differences in the life stage that is most sensitive to nutrient limitation, and in the degree of condition dependence of specific ejaculate traits. Together, these biologically relevant factors accounted for nearly 20% of the total variance in ejaculate responses to nutrient limitation. Interestingly, body size showed considerably stronger condition‐dependent responses compared to ejaculate traits, suggesting that ejaculate trait expression may be strongly canalised to protect important reproductive functions, or that the cost of producing an ejaculate is relatively low. Taken together, our findings show that condition‐dependence of ejaculate traits is taxonomically widespread, but there are also many interesting, biologically relevant sources of variation that require further investigation. In particular, further research is needed to understand the differences in selective pressures that result in differential patterns of ejaculate condition dependence across taxa and ejaculate traits.

Sperm and alternative reproductive tactics: a review of existing theory and empirical data

“…ART game theory models [9,11,16] can also be expanded by relaxing the assumption of equal reproductive budgets between sneakers and dominant males ( figure 1b,c). We know theoretically [76] and empirically [77,78] that ejaculate traits are influenced by male condition, independent of sperm competition risk. In many species with conditiondependent ARTs, sneaker males tend to be of lower quality [3], in which case they may have a smaller reproductive budget and lower sperm quality even if they have higher relative ejaculate expenditure ( figure 1c).…”

Influences of male age, mating history and starvation on female post mating aggression and feeding inDrosophila

“…Male ejaculates, however, are not uniform across individuals or time (Bretman, Fricke, & Chapman, 2009; Johnson & Gemmell, 2012; Macartney, Crean, Nakagawa, & Bonduriansky, 2019). Ejaculate component expression appears to be costly, suggesting it is condition-dependent, and males in a population can vary substantially in characteristics that may alter their ejaculate (Linklater, Wertheim, Wigby, & Chapman, 2007; Macartney et al, 2019; Perry et al, 2013). External social and ecological factors can determine how much males invest in their ejaculates.…”

“…A male’s individual condition is also critical for determining males’ ability to produce and transfer ejaculates. Intrinsic factors such as age, mating activity, and diet have all been shown to influence male ejaculate quality, quantity and composition, impacting both male and female fitness (Fricke, Bretman, & Chapman, 2008; Macartney et al, 2019; Sepil et al, 2020). In both vertebrate and invertebrate taxa, older males tend to transfer smaller or lower quality ejaculates, leading to a decline in fertility or offspring fitness (Dean et al, 2010; Preston, Saint Jalme, Hingrat, Lacroix, & Sorci, 2015; Ruhmann, Koppik, Wolfner, & Fricke, 2018).…”

“…Similarly, diet-induced changes in male ejaculates are common across taxa. When nutrients are limited, males have both reduced seminal fluid and sperm quantities, leading to reduced fertility or offspring survival (Macartney et al, 2019). Reductions in ejaculate quality mediated by male condition can therefore have important fitness consequences for females (Dean et al, 2010).…”

“…Here we use the fruit fly Drosophila melanogaster to test how variation in three male traits known to influence ejaculate characteristics affect an important female post-mating behaviour – female aggression. We chose male age, mating history, and adult feeding status as our male traits, as all three characters are related to male condition and have been shown to strongly influence some aspect of the ejaculate in D. melanogaster and other species (Fricke et al, 2008; Macartney et al, 2019; Sepil et al, 2020). In D. melanogaster , male reproductive function declines with age, but this is heavily dependent on male sexual activity and differs for different ejaculate components.…”