Condition dependent seminal fluid gene expression and intergenerational paternal effects on ejaculate quality

1. There is increasing evidence to show that the environment experienced by fathers can have intergenerational paternal effects on the phenotype of offspring. Paternal effects can be mediated by ejaculate traits beyond the genes carried by sperm, for example through methylation of DNA during spermatogenesis, or non-sperm components of the ejaculate such as small RNAs or seminal fluid proteins (sfp). 2. Theory suggests that ejaculate-mediated paternal effects can have important evolutionary consequences, especially if they exhibit condition dependent expression. Here we use the nutritional geometry approach to explore condition dependence in ejaculate traits and intergenerational paternal effects in the cricket Teleogryllus oceanicus. 3. We fed males one of 24 chemically defined diets that varied in macronutrient concentration and the ratio of protein (P) to carbohydrate (C). We measured paternal expenditure on testes and accessory gland growth, and the expression of three seminal fluid protein genes that are known to impact sperm viability and the survival of embryos to hatching. We also measured the hatching success and reproductive phenotypes of adult offspring. 4. We found linear effects of P and C on testes and accessory gland mass, and linear and correlated effects of P and C on the expression of two sfp genes. Paternal diet had no effect on the survival of embryos to hatching. 5. There were significant intergenerational effects of paternal diet on the viability of sperm produced by sons, but no paternal effects on the expression of sfp genes in sons or fecundity in daughters. 6. Our data suggest that ejaculate quality can have a significant non-genetic component determined by the paternal environment, which holds important implications for the evolutionary maintenance of variation in heritable male fitness.

1. 越来越多的证据表明，父本所处的环境可对子代表型产生跨代父本效应。父本效应可通过精子携带基因以外的精液性状介导，例如精子发生过程中的DNA甲基化，或精液中非精子组分（如小分子RNA或精液蛋白（seminal fluid proteins, sfp））。
2. 理论研究显示，由精液介导的父本效应可产生重要的进化后果，尤其当这类效应表现出条件依赖表达时。本研究采用营养几何模型方法，以大洋洲蟋（Teleogryllus oceanicus）为研究对象，探究精液性状的条件依赖性以及跨代父本效应。
3. 我们为雄性个体喂食24种化学成分明确的日粮中的一种，各日粮的宏营养素浓度以及蛋白质（P）与碳水化合物（C）之比各不相同。我们测定了父本在睾丸和附腺发育上的资源投入，以及3种已知可影响精子活力与胚胎孵化存活率的精液蛋白基因的表达水平；同时还测定了子代的孵化成功率以及成年个体的生殖表型。
4. 研究发现，蛋白质与碳水化合物的含量对睾丸和附腺重量存在线性影响，且二者对2种sfp基因的表达存在线性且相关的影响；父本日粮对胚胎的孵化存活率无显著作用。
5. 父本日粮对子代雄性个体产生的精子活力存在显著的跨代效应，但未对子代雄性的sfp基因表达以及子代雌性的繁殖力产生显著父本效应。
6. 本研究数据表明，精液质量存在由父本环境决定的重要非遗传组分，这一发现对可遗传雄性适合度变异的进化维持具有重要启示。