Sperm pre-fertilization thermal environment shapes offspring phenotype and performance

Abstract

The sperm pre-fertilization environment has recently been suggested to mediate remarkable transgenerational consequences for offspring phenotype (transgenerational plasticity, TGB), but the adaptive significance of the process has remained unclear. Here, we studied the transgenerational effects of sperm pre-fertilization thermal environment in a cold-adapted salmonid, the European whitefish (Coregonus lavaretus). We used a full-factorial breeding design where the eggs of five females were fertilized with the milt of 10 males that had been pre-incubated at two different temperatures (3.5°C and 6.5°C) for 15 h prior to fertilization. Thermal manipulation did not affect sperm motility, cell size, fertilization success or embryo mortality. However, offspring that were fertilized with 6.5°C-exposed milt were smaller and had poorer swimming performance than their full-siblings that had been fertilized with the 3.5°C-exposed milt. Furthermore, the effect of milt treatment on embryo mortality varied among different females (treatment×female interaction) and male–female combinations (treatment×female×male interaction). Together, these results indicate that sperm pre-fertilization thermal environment shapes offspring phenotype and post-hatching performance and modifies both the magnitude of female (dam) effects and the compatibility of the gametes. Generally, our results suggest that short-term changes in sperm thermal conditions may have negative impact for offspring fitness. Thus, sperm thermal environment may have an important role in determining the adaptation potential of organisms to climate change. Detailed mechanism(s) behind our findings require further attention.