Paternal‐effects in a terrestrial ectotherm are temperature dependent but no evidence for adaptive effects

Abstract

Global rising of average temperatures and increase in extreme climatic events may largely impact animal survival and reproduction. Yet, how variation in temperature may affect male fertility, in particular ejaculate traits, and whether this can in turn affect offspring fitness, is seldom addressed. Paternal effects may be of key importance as they could impact the rate and direction of evolutionary change in response to climate change. We tested the effects of temperature experienced by males on sperm traits, and asked whether the paternal environmental temperature affected offspring phenotype. We further explored the potential for paternal effects to be adaptive, which would occur when offspring fitness increased under the same environmental conditions experienced by the fathers. We exposed male field crickets to high or low temperatures at two life stages, either throughout development or as adults, and tested sperm traits (number and quality) and offspring fitness (hatching success and survival). We further assessed sperm traits in offspring, after they had also been exposed to the same or different temperature experienced by their father. We found that temperature affected sperm traits depending on the life‐stage of individuals. When the exposure was given during adulthood, males exposed to high temperature produced less sperm and of lower quality compared to males exposed to lower temperature, while if exposure was given during development, males exposed to high temperature produced more sperm and of better quality compared to males exposed to low temperatures. Offspring fitness was significantly affected by paternal temperature, evidence for anticipatory paternal effects on sperm traits was not found. Our study indicates that temperature can mediate cross‐generational effects, and that paternal effects may be mediated by changes in temperature and therefore much more widespread in nature than previously assumed. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13022/suppinfo is available for this article.

Ejaculate-mediated paternal effects: evidence, mechanisms and evolutionary implications

“…Within ecologically relevant boundaries, spermatozoa of some species can be remarkably tolerant to changes in temperature in terms of their absolute capacity to activate and fertilise oocytes. Nevertheless, there is evidence that changes in temperature experienced by males (or their ejaculates) prior to conception can have important implications for offspring fitness (Gasparini et al 2018, Kekäläinen et al 2018. Recent work suggests that epigenetic alterations to the germline may drive such effects.…”

The ecology of sexual conflict: Temperature variation in the social environment can drastically modulate male harm to females

“…In particular, sex peptides (SP) are harmful proteins that alter female fecundity and decrease their sexual receptivity, with important carry-over effects on their immunity, life span and fitness (Gioti et al, 2012;Perry et al, 2013;Wigby & Chapman, 2005). Studies conducted in other insects show that temperature can influence male fertility via damage to the testes and/ or sperm (Gasparini, Lu, Dingemanse Niels, & Tuni, 2017;Jørgensen, Sørensen, & Bundgaard, 2006;Lacoume, Bressac, & Chevrier, 2007;Nguyen, Bressac, & Chevrier, 2013;Rohmer, David, Moreteau, & Joly, 2004). Similarly, two studies in other Drosophilid species found that temperature affected sperm motility and fertility and ultimately caused partial sterility (Jørgensen et al, 2006;Rohmer et al, 2004).…”

Temperature as a modulator of sexual selection

“…For example, a recent study in the Mediterranean field cricket (Grillus bimaculatus) showed that 4ºC temperature differences (within the natural range of variation of the study population in the wild) significantly affected sperm production and quality. Males had higher sperm production and quality when they were exposed to hotter temperatures throughout development, but the opposite was true if they were exposed to hotter temperatures as adults (Gasparini et al, 2017). In addition, temperature also impacted on offspring fitness via effects on male sperm (i.e.…”

“…In most systems, we ignore whether cross-generational effects driven by paternal environment are driven by epigenetic mechanisms or mediated by other factors (e.g. direct or female-moderated paternal effects arising from variation in the nonsperm fraction of the ejaculate (Garcia-Gonzalez & Simmons, 2007;Gasparini et al, 2018)).…”