Oviductal fluid counterbalances the negative effect of high temperature on sperm in an ectotherm model

Abstract

Global warming is affecting biodiversity; however, the extent to which animal reproductive processes respond to predicted temperature increments remains largely unexplored. The thermal environment has a pronounced impact on metabolic rates of ectotherms; therefore, an interesting question to assess is whether temperature increase might affect specific reproductive mechanisms like sperm performance in ectotherms. Moreover, in many species, oviductal fluid (OF) is known to regulate and maintain sperm quality; however, the role of oviductal fluid in relation to the effects of high temperature on sperm remains unclear. Our aim was to experimentally test the effect of increased temperature on sperm velocity, swimming path and percentage of motility in neutral conditions at ejaculation (without OF) and in femalés reproductive tract fluid (with OF), in a social ectotherm lizard model, Tropidurus spinulosus, which has specific thermal requirements for reproduction. Our results suggest that a rising temperature associated with global warming (+4°C) affects negatively sperm dynamics and survival. However, OF fluid ameliorated the harmful effects of high temperature. This is an important point, as this study is the first that ever tested the role of OF to preserve sperm from a warmer pre-fertilization environment. These results contribute to our understanding of how thermal environment changes might affect post-copulatory reproductive mechanisms.

The Physiological and Evolutionary Ecology of Sperm Thermal Performance

“…For example, oviductal fluid extracted from females reduced the negative effect of high incubation temperature on sperm in spiny lava lizards ( Tropidurus spinulosus ). Specifically, sperm incubated at high temperature with oviductal fluid had significantly higher motility and velocity compared to those without oviductal fluid ( Rossi et al, 2021 ).…”

“…Available evidence is broadly consistent in ectotherms ( Sales et al, 2018 ). For example, decreased motility and velocity of ejaculated sperm at high temperature has been observed in lizards ( Rossi et al, 2021 ) and snakes ( Tourmente et al, 2011 ).…”

“…An important consideration when analyzing the performance of ejaculated sperm in internal fertilizers is the influence of the female reproductive tract. The female reproductive system interacts with sperm and influences sperm performance and fertilization success by dictating the physical and chemical environment that sperm experience ( Pitnick et al, 2009 ; Rosengrave et al, 2009 ; Sasanami et al, 2013 ; Lüpold and Pitnick, 2018 ; Rossi et al, 2021 ). Though rarely studied, available evidence suggests this interaction is important for sperm thermal performance.…”

“…Ejaculated sperm stored within the female reproductive system can still be effected by temperature. In the spiny lizard example, the performance of sperm incubated with oviductal fluid still decreased at high temperature ( Rossi et al, 2021 ). Indirect evidence for limits on female capacity to buffer sperm from high temperature damage is found in a study of the red flour beetle ( T. castaneum ).…”

Evolutionary interactions between thermal ecology and sexual selection

“…For instance, when interactions among gametes occur within the female reproductive tract, thermoregulatory adaptations in females can influence the environment and outcomes of post‐copulatory competition (Kekäläinen & Evans, 2018; Reinhardt et al, 2015; Wang & Gunderson, 2022). Some females can bias fertilisations by allocating reproductive fluid to the sperm of specific males (Gasparini et al, 2020; Gasparini & Pilastro, 2011), but these reproductive fluids may only be effective at specific body temperatures (Rossi et al, 2021). Such cryptic mate choice mechanisms may therefore only evolve in lineages where females have already evolved specific thermal preference ranges.…”