The Physiological and Evolutionary Ecology of Sperm Thermal Performance

Abstract

Ongoing anthropogenic climate change has increased attention on the ecological and evolutionary consequences of thermal variation. Most research in this field has focused on the physiology and behavior of diploid whole organisms. The thermal performance of haploid gamete stages directly tied to reproductive success has received comparatively little attention, especially in the context of the evolutionary ecology of wild (i.e., not domesticated) organisms. Here, we review evidence for the effects of temperature on sperm phenotypes, emphasizing data from wild organisms whenever possible. We find that temperature effects on sperm are pervasive, and that above normal temperatures in particular are detrimental. That said, there is evidence that sperm traits can evolve adaptively in response to temperature change, and that adaptive phenotypic plasticity in sperm traits is also possible. We place results in the context of thermal performance curves, and encourage this framework to be used as a guide for experimental design to maximize ecological relevance as well as the comparability of results across studies. We also highlight gaps in our understanding of sperm thermal performance that require attention to more fully understand thermal adaptation and the consequences of global change.

Evolutionary interactions between thermal ecology and sexual selection

“…In both ectotherms and endotherms, changes to an individual's body temperature can influence the number and quality of gametes that they produce (Parratt et al, 2021;Schou et al, 2021;van Heerwaarden & Sgrò, 2021;Wang & Gunderson, 2022). As a consequence, experiencing sublethal body temperatures can still substantially decrease individual-and population-level fitness.…”

“…However, studying how mate competition affects selection on the thermal sensitivity of fertility requires quantifying how temperature affects the fertility of individuals (Reinhardt et al, 2015). This could be accomplished by creating individual-level gamete thermal performance curves (Wang & Gunderson, 2022;Figure 1a) for the number of gametes produced, morphological indicators of gamete quality (e.g. sperm length and egg size), or gamete performance (e.g.…”

“…Post‐copulatory competition and the evolution of post‐copulatory sexual traits may be limited by an organism's thermal biology (Suzaki et al, 2018; Vasudeva et al, 2014). 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).…”

Duplicate genes as sources for rapid adaptive evolution of sperm under environmental pollution in tree sparrow

“…On the one hand, because of the close connection between male fertility and population growth, if sperm fails to adapt to the ever‐changing environment to buffer the detrimental effects caused by environmental change, a decrease in population fitness and subsequent population collapse will occur (Minnameyer et al, 2021; Walsh et al, 2019). On the other hand, the unique evolutionary feature of spermatozoa, which is that they undergo direct and strong selection such as sperm competition and cryptic female choice, gives sperm the capacity to evolve rapidly and provides hopes for adaptation to fast‐changing environments (Avidor‐Reiss, 2018; Birkhead & Pizzari, 2002; Wang & Gunderson, 2022). Several studies have found that sperm traits can evolve in a few generations to adapt to environmental stress (Breckels & Neff, 2014; Vasudeva et al, 2019).…”

Heat stress reveals a fertility debt owing to postcopulatory sexual selection

“…Climate warming and the incidence of heat waves is one of the most common and impactful consequences of anthropogenic environmental change (Bathiany et al, 2018;IPCC, 2022;Johnson et al, 2018;Varela et al, 2020), and male fertility is highly sensitive to increased temperatures (Chirgwin et al, 2021(Chirgwin et al, , 2020Iossa, 2019;Rodrigues et al, 2022;Sales et al, 2021;Vasudeva et al, 2019;Walsh et al, 2019;Wang and Gunderson, 2022). We therefore tested the general prediction that a history of strong sexual selection might lead to greater environmental sensitivity of male fertility by investigating how experimental evolution under different levels of natural and sexual selection affects the thermal sensitivity of fertility in the seed beetle, Callosobruchus maculatus, a model species for studies on postcopulatory sexual selection.…”