Defects in mating behavior and tail morphology are the primary cause of sterility in C. elegans males at high temperature

Abstract

Reproduction is a fundamental imperative of all forms of life. For all the advantages sexual reproduction confers, it has a deeply conserved flaw: it is temperature sensitive. As temperatures rise, fertility decreases. Across species, male fertility is particularly sensitive to elevated temperature. Previously, we have shown in the model nematode Caenorhabditis elegans that all males are fertile at 20°C, but almost all males have lost fertility at 27°C. Male fertility is dependent on the production of functional sperm, successful mating and transfer of sperm, and successful fertilization post-mating. To determine how male fertility is impacted by elevated temperature, we analyzed these aspects of male reproduction at 27°C in three wildtype strains of C. elegans: JU1171, LKC34 and N2. We found no effect of elevated temperature on the number of immature non-motile spermatids formed. There was only a weak effect of elevated temperature on sperm activation. In stark contrast, there was a strong effect of elevated temperature on male mating behavior, male tail morphology and sperm transfer such that males very rarely completed mating successfully when exposed to 27°C. Therefore, we propose a model where elevated temperature reduces male fertility as a result of the negative impacts of temperature on the somatic tissues necessary for mating. Loss of successful mating at elevated temperature overrides any effects that temperature may have on the germline or sperm cells.

Temperature Stressed Caenorhabditis elegans Males Prioritize Feeding over Mating Resulting in Sterility

“…We have also shown previously that males exposed to temperature stress at some point in their lives will complete mating without actually transferring sperm (Nett et al, 2019) or ejaculate on the hermaphrodite's body wall instead of in the reproductive tract (N.B.S. unpublished observations).…”

“…Fewer studies still are performed with wild isolate males. We’ve shown elsewhere that there are appreciable differences between wild isolate male fertility under temperature stress (Petrella, 2014; Nett et al, 2019; Sepulveda and Petrella, 2021), and in this study we’ve dissected fertility into several behavioral factors which also differ between isolates. The question remains however, how relevant are these differences in the wild?…”

“…Prior research has often focused on the negative impact of temperature stress on germline-associated processes in males, such as sperm production and quality in metazoans like fruit flies, cattle, and humans (Casady et al, 1953; Hjollund et al, 2002; David et al, 2005; Ahmad et al, 2012; Rao et al, 2016; Green et al, 2019; Llamas-Luceño et al, 2020). However, we have previously shown that in temperature stressed C. elegans males the impact of temperature stress on germline-associated processes like sperm production and activation is relatively minor (Nett et al, 2019), and cannot account for the near total sterility observed (Petrella, 2014; Sepulveda and Petrella, 2021). Rather, we found that in C. elegans , male sterility under temperature stress is largely defined by negative impacts on somatic-associated processes, specifically mating organ anatomy and mating behavior (Nett et al, 2019).…”

“…An adult male on a food source that has not experienced physical contact with a hermaphrodite will dramatically alter their locomotion resulting in food leaving in search of a mate (Barrios, 2014). Our previous work has shown both that male tail anatomy and the ability of males to respond the presence of hermaphrodites are negatively impacted under temperature stress (Nett et al, 2019), thus sensory and other male reproductive behaviors could be negatively impacted in a similar fashion.…”

Transcription Factors That Control Behavior—Lessons From C. elegans

“…In addition, connections between neurons can be different between the sexes ( Oren-Suissa et al, 2016 ; Cook et al, 2019 ; Molina-García et al, 2020 ), and a neuron may mediate sex-specific behavior depending on the sexual-context of the animal ( Lee and Portman, 2007 ). Like other behaviors, developmental factors as well as environmental conditions, such as food availability, temperature and CO 2 level can influence sex-specific behaviors ( Gruninger et al, 2006 ; Fenk and de Bono, 2015 ; Gouvêa et al, 2015 ; Nett et al, 2019 ). Here we describe the sex determination pathway and TFs that regulate sex-specific behaviors by controlling neuron development and synaptogenesis.…”