Natural Variants of C. elegans Demonstrate Defects in Both Sperm Function and Oogenesis at Elevated Temperatures

Abstract

The temperature sensitivity of the germ line is conserved from nematodes to mammals. Previous studies in C. briggsae and Drosophila showed that isolates originating from temperate latitudes lose fertility at a lower temperature than strains originating from tropical latitudes. In order to investigate these relationships in C. elegans, analysis of the fertility of 22 different wild-type isolates of C. elegans isolated from equatorial, tropical and temperate regions was undertaken. It was found that there are significant temperature, genotype and temperature × genotype effects on fertility but region of isolation showed no significant effect on differences in fertility. For most isolates 100% of the population maintained fertility from 20°C to 26°C, but there was a precipitous drop in the percentage of fertile hermaphrodites at 27°C. In contrast, all isolates show a progressive decrease in brood size as temperature increases from 20°C to 26°C, followed by a brood size near zero at 27°C. Temperature shift experiments were performed to better understand the causes of high temperature loss of fertility. Males up-shifted to high temperature maintained fertility, while males raised at high temperature lost fertility. Down-shifting males raised at high temperature generally did not restore fertility. This result differs from that observed in Drosophila and suggested that in C. elegans spermatogenesis or sperm function is irreversibly impaired in males that develop at high temperature. Mating and down-shifting experiments with hermaphrodites were performed to investigate the relative contributions of spermatogenic and oogenic defects to high temperature loss of fertility. It was found that the hermaphrodites of all isolates demonstrated loss in both spermatogenic and oogenic germ lines that differed in their relative contribution by isolate. These studies uncovered unexpectedly high variation in both the loss of fertility and problems with oocyte function in natural variants of C. elegans at high temperature.

Caenorhabditis elegans orthologs of human genes differentially expressed with age are enriched for determinants of longevity

“…As expected from prior studies (e.g. Gems et al ., 1998; Petrella, 2014), brood size was markedly lower for all worms at 25 than 15 °C (Fig. 5D).…”

Temperature Dependence of Cell Division Timing Accounts for a Shift in the Thermal Limits of C. elegans and C. briggsae

“…However, although adult worms can withstand short periods of heat shock (Lithgow et al, 1995), it affects their fertility (Aprison and Ruvinsky, 2014). Growth temperatures above 25 C are stressful for C. elegans and lead to sterility; this is true for natural isolates as well as the lab strain N2 (Matsuba et al, 2013;Hirsh et al, 1976;Anderson et al, 2011;Petrella, 2014). To date, five distinct clades of C. briggsae natural isolates have been identified.…”

Fitness effects of thermal stress differ between outcrossing and selfing populations inCaenorhabditis elegans

“…Byerly et al 1976;McMullen et al 2012;Petrella 2014, but see Zhang et al 2015). The decrease of reproductive function at high temperatures seems to be associated with functioning of both spermathogenic and oogenic germ lines (Aprison and Ruvinsky 2014;Petrella 2014), although the relative contribution of these two factors varies between strains (Petrella 2014).…”

“…Conceivably, the pattern observed in our study could have resulted from male and/or female gamete production failure. Indeed, it has been shown that increased temperature affects sperm and oocyte production, ovulation and spermatid activation in C. elegans (Aprison and Ruvinsky 2014;Petrella 2014). We might also expect thermal stress to result in elevated gamete death (McMullen et al 2012) as increased temperature during ovulation has been shown to reduce gamete viability in some fish species (Pankhurst and Van Der Kraak 1997).…”