Sex at the thermal edge: Exploring the physiological limits to sexual reproduction in geothermal bryophytes

Background/Question/Methods Understanding the processes controlling the evolution and maintenance of sex is a key unresolved problem in biology. However, relatively few studies have experimentally examined the relationship between environmental stress and sexual reproduction in natural systems, fewer still have sought to determine what limits sexual reproduction at the extreme edge of life. Recently, we have begun to examine the processes controlling sexual reproduction in several bryophyte species growing near the thermal limits of plant life on geothermal hot-springs in Lassen Volcanic National Park (CA). Using this system, our aim is to explore the relationship between sexual reproduction and stress, and to establish whether limits to sexual reproduction are a consequence of physiological constraints on reproduction or a selective optima because sexual reproduction is disadvantageous in extreme stress environments. Results/Conclusions Lassen geothermal bryophytes are remarkably stress tolerant and we have observed gametophytes growing with soil surface temperatures as high as 69ºC, while still maintaining average predawn PSII efficiencies of 0.6 ± 0.02 (n=20). Despite the high degree of stress tolerance observed in gametophytes, sporophytes are relatively uncommon in the geothermal habitat. We have found that sporophytes of Aulacomnium palustre were most common in cooler non-geothermal areas, but very rare in high temperature geothermal sites (n=41; Chi-Square = 17.97; P < 0.0001). Sporophytes were present on 0.6% ± 0.02 of ramets growing below 35ºC, and only found on 0.03% ± 0.07 of ramets in sites above 35ºC. Presently, the mechanisms contributing to reduced sporophyte formation in high-temperature environments are unknown, although our results suggest there are physiological limits to sexual reproduction in even the most stress-tolerant organisms. As sexual reproduction in bryophytes involves free-swimming flagellated motile gametes (sperm), we have begun to examine the impact of temperature stress on sperm motility in several bryophyte species. We hypothesize that sperm viability may be a significant factor limiting sporophyte formation in geothermal bryophyte communities. We have found that sperm motility in Pohlia nutans, a geothermal species, is strongly influenced by sperm density, temperature, and the composition of the swimming media. Surprisingly, we show that sperm from geothermal species display a remarkably long swim period (up to 16 days) ex planta, and may employ a novel cellular energy store.