Extreme temperatures compromise male and female fertility in a large desert bird

Abstract

Temperature has a crucial influence on the places where species can survive and reproduce. Past research has primarily focused on survival, making it unclear if temperature fluctuations constrain reproductive success, and if so whether populations harbour the potential to respond to climatic shifts. Here, using two decades of data from a large experimental breeding programme of the iconic ostrich (Struthio camelus) in South Africa, we show that the number of eggs females laid and the number of sperm males produced were highly sensitive to natural temperature extremes (ranging from −5 °C to 45 °C). This resulted in reductions in reproductive success of up to 44% with 5 °C deviations from their thermal optimum. In contrast, gamete quality was largely unaffected by temperature. Extreme temperatures also did not expose trade-offs between gametic traits. Instead, some females appeared to invest more in reproducing at high temperatures, which may facilitate responses to climate change. These results show that the robustness of fertility to temperature fluctuations, and not just temperature increases, is a critical aspect of species persistence in regions predicted to undergo the greatest change in climate volatility.

The mating system affects the temperature sensitivity of male and female fertility

“…Female reproduction is also sensitive to temperature, especially because egg maturation and oviposition are two highly temperaturedependent processes (Angilletta, 2009;Berger et al, 2008;Kingsolver & Huey, 2008;Schou et al, 2021), and it is likely that female TSF could be modulated further by pre-and post-fertilization mating interactions. For example, physical harm inflicted via male harassment of females during copulation, or physiological harm mediated via toxic ejaculate compounds (Arnqvist & Rowe, 2005;Dougherty et al, 2017;Parker, 2006), could increase female TSF if TSF is dependent on the condition of the individual and costly thermal buffering mechanisms.…”

Egg-laying increases body temperature to an annual maximum in a wild bird

“…Despite correlative evidence showing a negative relationship between ambient temperature and laying dates 7 , 9 , there are only limited experimental studies showing that spring temperatures affect the timing of laying directly 8 , 10 . Interestingly, in the sole study, we are aware of that measured the effect of changes in ambient temperature on laying in wild birds, Schou et al 98 identified a critical thermal window in captive ostrich ( Struthio camelus ), for which the rate of egg-laying peaked at 20 °C, dropping by 15% and 18% when temperatures increased and decreased by 5 °C, respectively. However, it is unknown which mechanisms contributed to these results.…”

Evolutionary trade-offs between heat and cold tolerance limit responses to fluctuating climates

“…We used daily records of temperature and reproductive success of 1277 individuals in experimental breeding pairs in the Klein Karoo region of South Africa over a 21-year period. Here daily temperatures can range from -5 to 45ºC during the breeding period (30). We focus on temperature effects on reproduction, as survival can underestimate how temperature affects fitness (14,30).…”

“…Here daily temperatures can range from -5 to 45ºC during the breeding period (30). We focus on temperature effects on reproduction, as survival can underestimate how temperature affects fitness (14,30). We analyze selection on female egg-laying rates as our recent work shows this is a key determinant of reproductive success and is influenced by temperature (30) (Fig.…”

“…Using these repeated estimates and a nine-generation pedigree we examined the genetic basis to heat and cold tolerance. success, as measured by egg-laying rates, rapidly declines with deviations from a thermal optimum of around 20ºC (30). Points are averages across females with standard errors binned according to the temperature variable.…”