Heritable variation in thermal profiles is associated with reproductive success in the world's largest bird.

Organisms inhabiting extreme thermal environments, such as desert birds, have evolved spectacular adaptations to thermoregulate during hot and cold conditions. However, our knowledge of selection for thermoregulation and the potential for evolutionary responses is limited, particularly for large organisms experiencing extreme temperature fluctuations. Here we use thermal imaging to quantify selection and genetic variation in thermoregulation in ostriches (Struthio camelus), the world's largest bird species that is experiencing increasingly volatile temperatures. We found that females who are better at regulating their head temperatures ("thermoregulatory capacity") had higher egg-laying rates under hotter conditions. Thermoregulatory capacity was both heritable and showed signatures of local adaptation: females originating from more unpredictable climates were better at regulating their head temperatures in response to temperature fluctuations. Together these results reveal that past and present evolutionary processes have shaped genetic variation in thermoregulatory capacity, which appears to protect critical organs, such as the brain, from extreme temperatures during reproduction.

Experimental evidence that group size generates divergent benefits of cooperative breeding for male and female ostriches.

Cooperative breeding allows the costs of parental care to be shared, but as groups become larger, such benefits often decline as competition increases and group cohesion breaks down. The counteracting forces of cooperation and competition are predicted to select for an optimal group size, but variation in groups is ubiquitous across cooperative breeding animals. Here, we experimentally test if group sizes vary because of sex differences in the costs and benefits of cooperative breeding in captive ostriches, Struthio camelus, and compare this to the distribution of group sizes in the wild. We established 96 groups with different numbers of males (1 or 3) and females (1, 3, 4, or 6) and manipulated opportunities for cooperation over incubation. There was a clear optimal group size for males (one male with four or more females) that was explained by high costs of competition and negligible benefits of cooperation. Conversely, female reproductive success was maximised across a range of group sizes due to the benefits of cooperation with male and female group members. Reproductive success in intermediate sized groups was low for both males and females due to sexual conflict over the timing of mating and incubation. Our experiments show that sex differences in cooperation and competition can explain group size variation in cooperative breeders.

Being a parent is hard work. The unrelenting demand for food and protection is exhausting. Now imagine being a parent on the hot African savannah. Food and water are scarce, and whenever you leave your offspring, they overheat, or something eats them. This is the reality for ostriches. They, like humans, cope with the challenges of parenthood by sharing childcare responsibilities. Ostriches live in groups, breed in a communal nest, and take it in turns to incubate their eggs. This helps to maximize the survival of their offspring, but it has its downsides. The bigger a group gets, the more its members have to compete over mates and space for their eggs in the nest. The balance between cooperation and competition should, in theory, result in one 'optimal' group size. But this pattern does not seem to hold true: in the wild, ostrich families vary wildly in size and composition. To find out why, Melgar et al. set up dozens of groups of breeding ostriches and gave them different opportunities to cooperate. For males, there was one group size that maximized the number of offspring they produced (reproductive success): a single male with four or more females. Males did not benefit much from cooperation, and suffered greatly from competing with other males for mates. For females, however, the story was different. They benefited much more than males from cooperation and did best in bigger groups where they could share egg care with other individuals. Middle-sized groups were not good for either sex because reproduction was hard to coordinate: males continued to pursue copulations after females had initiated incubation, resulting in eggs being exposed and broken. The different priorities of males and females explain why there is no single optimal group size for ostriches. How groups balance competition and cooperation is a fundamental question in biology. Why do some organisms prefer to live alone, while others thrive in large groups? Understanding more about the balance of priorities within a group could hold the answers. It could also help to inform conservation work and animal breeding by showing how different social pressures influence breeding success.

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

The evolutionary potential of species to cope with short-term temperature fluctuations during reproduction is critical to predicting responses to future climate change. Despite this, vertebrate research has focused on reproduction under high or low temperatures in relatively stable temperate climates. Here, we characterize the genetic basis of reproductive thermal tolerance to temperature fluctuations in the ostrich, which lives in variable environments in tropical and subtropical Africa. Both heat and cold tolerance were under selection and heritable, indicating the potential for evolutionary responses to mean temperature change. However, we found evidence for a negative, genetic correlation between heat and cold tolerance that should limit the potential for adaptation to fluctuating temperatures. Genetic constraints between heat and cold tolerance appear a crucial, yet underappreciated, factor influencing responses to climate change.

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

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.

Developing a female-only flock for artificial insemination purposes in ostriches: Progress and future directions.

The development of a flock of females that can produce eggs and maintain egg production rate without the presence of males is a prerogative for a viable artificial insemination protocol in ostriches. Over six consecutive breeding seasons (May-December, 2009-2014), we recorded the egg production performance of 40 single-penned (ART) South African Black ostrich females (2-9 years of age), and compared these records with the egg production of 162 pair-mated females of comparable age from the breeding flock (BP). ART females laid significantly fewer eggs than BP females (mean±SEM: 3.49±0.13 eggs per month vs. 4.64±0.09 eggs per month respectively; P<0.001). Both groups showed a similar pattern of laying, with a peak production in July to September. The mean egg weight of ART females was significantly lower than those of BP females (1367±2.25g vs. 1423±1.1g, respectively; P<0.001). Furthermore, female age significantly affected egg production and egg weight whereby BP females reached a peak egg production at 3 years of age, while in ART females, egg production was the highest at 5 years of age. Interestingly, the number of eggs produced, clutches and eggs per clutch of ART females were independent of visual stimulation from the males. These results indicate that male presence is not needed to ensure egg production. Continuous recruitment of young females based on human-friendly behaviour to breeding by artificial insemination from high egg production performance parents could improve egg production of the ART flock. Studies are also needed to gain a better understanding of underlying physiological mechanisms promoting spontaneous ovulation in this species.