Yuting Dong

If individuals fail to reproduce, populations can face extinction. Many biotic and abiotic factors, such as competition, predation, food availability, and environmental conditions, can substantially influence reproductive success. Despite facing all of these factors, spiders are rarely studied in the context of biotic and abiotic impacts on reproduction. Across the globe, spiders are the most abundant and ubiquitous predators of invertebrates. Thus, it is important to gain a more comprehensive understanding of their reproduction and the factors that shape population viability and persistence. Steatoda grossa, a false black widow spider, is a globally distributed species, commonly found around human residences in both urban and rural areas. The species has been spreading throughout most temperate areas and is potentially one of the most successful invasive spiders; as are the closely related S. nobilis and Latrodectus geometricus (same subfamily, Latrodectinae). S. grossa exhibits female-biased sexual dimorphism, and males show a set of ritualized courtship behaviours that are critical for male mating success. Here, I explore the fascinating mating and reproductive behaviour of S. grossa and then investigate how both biotic and abiotic factors influence the outcome of reproductive processes. In this thesis, I examine how male-male competition, mating behaviour, food availability and thermal stress affect reproduction in S. grossa.

In Chapter 2, I tested the role of male body size in mating success and male-male competition in S. grossa. Male body size is important for mating success in many species. In a female-biased sexually dimorphic animal, the benefit of a male having a large body size remains unclear. I designed the experiment which created encounters with a female using either two size-mismatched males (thus creating conditions of male-male competition for mating success) or a single male. I found that all males obtained a mating, regardless of body size when rivals were absent (i.e., non-competitive conditions). However, under competitive conditions, larger males achieved greater mating success; thus demonstrating an important role for male body size in pre-copulatory mating success in S. grossa. At the same time, I also found that copulation duration was significantly reduced when multiple males compete for copulations. Combined, this work sheds novel insight on male body size evolution in this species and provides a potential explanation for the extent of sexual size dimorphism observed in this species; the benefits of large male body size shown in this thesis help explain why male dwarfism (i.e., extremely small male size) has not evolved in S. grossa. Finally, my finding that male-male competition reduces copulation duration resulting from male-male competition may have potential ramifications for male and female reproductive success.

Next, in Chapter 3, I found that mating disruption (i.e., interruption of mating resulting in reduced copulation duration) decreases female spiders’ reproductive success. In sexually reproducing taxa, copulation is critical for the transfer of sperm from the male to the female. In many taxa, including spiders, with relatively long copulation duration, various biotic and abiotic factors have the potential to disrupt mating before it would be naturally terminated. This includes, for example, the male-male competition conditions investigated in Chapter 2, but also predation, and environmental conditions such as rain and wind. Here, I simulated the physical disruption of copulation (removing the male from the mating arena to prevent re-mating) at a range of time points (i.e., 2, 5, 10, 20 minutes compared to natural matings, lasting 40-60 minutes) and recorded female reproductive success. My results show that early disruption of copulation leads to significantly lower reproductive success in the false widow spider. Specifically, while copulations longer than 10 minutes resulted in equivalent reproductive success to natural matings, copulations less than 10 minutes resulted in fewer offspring. This suggests that a copulation of just 10-minutes allows the male to inseminate enough sperm for the female to fertilize most or all of her eggs. Following from this result, I also conducted an experiment to explore if an extended copulation functions as mate-guarding. I introduced virgin fresh males to females who either mated for a long duration or a short one and checked if female accepted another mating. Extended copulation duration did not influence female receptivity to fresh males 24 h later, but might influence oviposition and fertilization processes. Finally, I suggest that extended copulation in this species might play a role in sperm competition.

In Chapter 4, I tested the effects of food availability on female body mass changes and reproductive success in S. grossa. All organisms need food in order to grow, survive and reproduce. In most web-building spiders, females require more food to reach sexual maturity and are relatively larger than males. I provided females with different numbers and sizes of prey (house crickets) and measured their subsequent reproductive investment and success. I found that females provided with intermittent prey produced fewer progeny per egg sac and the interval between sequential egg sacs increased. Additionally, female spiders continuously invested almost half of their body mass in each reproductive event, but this investment showed a decreasing pattern over time, which also resulted in a decreasing pattern in egg sac mass. Moreover, starved females stopped reproducing for several months, but recommenced egg sacs production when fresh prey was provided. Indeed, females laid viable egg sacs within several days of feeding, and these in turn produced healthy spiderlings, indicating that reproductive capacity is only temporarily suspended during harsh conditions and extended periods of resource depletion. The synanthropic lifestyle of S. grossa might induce them to periodic prey scarcity in many human-related habitats, such as cupboards and sheds. This chapter shows the general pattern of spider reproduction over time and strategies to cope with food limitations.

Finally, in Chapter 5, I explored the impact of thermal stress on survival, development and reproduction across different life stages of S. grossa. Human-induced climate change is having a dramatic effect on the global thermal environment. In addition to increases in average local temperatures, climate change is predicted to drive increases in climatic extremes, including heatwaves. Importantly, these changes can pose a significant threat to the persistence of natural populations, and these threats might be especially critical for ectotherms given that body temperature regulation depends on external environmental conditions in ‘cold-blooded’ animals. In this chapter, I exposed different age-cohorts of the false widow spider to different temperatures and studied the effects of both constant thermal stress and extreme temperature events (i.e., heatwaves) on reproduction. Egg sacs of S. grossa perished precociously under both thermal conditions, whereas survival was high at lower temperatures, indicating a temperature threshold on neonate survival to hatching. For spiderlings, the growth trajectories were impacted by extreme ambient temperatures; spiderlings exposed to high temperatures exhibited severely depressed growth rates, whereas those reared at lower temperatures grew exponentially and attained significantly larger adult weights. However, female and male spiderlings showed a different growth rate under thermal exposure, suggesting a sex-specific thermal resistance. Finally, in adults, females exposed to a heatwave after mating suffered short-term impacts on reproductive success; females laid significantly smaller first egg sacs and produced significantly fewer spiderlings from these egg sacs. However, these negative impacts were only apparent in the first egg sac, and by the second egg sac female reproductive success appeared to recover. Combined, the findings in this chapter demonstrate that the effects of exposure to high temperatures are life stage-specific, sex specific and that exposure to heat more negatively affects the survival and development of eggs and younger spiderlings than adults.

In this thesis, I revealed size-dependent advantages in males S. grossa during competition for access to females. I argue that the benefits of larger size in males provide insights into male body size evolution and sexual size dimorphism in this species. Moreover, I show that male-male competition (i.e., mating disruption) leads to reductions in copulation duration. Following this, the impact of mating disruption on female reproductive success was analyzed and my findings suggest that sperm transfer takes place early during mating. The effects of food availability on female body mass changes and reproductive success were also investigated. That work highlighted significance of a large female body mass and the reproductive strategies in S. grossa under food limitation for trade-offing current and future reproductive success, for example producing fewer eggs per egg sac but more egg sacs over time; holding back on reproduction until abundant food is available. Additionally, my thesis evaluates the consequences of thermal stress on survival, development and reproduction across different life stages, providing insights into the species' potential adaptability to current climate change scenarios. Combined, this thesis enhances our understanding of spider reproductive ecology. Building on these findings, future research could explore the mechanisms underlying sperm transfer, extended copulation duration. Moreover, adaptive mechanisms in spiders for coping with the climate change challenges are interesting, for instance, the mechanisms for the transient reduced reproductive success. Climate change and climate extremes is posing threats to many organisms, leading to detrimental impacts on biodiversity. As the most abundant predator of invertebrates, spiders are often overlooked in biodiversity conservation efforts. It is important to study the impacts of thermal stress on a broader range of high-trophic-level animals, which provides a more comprehensive understanding of ecological resilience and the effects of climate change on biodiversity.