Chemical communication in the spider Pisaura mirabilis

Beyer, Michelle (2024): Chemical communication in the spider Pisaura mirabilis. Dissertation, LMU München: Fakultät für Biologie

Abstract

Chemical communication represents one of the most ancient and widespread forms of communication and has been extensively studied for more than a hundred years. Yet, for most of this period, research on chemical communication has been largely driven by traditional views on sex roles in reproduction, leading to biased literature that is skewed towards females chemically signalling and males detecting those signals. It was only in the last one to two decades that research slowly began to include investigations on male chemicals and females exerting choice based on those. While most of our understanding of chemical com-munication comes from studies on insects, other taxonomical groups, such as spiders, lag behind. Motivated by the need to expand our understanding on the functions of chemicals in a reproductive context for both sexes in this taxonomical group, I investigated in this thesis the influence of silk- and cuticle-borne chemical communication on male mate search and reciprocal assessment between male and female spiders. Specifically, I aimed to understand the role of silk- and cuticle-borne chemicals during inter-sexual communication in the web less hunting spider Pisaura mirabilis, a species known for its peculiar mating behaviour that involves male offering of nuptial-gifts to the female. Mate search is essential part of reproduction and particularly challenging in solitary animals, such as cursorial spiders, that live widespread in their habitats. Trails, which are paths in the environment for example created by pheromone deposition on a substrate, represent one of the most efficient and target-oriented means for mate search. Specifically, trails increase the chances of finding mates compared to random search, especially if these trails convey directionality information that indicate the movements of the trail producer. Yet, trail directionality is rarely investigated and poorly understood. In Chapter 1, I investigated presence of directionality information in female spider silk trails by exposing males to unidi-rectionally deposited female silk, and scoring male trail-following direction with reference to female movement. I further explored potential influences of female phenotypic traits on male trail-following behaviour. I found overall lack of general directional trail-following (i.e., males following trails in female direction). However, males followed trails more often when they were unwashed (opposed to washed with solvents to remove putative chemicals) or sourced from females that were relatively larger (opposed to smaller) than the male. These results suggest context-dependent male directional trail-following, possibly reflecting male mate choice, and likely based on chemical trail attributes assessed through probing of silk lines that convey information on female quality. Male mate choice has traditionally been overlooked, with mate preferences and choices largely attributed to females only. However, when there is large variation in female quality and/or when mating is costly for males, as for costly spider nuptial-gifts, selection should favour male discriminatory abilities and choice. Female reproductive potential varies with female developmental and reproductive state, and/or body condition, and males are expected to exert mate choice towards females that are of higher reproductive value. In Chapters 2 and 3, I studied male behavioural responses in the form of courtship investment or trail-following, when sequentially or simultaneously exposed to silk sourced from females varying in their phenotypic states. Females signal their developmental and reproductive state, but not mating state, as well as their body condition. Males adjusted their courtship investment and exerted trail-following choices based on these female states. Specifically, males courted adult females more often than juvenile or adult ones, preferred high-condition females over low-condition ones, and did not differentiate between mated and unmated females, whereas males decreased their courtship towards females that carried their fertilized egg-sacs. Such differentiated male behavioural responses might reflect a male strategy in light of the high costs of courtship. In the context of mate assessment, male chemicals are rarely viewed as secondary sexual traits that potentially affect female mating decisions. However, male chemicals are also important for reproduction as they potentially affect female mate choice either by reliably reflecting male underlying qualities or by manipulating the female into matings. In Chapters 4 and 5, I explored the presence and variation of male chemical signalling via the nuptial-gift and its role in female mate choice. For this purpose, I observed female mate acceptance behaviours to chemical properties of male gift silk, and investigated whether these behaviours are influenced by male phenotypic traits. I found that chemicals appear to be present on the silk covering male nuptial-gifts, shown by higher female acceptance of gifts with unwashed opposed to silk washed with solvents. However, there was no variation in mass-dependent silk-borne chemical signalling, as females accepted gifts produced by males of high and low mass equally likely. While male silk-borne chemicals prime female responses in mate choice, females may base their mate choice on directly accessible mate traits instead of silk-borne ones, most likely due to the male’s ability to use silk to mask non-nutritive gift contents and cheat females into mating in this system. Overall, this dissertation provides important knowledge on chemical communication in a reproductive context and without the limitations of traditional views on fixed sex roles. I show that an impressive variety of conditions and innate states influence both chemical signalling and mate choice, with the latter itself presenting in many facets ranging from courtship investment, trail-following decisions to direct mate acceptance. Both sexes in my model species assess and produce chemicals, consequently influencing mate choice decisions in the other sex. My work highlights the importance of conducting research unobstructed by sex-biases, as only such unbiased research offers to opportunity to fully understand inter-sexual chemical communication.

• Dokumententyp: Dissertationen (Dissertation, LMU München)
• Themengebiete: 500 Naturwissenschaften und Mathematik ; 500 Naturwissenschaften und Mathematik > 570 Biowissenschaften, Biologie
• Fakultäten: Fakultät für Biologie
• Sprache der Hochschulschrift: Englisch
• Datum der mündlichen Prüfung: 8. Februar 2024
• 1. Bericht­erstatter:in: Dingemanse, Niels