Sexual selection and alternative reproductive tactics in the nursery-web spider Pisaura mirabilis Paolo Giovanni Ghislandi PhD Thesis Sexual selection and alternative reproductive tactics in the nursery-web spider Pisaura mirabilis Paolo Giovanni Ghislandi SpiderLab Genetics, Ecology and Evolution, Department of Bioscience Faculty of Science and Technology Aarhus University November 2017 SUPERVISORS: Prof. Trine Bilde Department of Bioscience, Aarhus University, Denmark Dr. Cristina Tuni Department Biologie II, Ludwig-Maximilians University München, Germany CREDITS: Photos: Paolo Ghislandi SpiderLab Logo: Lena Grinsted CITE AS: Ghislandi P.G. (2017). Sexual selection and alternative reproductive tactics in the nursery- web spider Pisaura mirabilis. Ph.D. dissertation. Genetics, Ecology and Evolution, Department of Bioscience, Aarhus University, Denmark NUMBER OF PAGES: 103 PRINTED BY: Fællestrykkeriet – SUN, Aarhus University Table of Contents Acknowledgements…………………………………………………………………………….........1 Summary…………………………………………………………………………………………….3 Resumé………………………………………………………………………………………….........5 State of the ART……………………………………………………………………………………7 Reproductive tactics in the nursery-web spider Pisaura mirabilis……………………...………11 Types of ARTs: fixed or plastic traits?...........................................................................................15 Which ecological drivers influence the expression and maintenance of ARTs?........................20 References………………………………………………………………………………………….23 Chapter I - Behavioural plasticity and population variation in the expression of alternative reproductive tactics in the nuptial gift giving spider Pisaura mirabilis: are guys from the hood doing like we do? Manuscript..........................................................................................................28 Chapter II - Resource availability, mating opportunity, and sexual selection intensity influence the expression of male alternative reproductive tactics. Re-submitted to The Journal of Evolutionary Biology.....................................................................................................................56 Appendix to Chapter II - The effect of environmental variation on the expression and maintenance of ARTs……………………………………………………………………………...89 Chapter III - Silk wrapping of nuptial gifts aids cheating behaviour in male spiders Behavioral Ecology (2017), 00(00), 1–6. doi:10.1093/beheco/arx028……………………………93 Chapter IV - Extreme male mating behaviours: anecdotes in a nuptial gift-giving spider Arachnology (2015) 16 (8), 273–275……………………………………………………………..100 Acknowledgements I‟ve always been the spider guy. I had my first pet spider when I was 13, as a present from my father, a young adult female Chilean rose tarantula (Grammostola rosea, Walckenaer, 1837). I had no clue it was actually a female, so I called it “Ranieri”, like the prince of Monaco, just because to me it looked so regal and majestic that it really deserved that name. I spent a massive amount of hours watching what Ranieri was doing (not much by the way, as most mygalomorphs..), as there was something special over her that I was not really able to decode or easily grasp. Something I never experienced before, in the face of the huge amount of whatever other animal I previously kept in a terrarium, cage or aquarium. To me, Ranieri seemed different. The growing interest and passion for that difference brought me to have raised and bred more than 60 spider species from 20 different families and to be about to finish a PhD on spiders behaviour. Thanks, Ranieri. Among all the people I want to thank for this great experience, the first one is my partner, Daniela Boncinelli, who have always supported and encouraged me to pursue my PhD study far before I started it and continued doing that until today. And she does it with whatever project I decide to realize, from the smallest to the ones potentially changing our lives. A huge, huge thanks goes to my parents and my entire family, for always supporting and feeding my interest and for having allowed me to keep whatever animal at home not to limit my passion, even when it came to black widows, brown recluse spiders or deadly poisonous centipedes. Grazie mamma, grazie papà. Thanks to Myriam and Luciano Boncinelli, Daniela‟s parents, for all the support and lovely advice helping me figuring out which was the right direction to go. Thanks to all the friends who were always with me, before, during and (hopefully) after this PhD. Then thanks to myself, for having never given up on my passion and dedication, even when it seemed it wasn‟t really leading me anywhere, or when I had the feeling I could have had better things to do. 1 To my supervisor Trine Bilde, thanks for all the things I‟ve learnt, for helpful discussions, for “cooling down” my love for spiders when it had to be more scientific and less emotional, and for all the kindness and human support which had nothing to do with being one‟s supervisor. Thanks to my co-supervisor, Cristina Tuni, for being a friend more than a co-worker, and for involving me in a lot of supercool side projects taking time away from my real, massive Phd project. Thanks to Virginia “Vivi” Settepani, Magnus Jacobsen and André Walter for being great friends and helpful colleagues, for all the fun in South Africa doing field work, for Pevestorf and for all the rather unfruitful fishing trips. Thanks to Jesper Bechsgaard, Bram Vanthournout, Tommaso Manenti, Marie Rosenstand and “the LMU crew”, Philipp Sprau, Petri Niemelä, Marco La Fortezza and Alex Hutfluss for all the beers, fun and also, sometimes, advice. Thanks to all the students who helped me collecting data. I would have never forgotten to thank Fabio De Vita, the biggest spider lover and experienced breeder I have ever met, and Carlo Paoletti, the biggest amphibian lover and curiosity-driven- zoology fan I have ever met, for being two of my best friends and for walking me in the world of terraristics and taxonomy when I was just a bit more than a kid. Grazie fratellone, grazie Carletto. Last but not least, thanks to Emanuele Biggi and Francesco Tomasinelli, for all the hours at the phone talking about spiders when I was a kid, for being great friends and for the always too-few collecting trips together, grazie Ema and grazie Francio! And obviously, thanks to something like 7.360 Pisaura mirabilis which “spontaneously” collaborated to my PhD project. 2 Summary The evolution and maintenance of alternative reproductive tactics ARTs represent a topic of broad interest in evolutionary and behavioural biology. In this thesis, I studied the characteristics and factors that influence the expression of ARTs in the nuptial gift-giving spider Pisaura mirabilis, where males offer either genuine or worthless nuptial gifts but can also mate without a gift, and where males also facultatively perform thanatosis, a death feigning behaviour associated with courtship. I addressed the following questions: 1. Are ARTs fixed or plastic? I conducted a study in five different populations to investigate whether nuptial gift traits and thanatosis represent fixed or plastic tactics, and show that ARTs are plastic labile traits. 2. Is there variation in the expression of ARTs display among populations? Populations may diverge in the expression of ARTs in response to variation in ecological factors. As a first step to gain insight into population differences, I determined variation in the expression of ARTs among populations, and found evidence for population variation in the frequencies of trait expression. 3. Which ecological factors influence the expression and maintenance of ARTs? Ecological factors may influence the expression of ARTs, and variation in ecological factors over the reproductive season may influence the maintenance of ARTs. I conducted a field study to explore whether the nuptial gift tactics vary with ecological factors. I found patterns of correlation between sexual selection, male body condition and prey availability and the expression of tactic, suggesting that the interplay and variation in ecological factors over time influence the maintenance of ARTs in wild populations. 4. How do seasonal changes in ecological factors shape ARTs? Based on the empirical data collected in my thesis, I aimed to develop and parameterize a model to investigate how variation in ecological factors influence the maintenance of ARTs, this work is recently initiated and ongoing, and represented as a short sketch of the model. 5. What is the role of silk wrapping in alternative nuptial gift tactics? Silk is used to wrap the nuptial gift, and can potentially be used to enlarge the gift or disguise gift content. I performed a study to test whether males make strategic use of silk when offering nuptial gifts, and found that males wrap worthless gifts with more silk than genuine gifts, possibly to 3 compensate for their lower nutritive value and to increase copulation time. Finally, while collecting data on male reproductive behaviour, I observed that males perform rather extreme behaviours in additions to those reported above, this is reported in a paper presenting extreme ARTs. 4 Resumé Evolutionen og opretholdelse af alternative reproduktionstaktikker (ARTs) repræsenterer et emne af bred interesse indenfor evolutionær- og adfærdsbiologi. I denne afhandling, har jeg studeret karakteristika og faktorer der influerer udtrykket af ARTs hos edderkoppen, Pisaura mirabilis, hvor hanner oftest tilbyder enten spiselige eller værdiløse bryllupsgaver.