Mate choice and the evolution of female promiscuity in a socially monogamous species Dissertation der Fakultät für Biologie der Ludwig-Maximilians-Universität München durchgeführt am Max-Planck-Institut für Ornithologie Seewiesen vorgelegt von Daiping Wang August 2018 Mate choice and the evolution of female promiscuity in a socially monogamous species Dissertation der Fakultät für Biologie der Ludwig-Maximilians-Universität München durchgeführt am Max-Planck-Institut für Ornithologie Seewiesen vorgelegt von Daiping Wang August 2018 Erstgutachter: Prof. Dr. Bart Kempenaers Zweitgutachter: Prof. Dr. Jochen Wolf Eingereicht am: 7.8.2018 Tag der mündlichen Prüfung: 5.2.2019 Diese Dissertation wurde unter der Leitung von Dr. Wolfgang Forstmeier angefertigt. Contents General introduction ................................................................................................................. 5 Chapter 1: Male zebra fiches have limited ability to identify high-fecundity females ........... 15 Chapter 2: No mutual mate choice for quality in zebra finches: time to question a widely-held assumption ..................................................................................... 39 Chapter 3: Irreproducible text-book ‘knowledge’: the effects of color bands on zebra finch fitness ................................................................................................. 63 Chapter 4: Scrutinizing assortative mating in birds .............................................................. 101 Chapter 5: Genetic constraints of female promiscuity: male corollary or independent trajectory? ........................................................................................................... 151 General discussion ................................................................................................................. 203 Addresses of co-authors ........................................................................................................ 211 Author contributions ............................................................................................................. 215 Acknowledgments ................................................................................................................. 217 Curriculum vitae .................................................................................................................... 219 Statutory declaration and statement .................................................................................... 221 General introduction Sexual selection and mate choice In his book On the Origin of Species by Means of Natural Selection, Charles Darwin first proposed the concept of sexual selection. In the book (p 87-87, CHAP. IV., Darwin 1859) he wrote: “And this leads me to say a few words on what I call Sexual Selection. This depends, not on a struggle for existence, but on a struggle between the males for possession of the females; the result is not death to the unsuccessful competitor, but few or no offspring.” However, the more clear definition and detailed description of sexual selection came later in his other famous book The Descent of Man, and Selection in Relation to Sex. For instance, in that book (p 254-255, Part I. Darwin 1871) he said: ‘‘We are, however, here concerned only with that kind of selection, which I have called sexual selection. This depends on the advantage which certain individuals have over other individuals of the same sex and species, in exclusive relation to reproduction.’’ Further, Darwin suggested that (p 398 GENERAL SUMMARY Part II. Darwin 1871): “The sexual struggle is of two kinds; in the one it is between the individuals of the same sex, generally the male sex, in order to drive away or kill their rivals, the females remaining passive; whilst in the other, the struggle is likewise between the individuals of the same sex, in order to excite or charm those of the opposite sex, generally the females, which no longer remain passive, but select the more agreeable partners.” Progress after Darwin In the more than 150 years after Darwin’s propositions, much progress has achieved in developing and supporting the core parts of sexual selection, either theoretically by modeling or 6 | General introduction practically with empirical examples (Andersson and Simmons 2006; Jones and Ratterman 2009). The first core part of sexual selection, that is ‘male-male combat’ (intra-sexual selection), seems easy to understand because of many solid examples such as male kudus Tragelaphus strepsiceros enormous horns (Davies et al. 2012) and much bigger size relative to females (3 to 7.5 times as heavy) of the male northern elephant seal Mirounga angustirostris (Le Boeuf and Reiter 1988). However, female choice, perhaps more specifically, why females are choosy, the other core part of Darwin’s sexual selection, has intrigued many behavioral ecologists for decades (Andersson 1994). Under a framework of adaption which focuses on benefits the female will gain from choosiness, models have been developed for its evolutionary explanation. Each kind of model is supported by some empirical examples (Jones and Ratterman 2009; Davies et al. 2012). a. direct-benefits models The direct-benefits models suppose that females (or males in sex-role-reversed species) could benefit directly from their chosen mates, through better parental care, a nuptial gift, or territory defence. For instance, female North American bullfrogs Rana catesbeiana (Howard 1978a, b) choose males that have good territories and lay their eggs in those territories, which can increase the survival of eggs. Males of the bushcricket Ephippiger ephippiger (Gwynne 1984) and hanging fly Hylobittacus apicalis (Dussourd et al. 1991) provide a nuptial gift to their mates that the female can eat during or after copulation. Evolution of choice for direct benefits is conceptually simple because the advantage resulting from choosing is obvious. Nevertheless, one point needed to be kept in mind for these direct-benefits models is that male-male competition often goes hand in hand with female choice in the process of providing direct benefits. For example, male northern elephant seals which are bigger relative to females have more chances to win against other males. At the same time, bigger male seals also provide better protection to their harems. b. indirect-benefits models In earlier years, the Fisherian Models (Fisher 1930; Kirkpatrick 1982; Mead and Arnold 2004) were one kind of representative indirect-benefits model explaining the evolution of female choice of one specific male trait. Assuming female preference for a male trait (no matter if this male trait is a reliable quality indicator or just attractive to females), as soon as this preference of the male trait leads to genetic benefits to females, female mate choice will result in a genetic correlation between the female preference and the male trait. This genetic correlation will develop into positive feedback between female preference and the male trait until conflicts arise between sexual selection and natural selection. Evidence for this model came from a lekking sandfly Lutzomyia longipalpis which showed generally attractive males fathered sons General introduction | 7 who were then chosen when they in turn formed leks (Jones et al. 1998). Other supportive studies showed there is a positive genetic correlation between preference and a male trait: stalk-eyed fly Cyrtodiopsis dalmanni, (Wilkinson and Reillo 1994); guppy Poecilia reticulate (Houde and Endler 1990; Brooks 2000) and three-spined stickleback Gasterosteus aculeatus (Milinski and Bakker 1990). Perhaps the most famous indirect-benefits model is the ‘good genes’ with a more adaptive way of thinking (Zahavi 1975, 1977; Hamilton and Zuk 1982). The assumption of this model requires the male trait to be a reliable quality indicator (e.g. a costly ornament) or indicates good genes (e.g. an ornament genetically correlated to viability traits). Female choice evolves because females who chose the male trait (e.g. more elaborately ornamented male) could produce offspring with higher viability or that will be in good condition as adults. This model enjoys the most empirical support by showing the phenotypic correlation between the focal male trait and male reproductive traits. One famous example is the extraordinary tail of the male Indian peafowl (Pavo cristatus) which signals a male’s genetic quality (Petrie et al. 1991; Petrie 1994). However, even though this is such a famous example, in another study of this species, the authors did not find that females preferred males with more elaborate tails (Takahashi et al. 2008). c. other models Besides direct-benefits and indirect-benefits models, several other models have been proposed for explanation of female choice. For instance, a class of models focused on the genetic compatibility between female and male mates. Polymorphic genes of the major histocompatibility complex (MHC) are regarded as essential genes for individual fitness under conditions of natural and sexual selection (Milinski 2006). Studies showed that, with reference to their own MHC profile, female sticklebacks preferred to mate with a male sharing an intermediate MHC diversity to get an optimal complement. Therefore, this could provide resistance against parasites, which could be revealed by the expression of costly secondary sexual characters (Eizaguirre et al. 2009). Another class of models suggested that males evolve sexually selected traits because of the preexisting