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Females Don't Always Sing in Response to Male Song bioRxiv preprint doi: https://doi.org/10.1101/860882; this version posted November 30, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Females don’t always sing in response to male song, 2 but when they do, they sing to males with higher 3 pitched songs 4 5 Alexander N. G. Kirschel1,2,3, Zacharo Zanti1, Zachary T. Harlow3, Edgar E. 6 Vallejo4†, and Martin L. Cody3, and Charles E. Taylor3. 7 8 †Deceased 19th June 2019 9 1Department of Biological Sciences, University of Cyprus, P.O. Box 20537, Nicosia 10 1678, Cyprus 11 2Edward Grey Institute, Department of Zoology, University of Oxford, South Parks 12 Road, Oxford OX1 3PS, United Kingdom 13 3Department of Ecology and Evolutionary Biology, University of California, 621 14 Charles E. Young Dr. South, Los Angeles, CA 90095–1606 15 4Department of Information Technologies and Computer Science, ITESM-Campus 16 Estado de México, Estado de México, Mexico 17 Email of corresponding author: [email protected] 18 Author contributions: ANGK, EEV, MLC and CET conceived of the study and 19 ANGK designed the research; ANGK and ZTH collected field data, assisted by 20 EEV; ANGK and ZZ analysed data; and ANGK wrote the manuscript, with 21 contributions from MLC and CET. bioRxiv preprint doi: https://doi.org/10.1101/860882; this version posted November 30, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 22 Abstract 23 The long-held view that bird song is exclusively a male trait has been challenged 24 recently by a number of studies and reviews highlighting the prevalence of female 25 song. In spite of that, there remains a lack of knowledge on the function of female 26 song, with most evidence thus far focusing on females performing duets with males in 27 courtship displays, for joint territory defence, or for mate guarding purposes. Here we 28 show in a tracheophone suboscine passerine Formicarius moniliger, a sexually 29 monomorphic species in which both sexes sing, that females may participate in both 30 intrasexual and intersexual territory defence. Females sing more in response to 31 females than to males yet demonstrate an unexpected pattern of singing back to 32 playback of males singing higher frequency song than themselves. Unlike males, who 33 respond indiscriminately to playback of any song performed by either sex, females 34 appear to discern not only the sex, but also the siZe of the presumed intruder, 35 perceiving a strong negative relationship between body mass and frequency. Our 36 findings suggest females will only engage in territory defence with males when they 37 expect those males to be weaker than they are. While our results are consistent with 38 expectations of a shared ancestral function of song in territory defence, they also 39 suggest females may suffer greater costs in engaging in territorial disputes and thus 40 limit their vocal contribution according to the perceived threat. 41 Keywords: Animal communication, female song, intersexual interactions, sex 42 roles, intrasexual territoriality, Neotropical birds. 43 44 45 46 bioRxiv preprint doi: https://doi.org/10.1101/860882; this version posted November 30, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 47 Introduction 48 Sexual dimorphism is manifested in animals in a variety of ways. Male elephant seals 49 can be 10 times the siZe of females (Mccann et al., 1989), and sport highly modified 50 proboscises; male deer grow antlers; male peacocks develop iridescent plumage and a 51 long train with eyespots (Yorzinski et al., 2013); all this in aid of attracting females 52 and fighting off rival males (Lande, 1980). Such dimorphism represents conventional 53 sex roles of males competing for mates and females investing in parental care (Kokko 54 and Jennions, 2008). 55 Yet many species are sexually monomorphic. No differences in body siZe; no 56 differences in colour or pattern. Genetic correlations in body siZe between the sexes 57 may constrain sexual dimorphism (Merilä et al., 1998). Also, strong stabiliZing 58 selection acting on the sexes (Price and Grant, 1985), largely driven by them 59 occupying similar niches, might explain their lack of dimorphism (SZékely et al., 60 2007). Many such animals use acoustic communication for mate attraction and 61 territory defence. Insects, frogs and birds create a cacophony of sounds in natural 62 habitats as a result (Kirschel et al., 2009a), but except in some cases of sex-role 63 reversal (Goymann et al., 2004), song has typically been considered a sexually 64 divergent behaviour performed by males (Odom et al., 2014). 65 There are, however, some animals in which both sexes sing. For instance in 66 tropical birds, many females sing as well as males (Slater and Mann, 2004). 67 Females in these instances may at times sing loosely in association with the male or 68 at others sing a tightly-coordinated duet (Slater and Mann, 2004), the latter a 69 phenomenon which has received much attention in the literature (Langmore, 1998, 70 Slater and Mann, 2004, Hall, 2004). Duetting has been attributed to territory defence, 71 whereby the female sings to defend the territory jointly with her mate from a rival of bioRxiv preprint doi: https://doi.org/10.1101/860882; this version posted November 30, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 72 either sex (Fedy and Stutchbury, 2005, Hall, 2004), or she may sing to defend the 73 territory specifically from same sex rivals (Langmore, 1998, Cain and Langmore, 74 2015). Alternatively, duets could function in mate guarding, whereby either the male 75 or the female ensures their partner is not singing solo in an attempt to attract extra- 76 pair mating opportunities (Levin, 1996a, Levin, 1996b, Seddon and Tobias, 2006, 77 Tobias and Seddon, 2009). 78 The prevalence of female song in the tropics has been attributed to sex role 79 convergence in locations where birds are resident and defend territories year-round 80 (Slater and Mann, 2004), but this view has been challenged by studies suggesting 81 female song is ancestral in songbirds (Odom et al., 2014, Riebel et al., 2019). So 82 while songs may represent ornaments attractive to the opposite sex, their primary 83 function in females is thought to be in intrasexual competition in species defending 84 territories year-round from same-sex rivals (Tobias et al., 2011, Tobias et al., 2012b). 85 A further study across all birds identified year-round territoriality as the trait most 86 closely associated with duetting (Tobias et al., 2016). Such year-round territoriality is 87 particularly evident in insectivorous birds (Hau et al., 2000, Slater and Mann, 2004, 88 Tobias et al., 2011), with much previous work on duetting birds focusing on 89 insectivorous wrens and antbirds (Fedy and Stutchbury, 2005, Levin, 1985, Seddon 90 and Tobias, 2006). Female song is also common in many Australian passerines, 91 including in the insectivorous fairy-wrens, whistlers, shrike-thrushes, and bell birds, 92 which like the wrens and antbirds, have extended longevity when compared to most 93 temperate passerines, and defend territories year-round. In these taxa, the sexes are 94 either sexually dimorphic or dichromatic (e.g., antbirds, (Kirschel et al., 2019, Tobias 95 and Seddon, 2009), fairy-wrens and whistlers (Hall and Peters, 2008, van Dongen and 96 Mulder, 2008), sing distinctly different songs (e.g., wrens (Mennill and Vehrencamp, bioRxiv preprint doi: https://doi.org/10.1101/860882; this version posted November 30, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 97 2008), or both (again antbirds (Tobias and Seddon, 2009), and fairy-wrens (Hall and 98 Peters, 2008), suggesting songs may still serve different functions among the sexes. 99 Might there be situations in species where the sexes are monomorphic and sing 100 indistinguishable songs, and what might such cases reveal regarding sex roles? 101 Perhaps sexually monomorphic vocalisations could play a role in intersexual 102 competition (Tobias et al., 2012a). Here we examine such a case. We studied a 103 population of sexually monomorphic Mexican antthrush – a.k.a. Mayan antthrush 104 (Krabbe and Schulenberg 2019) - (Formicarius moniliger), for which previous studies 105 have shown both sexes sing (Blumstein et al., 2011, Kirschel et al., 2009b). Despite 106 evidence showing that individuals can reliably be recogniZed from the subtle spectral 107 and temporal idiosyncrasies in their songs, efforts thus far have not been able to 108 distinguish male from female song (Kirschel et al., 2011b). 109 Mexican antthrush is a tracheophone suboscine passerine (Tobias et al., 110 2012a), a group whose simple stereotypic songs have allowed investigators to identify 111 songs to species (Trifa et al., 2008), and to track movements of individuals in space 112 and time using an acoustic sensor network (Collier et al., 2010).
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