How Do Brief Social Interactions Change Over Time in Pair-Bonded Zebra
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bioRxiv preprint doi: https://doi.org/10.1101/2020.06.18.160051; this version posted June 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 4.0 International license. 1 Monogamy in a moment: how do brief social interactions change over time in pair-bonded zebra 2 finches (Taeniopygia guttata)? 3 Nora H. Prior1, *, Edward Smith1, Robert J. Dooling1, Gregory F. Ball1 4 5 1 Department of Psychology, University of Maryland, College Park, USA 6 7 8 9 *Corresponding author 10 Biology-Psychology Bldg. 11 University of Maryland 12 4094 Campus Dr. 13 College Park, MD 20742 14 Email: [email protected] 15 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.18.160051; this version posted June 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 4.0 International license. 16 Abstract 17 Research on monogamy has largely focused on marked behaviors that are unique to pair bonded 18 partners. However, these marked behaviors represent only a subset of the pair-directed behaviors that 19 partners engage in; the influence of pair bonding on mundane or subtle social interactions among 20 partners remains largely unknown. In the current study, we describe the changes that occur during brief 21 social reunions (or greets) over the course of pair bonding in zebra finches. We quantified pair-directed 22 behavior during five-minute reunions from three stages of pair bonding: initial pairing (between 4-72 23 hrs), early pairing (1-2 weeks) and late pairing (>1 month). These social interactions were 24 operationalized in multiples ways. First, we quantified the overall activity levels (call and movement 25 rates) for both the male and female. Overall, females were more active than males, but for both males 26 and females calling activity was highest during the initial timepoint (between 4-72 hrs post-pairing). We 27 quantified behavioral coordination between partners in two ways, 1) similarity in call and movement 28 rates between partners, and 2) temporal synchrony between calls and movements (via sliding 29 correlation coefficients of time-stamped calls and movements). Overall there were no effects of pairing 30 on behavioral coordination. Finally, we used principal component analyses to disentangle behavioral 31 coordination from the activity levels of the male and female. These results contribute to a growing line 32 of evidence that male and female zebra finches differentially contribute to social dynamics and highlight 33 the influence of pair bonding on the development of social dynamics. Behavioral coordination is clearly 34 important for marked interactions (e.g. duetting, courtship displays and biparental care). Our results 35 raise the question of what the roles of such mundane social interactions are in monogamous 36 partnerships. 37 38 Keywords: Behavioral synchrony, interactional synchrony, sex differences, stack call 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.18.160051; this version posted June 20, 2020. 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 4.0 International license. 39 Introduction 40 In monogamous species, the formation and maintenance of a pair bond is necessary for the 41 successful rearing of offspring (Lack, 1968; Reichard & Boesch, 2003). The majority of research on the 42 mechanisms underlying pair bonding has focused on marked, pair-specific behaviors and interactions of 43 partners (Aragona et al., 2006; Soma & Garamszegi, 2015; Wachtmeister, 2001; Young et al., 2011; 44 Young & Wang, 2004). This approach has revealed remarkable conservation in the mechanisms of pair 45 bonding across taxa (Bales et al., 2007; Donaldson & Young, 2016; O’Connell & Hofmann, 2012; Walum 46 & Young, 2018). 47 Highly-marked behaviors and interactions are particularly evident during courtship and initial 48 pair-bond formation. For example, in prairie voles (Microtus ochrogaster), the establishment of a pair 49 bond is clearly marked by the development of selective preference/affiliation for a mate (Resendez et 50 al., 2016; Williams et al., 1992; Young et al., 2011). This marked selective attachment has been used to 51 identify the mechanisms underlying pair formation. However, these marked behaviors represent only a 52 subset of those that partners engage in, and more detailed understandings of partner interactions are 53 needed in order to further elucidate mechanisms of pair bonding. During partner preferences tests, the 54 pattern of approach and proximity time between partners continues even after initial establishment of 55 the pair bond, with the focal individual spending more time with their partners at later stages of pair 56 bonding (Scribner et al., 2020). Furthermore, important long-term impacts of pair bonding on the brain 57 and behavior of voles are revealed by differences in approach of an individual to its mate versus a 58 stranger (Scribner et al., 2020). Even in the most commonly studied model systems, remarkably little is 59 known about the consequences of pair bonding on mundane or subtle features of partner interactions. 60 Whereas monogamy is rare in mammals (<4% of species), the vast majority of birds form some 61 type of monogamous partnership (~90% of species) (Reichard & Boesch, 2003). Across bird species there 62 is considerable variation in the phenotype of monogamous bonds. Monogamous bonds vary in how long 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.18.160051; this version posted June 20, 2020. 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 4.0 International license. 63 they are maintained; they may be transient, lasting only a season, or life-long (Black & Hulme, 1996). As 64 with prairie voles, the majority of studies focus on marked features of pair bonding (e.g. partner 65 preference, proximity time, allopreening and clumping) (Kenny et al., 2017; Prior et al., 2013; Smiley et 66 al., 2012; Tomaszycki & Adkins-Regan, 2005). However, the importance of brief social interactions has 67 also been described in numerous species: at the nest, brief social interactions appear to be essential for 68 the active coordination of parental duties between partners (I. C. A. Boucaud et al., 2016; Mariette & 69 Griffith, 2012, 2015; van Rooij & Griffith, 2013). This raises the question more broadly of how subtle 70 features of social interactions are shaped by pair bonding. 71 Here we describe the effect of pair bonding on brief social interactions in monogamous zebra 72 finch pairs. Zebra finches maintain sexually monogamous life-long pair bonds, are non-territorial, and 73 are highly gregarious. Interestingly, traditional partner preference paradigms may fail to demonstrate 74 selective preference for the partner (Prior et al., 2013), although other behavioral assays clearly show 75 that many aspects of pair-directed behavior are reserved for or more common between partners than 76 familiar conspecifics (Fernandez et al., 2017; Gill et al., 2015). Additionally, intra-pair calling dynamics, 77 across multiple contexts, appear to be important behavioral components of the zebra finch pair bond (I. 78 Boucaud et al., 2016; Pietro Bruno D’Amelio et al., 2017a; Elie et al., 2010; Fernandez et al., 2017; Gill et 79 al., 2015). 80 In the current study, we operationalize brief social reunions (both calls and movements) of pairs 81 over the course of pair bonding: initial pairing (between 4-72 hrs), early pairing (1-2 weeks) and late 82 pairing (>1 month). First, we quantified the overall activity levels (call and movement rates) for both 83 males and females. Second, we used two approaches to estimate the coordination of the activity 84 between partners, including quantifying the similarity in call and movement rates between partners as 85 well as quantifying the sliding correlation coefficients for time-stamped calls and movements (a measure 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.18.160051; this version posted June 20, 2020. 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 4.0 International license. 86 of temporal synchrony). Finally, we used principal component analyses to disentangle behavioral 87 coordination from the activity levels of the male and female. 88 89 Materials and Methods 90 Subjects and establishment of pairs 91 Twenty adult zebra finches (5-6 months old) were used in this study (10 females and 10 males). 92 Throughout the study, zebra finches were housed with ad libitum seed, water and grit on a 12L:12D light 93 cycle. This same cohort of zebra finches was also used for a subsequent experiment (Prior et al., 2019). 94 Prior to pairing, zebra finches were housed in same-sex flocks. In order to provide the 95 opportunity for pairs to freely form, birds were moved to mixed-sex flocks for 72 hours. Providing 96 individuals with the opportunity to freely form monogamous bonds is important as forced pairing can be 97 associated with lower pair fecundity (Griffith et al., 2017). Thus, birds were housed in mixed-sex flocks 98 with either a male- or female-biased sex ratio (2 females with 3 males or 3 females with 2 males).