Sex-Biased Dispersal Patterns of a Social Passerine: Complementary Approaches and Evidence for a Role of Spatial Scale

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Sex-Biased Dispersal Patterns of a Social Passerine: Complementary Approaches and Evidence for a Role of Spatial Scale This is a repository copy of Sex-biased dispersal patterns of a social passerine: complementary approaches and evidence for a role of spatial scale. White Rose Research Online URL for this paper: http://eprints.whiterose.ac.uk/155063/ Version: Accepted Version Article: Li, J., Lv, L., Wang, P. et al. (3 more authors) (2019) Sex-biased dispersal patterns of a social passerine: complementary approaches and evidence for a role of spatial scale. Biological Journal of the Linnean Society, 128 (3). pp. 592-602. ISSN 0024-4066 https://doi.org/10.1093/biolinnean/blz122 This is a pre-copyedited, author-produced version of an article accepted for publication in Biological Journal of the Linnean Society following peer review. The version of record, Jianqiang Li, Lei Lv, Pengcheng Wang, Yong Wang, Ben J Hatchwell, Zhengwang Zhang, Sex-biased dispersal patterns of a social passerine: complementary approaches and evidence for a role of spatial scale, Biological Journal of the Linnean Society, Volume 128, Issue 3, November 2019, Pages 592–602, is available online at: https://doi.org/10.1093/biolinnean/blz122. Reuse Items deposited in White Rose Research Online are protected by copyright, with all rights reserved unless indicated otherwise. They may be downloaded and/or printed for private study, or other acts as permitted by national copyright laws. The publisher or other rights holders may allow further reproduction and re-use of the full text version. This is indicated by the licence information on the White Rose Research Online record for the item. Takedown If you consider content in White Rose Research Online to be in breach of UK law, please notify us by emailing [email protected] including the URL of the record and the reason for the withdrawal request. [email protected] https://eprints.whiterose.ac.uk/ 1 Running title: Female-biased dispersal in black-throated tit 2 Sex-biased dispersal patterns of a social passerine: complementary 3 approaches and evidence for a role of spatial scale 4 Jianqiang Li1*, Lei Lv2, Pengcheng Wang3, Yong Wang4, Ben J. Hatchwell5, 5 Zhengwang Zhang3 6 1School of Nature Conservation, Beijing Forestry University, Beijing 100083, China 7 2School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China 8 3Ministry of Education Key Laboratory for Biodiversity Sciences and Ecological 9 Engineering, College of Life Sciences, Beijing Normal University, Beijing 100875, 10 China 11 4Department of Biological and Environmental Sciences, School of Agricultural, Life 12 and Natural Sciences, Alabama A&M University, Normal, AL 35762, USA 13 5Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 14 2TN, UK 15 *Jianqiang Li (corresponding author) 16 School of Nature Conservation, Beijing Forestry University, Beijing 100875, China 17 Tel: +86-10-62335808 18 Fax: +86-10-62336724 19 Email: [email protected] 1 20 ABSTRACT 21 Animal dispersal patterns have important implications for many biological processes, 22 but measuring dispersal is challenging and often requires the use of complementary 23 approaches. In this study, we investigated local-scale sex-biased dispersal pattern in a 24 social bird, the black-throated tit (Aegithalos concinnus), in central China. Spatial 25 genetic autocorrelation analyses suggested that significant fine scale genetic structure 26 existed in males but not in females. Mark-recapture analyses of individuals ringed 27 also showed that female offspring were more dispersive than male offspring, 28 supporting genetic evidence of local female-biased dispersal. These results were 29 contrary to a previous finding of male-biased long-distance dispersal in this species 30 that was based on analyses of gene flow across the species’ range in China. This 31 implies that the species may potentially have a scale-dependent dispersal strategy, 32 with females frequently dispersing further than males at the local level, but a 33 proportion of males occasionally disperse long distances, contributing more to gene 34 flow at a larger geographic scale. Long-distance dispersal by male black-throated tits 35 may be induced by competition for resources or by unfavourable environmental 36 conditions, warranting further investigation, but our findings increase evidence that 37 geographic scale is an important factor to be considered when investigating animal 38 dispersal patterns. 39 KEYWORDS: Aegithalos concinnus black-throated tit long-distance dispersal 40 mark-recapture microsatellite – scale-specific dispersal – sex-biased dispersal 41 short-distance dispersal. 2 42 INTRODUCTION 43 Animal dispersal patterns are a major focus of research in evolutionary biology and 44 ecology (Dieckmann et al., 1999; Clobert et al., 2001; Clobert et al., 2012; Jønsson et 45 al., 2016) because they are essential to understand diverse processes, including 46 population dynamics (Paradis et al., 1999; Lowe, 2003), gene flow (Slatkin, 1985; 47 Bohonak, 1999) and speciation (Belliure et al., 2000; Bilton et al., 2002). Dispersal 48 strategies will depend on selective pressures such as availability of resources and 49 mates, and the risk of inbreeding and competition with kin (Pusey, 1987; Dieckmann 50 et al., 1999; Gandon, 1999; Perrin & Mazalov, 2000; Szulkin & Sheldon, 2008). 51 When these selective pressures generate differing trade-offs between males and 52 females of a species, sex-biased dispersal is expected to evolve (Lawson Handley & 53 Perrin, 2007). For example, in many species with polygynous mating systems (e.g. 54 most mammals) where female competition for resources and male competition for 55 mates are usually intense, male-biased dispersal is observed (Greenwood, 1980; 56 Dobson, 1982; Lawson Handley & Perrin, 2007). On the other hand, in many taxa 57 exhibiting monogamous systems (e.g. most passerines) where males must defend a 58 territory in order to pair up with a female and breed, males are expected to be more 59 philopatric (Greenwood, 1980; Greenwood & Harvey, 1982; Clarke et al., 1997). 60 A better understanding of the selection pressures driving sex differences in 61 dispersal within and between species depends on accurate documentation of dispersal 62 patterns, despite the inherent difficulties of doing so. Traditional methods, such as 63 direct observation, capture-mark-recapture and radio-tracking techniques usually only 3 64 allow researchers to work in finite areas, and fail to detect long-distance or infrequent 65 dispersal, thus underestimating gene flow (Slatkin, 1985; Koenig et al., 1996; 66 Prugnolle & De Meeûs, 2002). Genetic techniques, on the other hand, require less 67 intensive field work and can effectively measure the extent of gene flow (Prugnolle & 68 De Meeûs, 2002; Broquet & Petit, 2009; Woltmann et al., 2012; van Dijk et al., 2015; 69 Lagerholm et al., 2017). Genetic results may be consistent with those obtained by 70 observational methods (Temple et al. 2006; Graham et al. 2017), but they sometimes 71 reveal patterns that differ from those found through observation (Baker et al., 2001; 72 Li & Merilä, 2010; Blackmore et al., 2011). Moreover, direct observations are more 73 likely to reveal proximate causes of dispersal than genetic methods (Harris et al., 74 2009). Therefore, it has been argued that these complementary approaches should be 75 integrated to overcome potential biases of a single method (Nathan, 2001; Nathan et 76 al., 2003; Cayuela et al., 2018). 77 A critical distinction between genetic and observational approaches is the spatial 78 scale at which dispersal can be detected (Koenig et al., 1996; Dieckmann et al., 1999; 79 Nathan, 2001; Bowler & Benton 2005), and a growing number of studies have 80 revealed an unexpected role of geographic scale in dispersal patterns. For example, 81 Fontanillas et al. (2004) found that dispersal in greater white-toothed shrews 82 (Crocidura russula) was female-biased at the local scale (breeding-group level), but 83 not at the larger scale (among local populations). Similarly, Gauffre et al. (2009) 84 reported that local-scale dispersal was strongly male-biased in the common vole 85 (Microtus arvalis), while long-distance dispersal was more balanced between sexes. 4 86 An effect of spatial scale on sex-biased dispersal patterns in birds has also been 87 documented. In Siberian jay (Perisoreus infaustus), where male philopatry is 88 observed at a fine spatial scale, Li and Merilä (2010) found strong genetic evidence 89 for male dispersal across populations. In contrast, Cabanis’s greenbuls 90 (Phyllastrephus cabanisi) exhibit female-biased dispersal at small spatial scales, but 91 not at the landscape level (Vangestel et al. (2013). These cases suggest that patterns 92 and underlying mechanisms of sex-biased dispersal are not fully understood. They 93 also demonstrate that combining direct observations and molecular methods may be 94 necessary to overcome scale-dependent biases in dispersal studies and to reliably 95 estimate gene flow resulting from long-distance dispersal. 96 In this study, we used both observational and genetic data to investigate local 97 dispersal of a small passerine bird, the black-throated tit (Aegithalos concinnus). We 98 also use our data to compare local dispersal with long-distance dispersal patterns 99 reported in the literature (see below). The black-throated tit is distributed in South and 100 East Asia, with most of its range occurring in Central and Southern China (Harrap, 101 2008; Zheng, 2017). Using samples collected across its distribution within China, Dai 102 et al. (2013) found evidence for male-mediated gene flow and suggested 103 long-distance male-biased dispersal to occur in this species. However, this 104 male-biased dispersal pattern is contrary to that of the congeneric long-tailed tit (A. 105 caudatus), which shows female-dispersal, at least at the local scale (Sharp et al., 106 2008a; Sharp et al., 2008b; Leedale et al., 2018). Furthermore, the black-throated tit is 107 a facultative cooperative breeder in which males typically provide help at a small 5 108 proportion of nests of nestling stage (Li et al., 2012), a behaviour that is commonly 109 associated with male philopatry in other bird species (Cockburn et al., 2017).
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