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Vocal dialect and genetic subdivisions along a geographic gradient in the orange-tufted sunbird

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Abstract

At least four hypotheses have been suggested to explain the formation and maintenance of song dialects among birds: historic processes (epiphenomenon), genetic or local adaptation, acoustic adaptation, and social adaptation. We studied spatial and temporal distribution of dialect in the orange-tufted sunbird (Nectarinia osea), a small nectarivorous bird that expanded its breeding range in Israel during the past 100 years from the southern part of Rift Valley to the entire country. Sunbird range expansion was concurrent with the establishment of many small settlements with an ethos of gardening, which introduced many ornithophilous plants. We recorded songs and genetically screened individual sunbirds in 29 settlements distributed across a 380 km north–south gradient along the Rift Valley. We show that dialects cluster together into geographical regions in 70% of cases, a moderate concurrence to geography. Settlement establishment date, geographical position, and genetic distance between local populations (i.e., settlements) were all poor predictors for the variance among song dialects. The specific effect of habitat was not tested because all sampled localities were similar in their physical and acoustic properties. Using a network analysis, we show that dialects seem to aggregate into several network communities, which clustered settlement populations from several regions. Our results are best explained by either the epiphenomenon hypothesis or the social adaptation hypothesis, but at present our data cannot state unequivocally which of these hypotheses is better supported. Last, we discovered a negative association between network centrality and genetic diversity, a pattern that requires further examination in other systems.

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References

  • Aharoni I (1943/6) Memories of a zoologist. Am Oved, Tel Aviv. In Hebrew.

  • Andrew RJ (1962) Evolution of intelligence and vocal mimicking. Science 137:585–589

    Article  PubMed  CAS  Google Scholar 

  • Baker MC (1982) Vocal dialect recognition and population genetic consequences. Am Zool 22:561–569

    Google Scholar 

  • Baker MC, Cunningham M (1985) The biology of bird-song dialects. Behav Brain Sci 8:85–133

    Article  Google Scholar 

  • Baker MC, Spitler-Nabors KJ, Bradley DC (1981) Early experience determines song dialect responsiveness of female sparrows. Science 214:819–820

    Article  PubMed  CAS  Google Scholar 

  • Baker MC, Bierke TK, Lampe H, Espmark Y (1986) Sexual response of female great tits to variation in size of male’s song repertoires. Am Nat 128:491–498

    Article  Google Scholar 

  • Baptista LF (1975) Song dialects and demes in sedentary populations of the white-crowned sparrow (Zonotrichia leucophrys nuttalli). Publ Zool Univ Calif 105:1–52

    Google Scholar 

  • Brenowitz EA (1982) Long-range communication of species identity by song in the red-winged blackbird. Behav Ecol Sociobiol 10:29–38

    Article  Google Scholar 

  • Brown TJ, Handford P (2000) Sound design for vocalizations: quality in the woods, consistency in the fields. Condor 102:81–92

    Article  Google Scholar 

  • Catchpole CK, Slater PJB (2008) Bird song: biological themes and variations. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Cheke RA, Mann CF, Allen R (2001) Sunbirds. Yale University Press, New Haven

    Google Scholar 

  • Clarke KR, Ainsworth M (1993) A method of linking multivariate community structure to environmental variables. Mar Ecol Prog Ser 92:205–219

    Article  Google Scholar 

  • Clarke KR, Gorley RH (2006) PRIMER v6: user manual/tutorial. Primer-e, Plymouth

    Google Scholar 

  • Coleing A (2009) The application of social network theory to animal behaviour. Biosci Horiz 2:32–43

    Article  Google Scholar 

  • Enis R, Ben Arav Y (1994) Gardens and landscape in the kibbutz: 60 years of development (1910–1970). Ministry of Defense Publishing House, Tel Aviv, In Hebrew

    Google Scholar 

  • Fahn A, Zohary M (1981) The cultivated plants of Israel. Hakibbutz Hameuchad, Tel Aviv, In Hebrew

    Google Scholar 

  • Freeman LC, Borgatti SP, White DR (1991) Centrality in valued graphs: a measure of betweenness based on network flow. Soc Networks 13:141–154

    Article  Google Scholar 

  • Gibbs HL (1990) Cultural evolution of male song types in Darwin’s medium ground finch Geospiza fortis. Anim Behav 39:253–263

    Article  Google Scholar 

  • Girvan M, Newman MEJ (2002) Community structure in social and biological networks. Proc Natl Acad Sci USA 99:7821–7826

    Article  PubMed  CAS  Google Scholar 

  • Goudet J (1995) FSTAT (vers. 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Grimes LG (1974) Dialects and geographical variation in the song of the splendid sunbird Nectarinia coccinigaster. Ibis 116:314–329

    Article  Google Scholar 

  • Handford P, Nottebohm F (1976) Allozymic and morphological variation in population samples of rufous-collared sparrow, Zonotrichia capensis, in relation to vocal dialects. Evolution 30:802–817

    Article  Google Scholar 

  • Hansen P (1979) Vocal learning: its role in adapting sound structures to long-distance propagation and a hypothesis on its evolution. Anim Behav 27:1270–1271

    Article  Google Scholar 

  • Inbar R (1975/6) The birds of Eretz Israel. Yavneh, Tel Aviv, In Hebrew

  • King JR (1972) Variation in the song of the rufous collared sparrow, Zonotrichia capensis, in northwestern Argentina. Z Tierpsychol 30:344–373

    Article  Google Scholar 

  • Leader N, Wright J, Yom-Tov Y (2000) Microgeographic song dialects in the orange-tufted sunbird (Nectarinia osea). Behaviour 137:1613–1627

    Article  Google Scholar 

  • Leader N, Wright J, Yom-Tov Y (2002) Dialect discrimination by male orange-tufted sunbirds (Nectarinia osea): reactions to own and neighboring dialects. Ethology 108:367–376

    Article  Google Scholar 

  • Leader N, Wright J, Yom-Tov Y (2005) Acoustic properties of two urban song dialects in the orange-tufted sunbird (Nectarinia osea). Auk 122:231–245

    Article  Google Scholar 

  • Leader N, Geffen E, Mokady O, Yom-Tov Y (2008) Song dialects do not restrict gene flow in an urban population of the orange-tufted sunbird Nectarinia osea. Behav Ecol Sociobiol 62:1299–1305

    Article  Google Scholar 

  • Lougheed SC, Handford P (1992) Vocal dialects and the structure of geographic variation in morphological and allozymic characters in the rufous-collared sparrow, Zonotrichia capensis. Evolution 46:1443–1456

    Article  Google Scholar 

  • Lougheed SC, Handford P, Baker AJ (1993) Mitochondrial-DNA hyperdiversity and vocal dialects in a subspecies transition of the rufous-collared sparrow. Condor 95:889–895

    Article  Google Scholar 

  • Lulav S (1969) In: Kroodsma DE, Miller EH (eds) The population mimetics of birdsong. Ecology and evolution of acoustic communication in birds. Cornell University Press, Ithaca, pp 181–197

    Google Scholar 

  • MacDougall-Shackleton EA, MacDougall-Shackleton SA (2001) Cultural and genetic evolution in mountain white-crowned sparrows: song dialects are associated with population structure. Evolution 55:2568–2575

    PubMed  CAS  Google Scholar 

  • McLachlan GJ (1992) Discriminant analysis and statistical pattern recognition. Wiley Interscience

  • Morton ES (1975) Ecological sources of selection on avian sounds. Am Nat 109:17–34

    Article  Google Scholar 

  • Mundinger PC (1982) In: Kroodsma DE, Miller EH (eds) Microgeographic and macrogeographic variation in the acquired vocalizations of birds. Ecology and evolution of acoustic communication in birds. Cornell University Press, Ithaca, pp 147–208

    Google Scholar 

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19:153–170

    Article  PubMed  CAS  Google Scholar 

  • Newman MEJ, Girvan M (2004) Finding and evaluating community structure in networks. Phys Rev 69:026113

    CAS  Google Scholar 

  • Nelson DA, Marler P (1989) Categorical perception of a natural stimulus continuum—birdsong. Science 244:976–978

    Article  PubMed  CAS  Google Scholar 

  • Nicholls JA, Austin JJ, Moritz C, Goldizen AW (2006) Genetic population structure and call variation in a passerine bird, the satin bowerbird, Ptilonorhynchus violaceus. Evolution 60:1279–1290

    PubMed  CAS  Google Scholar 

  • Noad MJ, Cato DH, Bryden MM, Jenner MN, Jenner KCS (2000) Cultural revolution in whale songs. Nature 408:537–537

    Article  PubMed  CAS  Google Scholar 

  • Nordby JC, Campbell ES, Beecher MD (2007) Selective attrition and individual song repertoire development in song sparrows. Anim Behav 74:1413–1418

    Article  Google Scholar 

  • Nottebohm F (1969) The song of the chingolo (Zonotrichia capensis) in Argentina: description and evaluation of a system of dialects. Condor 71:299–315

    Article  Google Scholar 

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    Article  PubMed  CAS  Google Scholar 

  • Payne RB (1978) Microgeographic variation in songs of the splendid sunbird Nectarinia coccinigaster: population phenetics, habitats, and song dialects. Behaviour 65:282–308

    Google Scholar 

  • Payne RB (1981) Song learning and social interactions in Indigo Buntings. Anim Behav 29:688–697

    Article  Google Scholar 

  • Payne RB, Thompson WL, Fiala KT, Sweany LL (1981) Local song traditions in indigo buntings: cultural transmissions of behavior patterns across generations. Behaviour 77:199–221

    Article  Google Scholar 

  • Paz U (1986) Birds. Vol. 6. In: Alon A (ed) Plants and animals of the land of Israel. Ministry of Defence and SPNI, Israel, In Hebrew

    Google Scholar 

  • Petrinovich L, Patterson TL, Baptista LF (1981) Song dialects as barriers to dispersal: a reevaluation. Evolution 35:180–188

    Article  Google Scholar 

  • Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first generation migrants detection. J Hered 95:536–539

    Article  PubMed  CAS  Google Scholar 

  • Podos J, Warren PS (2007) The evolution of geographic variation in birdsong. Adv Study Behav 37:403–458

    Article  Google Scholar 

  • Proulx SR, Promislow DEL, Phillips PC (2005) Network thinking in ecology and evolution. TREE 20:345–353

    PubMed  Google Scholar 

  • Pytte CL (1997) Song organization of house finches at the edge of an expanding range. Condor 99:942–954

    Article  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201

    Article  PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rothstein SI (1994) The cowbird’s invasion of the far west: history, causes and consequences experienced by host species. Stud Avian Biol 15:301–315

    Google Scholar 

  • Rothstein SI, Fleischer RC (1987) Vocal dialects and their possible relation to honest status signalling in the brown-headed cowbird. Condor 89:1–23

    Article  Google Scholar 

  • Rozenfeld AF, Arnaud-Haond S, Hernandez-Garcia E, Eguiluz VM, Serrao EA, Duarte CM (2008) Network analysis identifies weak and strong links in a metapopulation system. Proc Natl Acad Sci USA 105:18824–18829

    Article  PubMed  Google Scholar 

  • Ruegg K, Slabbekoorn H, Clegg S, Smith TB (2006) Divergence in mating signals correlates with ecological variation in the migratory songbird, Swainson’s thrush (Catharus ustulatus). Mol Ecol 15:3147–3156

    Article  PubMed  CAS  Google Scholar 

  • Ryan MJ, Brenowitz EA (1985) The role of body size, phylogeny, and ambient noise in the evolution of bird song. Am Nat 126:87–100

    Article  Google Scholar 

  • Shirihai H (1996) The birds of Israel. Academic, London

    Google Scholar 

  • Slabbekoorn H, Smith TB (2002a) Bird song, ecology, and speciation. Phil Trans Roy Soc Lond B 357:493–503

    Article  Google Scholar 

  • Slabbekoorn H, Smith TB (2002b) Habitat-dependent song divergence in the little greenbull; an analysis of environmental selection pressures on acoustic signals. Evolution 56:1849–1858

    PubMed  Google Scholar 

  • Slabbekoorn H, Peet M (2003) Birds sing at a higher pitch in urban noise—great tits hit the high notes to ensure that their mating calls are heard above the city’s din. Nature 424:267

    Article  PubMed  CAS  Google Scholar 

  • Slabbekoorn H, Ellers J, Smith TB (2002) Birdsong and sound transmission: the benefits of reverberations. Condor 104:564–573

    Article  Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequency. Genetics 139:457–462

    PubMed  CAS  Google Scholar 

  • Smoli E (1957) Birds in Israel. Massada, Tel Aviv. In Hebrew

  • Soha JA, Nelson DA, Parker PG (2004) Genetic analysis of song dialect populations in Puget Sound white-crowned sparrows. Behav Ecol 15:636–646

    Article  Google Scholar 

  • Statistical Abstracts of Israel (2001) No. 52. Central Bureau of Statistics, Jerusalem

  • Tristram HB (1884) Fauna and flora of Palestine. Palestine Exploration Fund, London

    Google Scholar 

  • Vaknin Y, Yom-Tov Y, Eisikovitch D (1996) Flowering seasonality and flower characteristics of Loranthus acaciae Zucc. (Lorantaceae): implications for advertisement and bird-pollination. Sex Plant Repro 9:279–285

    Article  Google Scholar 

  • Vaneechoutte M (1997) Bird song as a possible cultural mechanism for speciation. J Memetics Evol Models Inform Transm 1

  • Walsh PS (1991) CHELEX-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513

    PubMed  CAS  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wey T, Blumstein DT, Shen W, Jordan F (2008) Social network analysis of animal behaviour: a promising tool for the study of sociality. Anim Behav 75:333–344

    Article  Google Scholar 

  • Wiley RH, Richards DG (1978) Physical constraints on acoustic communication in atmosphere—implications for evolution of animal vocalizations. Behav Ecol Sociobiol 3:69–94

    Article  Google Scholar 

  • Wright TF, Wilkinson GS (2001) Population genetic structure and vocal dialects in an Amazon parrot. Proc Royal Soc Lond B 268:609–616

    Article  CAS  Google Scholar 

  • Wright TF, Rodriguez AM, Fleischer RC (2005) Vocal dialects, sex-biased dispersal, and microsatellite population structure in the parrot Amazona auropalliata. Mol Ecol 14:1197–1205

    Article  PubMed  CAS  Google Scholar 

  • Yom-Tov Y, Mendelssohn H (1988) Changes in the distribution and abundance of vertebrates in Israel during the 20th century. In: Yom-Tov Y, Tchernov E (eds) The zoogeography of Israel. Dr. W. Junk, Dordrecht, pp 515–547

    Google Scholar 

  • Zilberman R, Moav B, Yom-Tov Y (2001) Territoriality and mate guarding in the Orange-tufted Sunbird. Israel J Zool 47:275–286

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Dini Eisikovitz, Yossi Lev-Ari, and Uzi Paz for unpublished information and advice; to Stephen I. Rothstein, Jonathan Wright, and Shai Markman for their constructive comments; and to Naomi Paz for editing the article. We acknowledge useful suggestions and constructive criticism provided by Melissa Hughes and three anonymous reviewers. This research was supported by The Israel Science Foundation (grant no. 900/04) to YYT and by the Israel Cohen Chair for Environmental Zoology to YYT.

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Authors and Affiliations

  1. Department of Zoology, Tel Aviv University, Tel Aviv, 69978, Israel

    Kinneret Yoktan, Eli Geffen, Amiyaal Ilany, Yoram Yom-Tov, Adit Naor & Noam Leader

  2. Ecology Department, Israel Nature and Parks Authority, Jerusalem, 95463, Israel

    Noam Leader

Authors
  1. Kinneret Yoktan
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  2. Eli Geffen
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  3. Amiyaal Ilany
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  4. Yoram Yom-Tov
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  5. Adit Naor
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  6. Noam Leader
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Correspondence to Eli Geffen.

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Communicated by M. Hughes

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Location means (±SD) of the seven trill variables used (DOC 89 kb)

Appendix 1

Appendix 1

Number of components (i.e., a component is a set of connected populations) and mean component diameter as a function of squared Mahalanobis distance threshold value. The network percolation point is defined as the threshold squared Mahalanobis value where number of components equals one (i.e., single network with all populations connected) and the mean component diameter is maximal.

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Yoktan, K., Geffen, E., Ilany, A. et al. Vocal dialect and genetic subdivisions along a geographic gradient in the orange-tufted sunbird. Behav Ecol Sociobiol 65, 1389–1402 (2011). https://doi.org/10.1007/s00265-011-1149-7

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