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Implications for Population Divergence. Author(S): Julie E The University of Chicago Female, but Not Male, Tropical Sparrows Respond More Strongly to the Local Song Dialect: Implications for Population Divergence. Author(s): Julie E. Danner, Raymond M. Danner, Frances Bonier, Paul R. Martin, Thomas W. Small, and Ignacio T. Moore Source: The American Naturalist, Vol. 178, No. 1 (July 2011), pp. 53-63 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/10.1086/660283 . Accessed: 26/06/2014 10:22 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press, The American Society of Naturalists, The University of Chicago are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist. http://www.jstor.org This content downloaded from 128.173.125.76 on Thu, 26 Jun 2014 10:22:38 AM All use subject to JSTOR Terms and Conditions vol. 178, no. 1 the american naturalist july 2011 Female, but Not Male, Tropical Sparrows Respond More Strongly to the Local Song Dialect: Implications for Population Divergence Julie E. Danner,1,* Raymond M. Danner,1 Frances Bonier,1,2 Paul R. Martin,2 Thomas W. Small,1 and Ignacio T. Moore1 1. Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia 24061; 2. Department of Biology, Queen’s University, Kingston, Ontario K7L 3N6, Canada Submitted August 11, 2010; Accepted March 15, 2011; Electronically published May 25, 2011 Dryad data: http://dx.doi.org/10.5061/dryad.8837. morphology, occur at higher densities at lower latitudes abstract: In addition to the observed high diversity of species in (Martin and McKay 2004; Martin and Tewksbury 2008). the tropics, divergence among populations of the same species exists over short geographic distances in both phenotypic traits and neutral Similarly, greater neutral genetic divergence is found genetic markers. Divergence among populations suggests great among bird (Hackett and Rosenberg 1990; Chek et al. potential for the evolution of reproductive isolation and eventual 2003) and plant (Eo et al. 2008) populations in the tropics, speciation. In birds, song can evolve quickly through cultural trans- especially when separated by topographic barriers, such as mission and result in regional dialects, which can be a critical com- large rivers and mountains (Brumfield and Capparella ponent of reproductive isolation through variation in female pref- 1996; Bates et al. 1999; Aleixo 2004). erence. We examined female and male behavioral responses to local and nonlocal dialects in two allopatric populations of rufous-collared Given the importance of population divergence for al- sparrows (Zonotrichia capensis) in the Andes Mountains of Ecuador. lopatric speciation, the morphological and genetic differ- Here we show that female sparrows prefer their natal song dialect ences observed among tropical populations over short dis- to the dialect of an allopatric population that is just 25 km away tances suggest a great potential for the evolution of and separated by an unsuitable higher-elevation habitat (pass of 4,200 reproductive isolation and eventual speciation. When pop- m), thus providing evidence of prezygotic reproductive isolation ulations are separated, variation among sexually selected among populations. Males showed similar territorial responses to all conspecific dialects with no consistent difference with respect to dis- traits, such as male mating signals, may increase and then tance, making male territoriality uninformative for estimating re- act as a premating barrier to interbreeding (Coyne and productive isolation. This study provides novel evidence for culturally Orr 2004). For instance, divergent sexually selected vocal based prezygotic isolation over very short distances in a tropical bird. signals in tropical frogs (Ryan et al. 2003; Hoskin et al. 2005; Boul et al. 2007) have been shown to lead to be- Keywords: reproductive isolation, tropics, female choice, song dialects, Zonotrichia capensis. havioral isolation among populations. However, direct measures of components of reproductive isolation among populations, such as measures of female preference for Introduction local versus foreign mates or hybrid fitness, are rare (Mittelbach et al. 2007; Schemske 2009; but see Boul et Many tropical species exhibit among-population diver- al. 2007; Kay and Schemske 2008). Estimating reproductive gence over short geographic distances (Fouquet et al. 2007; Koscinski et al. 2008). Phenotypic traits, including col- isolation is critical for understanding the process and spa- oration and vocalizations, vary over short distances in tial scale of speciation among populations. tropical frogs (Boul et al. 2006) and birds (Nottebohm Song plays an important role in female mate choice and 1969; Nyari 2007; Podos 2007; Seddon and Tobias 2007; reproductive isolation in birds (Nowicki and Searcy 2002). Tobias and Seddon 2009), and bird subspecies, defined by In oscines, song is learned (Marler and Tamura 1964) and dialects can vary among populations (Nottebohm 1969), * Corresponding author; e-mail: [email protected]. arising through both genetic and cultural evolution (Lynch 1996; Podos and Warren 2007). These dialects can have Am. Nat. 2011. Vol. 178, pp. 53–63. ᭧ 2011 by The University of Chicago. 0003-0147/2011/17801-52368$15.00. All rights reserved. important implications for reproductive isolation among DOI: 10.1086/660283 populations (Irwin et al. 2001). A lack of female recog- This content downloaded from 128.173.125.76 on Thu, 26 Jun 2014 10:22:38 AM All use subject to JSTOR Terms and Conditions 54 The American Naturalist nition of or preference for dialects from other populations and asynchronous reproductive phenologies (Moore et al. may serve as a primary prezygotic isolating mechanism 2005). Last, the males in the two study populations sing among bird populations (Martens 1996; Price and Bouvier different song dialects (Moore et al. 2005; fig. 1). 2002; Price 2008). Thus, female response to song could We broadcast songs from conspecific populations that be an informative measure of reproductive isolation occur at different distances from each focal population, as among allopatric populations. However, estimates of re- well as a song from a distantly related control species, and productive isolation among allopatric populations of birds recorded the behavioral responses of both females and typically focus on phenotypic or neutral genetic differences males. Female preference was estimated by the number of (Mayr and Ashlock 1991; Helbig et al. 2002; Price 2008) copulation solicitations given in response to songs. Male or on territorial response to songs from other populations response was measured by behaviors that characterize ter- (Ratcliffe and Grant 1985; Grant and Grant 2002; Irwin ritoriality, including their approach toward the broadcast et al. 2005; Seddon and Tobias 2007; Uy et al. 2009). speaker and vocalizations. Studies of tropical species rarely consider female mate choice, despite its significance in prezygotic isolation and Female Trials speciation of birds (Price and Bouvier 2002; Price 2008). We examined both female preference for and male ag- We used mist nets to capture 13 female and 4 male Z. gressive response toward male song over differing geo- capensis from each of the two Ecuadorian populations be- graphic distances in a nonmigratory tropical bird, the fore the start of their respective breeding season (Papal- rufous-collared sparrow (Zonotrichia capensis). Despite the lacta: late July–August 2007; Pintag: May–June 2008). The large geographic range of Z. capensis, variation in song experiments were conducted at different times of the year dialects can be observed over short geographic distances to correspond with the respective breeding seasons at each (20 km; Lougheed et al. 1989) and in the presence or site. We implanted females with two subcutaneous silastic absence of geographic barriers (Nottebohm 1969, 1975; implants filled with 17b-estradiol (length p 12 mm, Handford and Nottebohm 1976; Moore et al. 2005). We inner diameter p 1.47mm, outer diameter p 1.96 mm; specifically asked the following two questions: How does Dow Corning; O’Loghlen and Beecher 1997) to heighten female preference for male song dialect vary with geo- the females’ reproductive receptiveness and to control for graphic distance between populations? And given that individual hormonal variation (Moore 1982). It is worth male response is often used to estimate biological species noting that smaller doses of 17b-estradiol might have suf- limits in birds, how do patterns of female preference for ficed, but this dose was chosen on the basis of previous male song compare with male territorial response to the studies. We allowed each bird 7 days to recover from sur- same songs? We predicted that females would prefer the gery and to allow hormone levels to stabilize before per- local dialect. Furthermore, we predicted that females forming the song-preference trials. To avoid interference would display a higher level of discrimination among di- by local male birds during
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