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The Song Sparrow, Melospiza Melodia, As a Ring Species 35

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The Song Sparrow, Melospiza Melodia, As a Ring Species 35 Systematics and Biodiversity 7 (1): 33–62 Issued 22 February 2009 doi:10.1017/S1477200008002867 Printed in the United Kingdom C The Natural History Museum Michael A. Patten1, 2, 3∗ & Christin L. Pruett1, 2 The Song Sparrow, Melospiza melodia,as 1Oklahoma Biological Survey, University of Oklahoma, a ring species: patterns of geographic Norman, Oklahoma 73019, USA 2Sutton Avian Research Center, University of Oklahoma, Box variation, a revision of subspecies, and 2007, Bartlesville, Oklahoma 74005, USA implications for speciation 3San Diego Natural History Museum, P.O. Box 121390, San Diego, California 92112, USA Abstract Identification and analysis of ring species are important to our understand- submitted April 2007 accepted June 2008 ing of evolution and speciation. We review geographic variation in the Song Sparrow (Melospiza melodia) in the context of a ring species, one of few known from the highly vagile class Aves. Although 52 subspecies have been named, our reassess- ment of morphological variation across the entire species reveals that 25 subspecies are diagnosable throughout the species’ range, which includes much of the North American continent. We include an analysis of plumage variation in M. m. heermanni of coastal California and M. m. fallax of the Sonoran Desert and a description of the contact zone between these subspecies, which forms the contact points of a ring centred around the Sierra Nevada and Mojave Desert. These two subspecies come into contact in a narrow hybrid zone, where interbreeding is limited. In addition to substantial differences in plumage, songs of these subspecies vary concomitantly with differences in the structure of occupied habitat. Females tend to exhibit assort- ative preferences for plumage and song and males exhibit assortative recognition (and associated agonistic behaviour) of song. Plumage variation across the Song Sparrow varies according to climate and habitat, suggesting both geographical and ecological components to the species’ diversification. Key words geographic variation, Melospiza melodia, ring species, subspecies, speciation We question whether study of geographic variation of intermediate forms. The pattern of variation in ring species in song sparrows leads to insights concerning demonstrates that intraspecific variation can be great enough speciation. to lead to species formation – that the microevolutionary pro- cesses that lead to population differentiation are related to the Zink and Dittmann (1993) processes that lead to speciation (Irwin et al., 2001a; Irwin & Irwin, 2002). In other words, differences among individuals Introduction are of the same kind as differences among populations, which in turn are of the same kind as differences among species. The study of geographic variation has formed, in animals at These differences are only a matter of degree. least, the basis for our understanding of speciation (Mayr, Classic ring species are well documented in the mouse 1942). Ring species exemplify perhaps the most interesting Peromyscus maniculatus (Murie, 1933), the salamander En- pattern of variation. A ‘ring species’ is a species comprised of satina eschscholtzii (Moritz et al., 1992; Alexandrino et al., multiple subspecies whose connected ranges form a circle or 2005; Kuchta, 2005; Wake, 2006; cf. Highton, 1998; Wake ring (Mayr, 1942; Irwin et al., 2001a; Irwin & Irwin, 2002) & Schneider, 1998), and the millipede Rhymogona monti- and whose subspecies at opposite poles of the ring behave vaga (Pedroli-Christen & Scholl, 1996), with more conten- like good biological species (or nearly so), in that they are tious examples in the pocket mouse Perognathus longimem- reproductively isolated (and, typically, morphologically or be- bris/P. amplus (McKnight, 1995), the mouse Mus musculus haviourally distinct from each other). Subspecies connecting (Bonhomme, 1994), the tree Acacia karroo (Brain, 1989), and these endpoints grade into each other to form a continuous set the butterfly Junonia lavinia (Mayr 1942:181). See Irwin et al. (2001a, b) for reviews and critiques of these and other claimed ∗Corresponding author. Email: [email protected] ring species. 33 34 Michael A. Patten and Christin L. Pruett Mayr’s (1942:182) comment that ring species are ‘rather and the evidence from the connecting points of the ring are frequent’ in birds notwithstanding, most evolutionary biolo- strongly associated with ecological factors (e.g. habitat struc- gists have assumed that they would be rare in birds, if not ture, temperature, rainfall). In this respect, the Song Sparrow is impossible, principally because birds are so mobile. Indeed, an excellent species in which to study the process of speciation, various examples in birds do not hold up to scrutiny. The text- from both geographical and ecological perspectives. book case of the Herring Gull (Larus argentatus) complex encircling the North Pole (Mayr, 1940; Ridley, 1993:41), for example, does not appear to constitute a true ring species: Geographic variation in the Song neighbouring subspecies are allopatric or different biological Sparrow species (Cramp & Simmons, 1983; Kennerley et al., 1995; American Ornithologists’ Union, 1998), and recent genetic re- The Song Sparrow is generally of medium build, though its search supports a model of divergence by vicariance in glacial size varies substantially, ranging from as large as a Califor- refugia rather than isolation by distance in a ring (Liebers et al., nia Towhee (Pipilo crissalis; ± 50 g) in the Aleutian Islands 2004). The Great Tit (Parus major) was also thought to be a of Alaska to as small as a Savannah Sparrow (Passerculus ring species across Eurasia (Mayr, 1940; Martens, 1996), but sandwichensis; ± 18 g) on the Channel Islands of California this example is confounded by recent sympatry resulting from (Aldrich, 1984; Rising, 1996). Its plumage is generally char- habitat alteration by humans (Nazarenko et al., 1999), and acterised by a streaked breast and mantle, although popula- the purported ‘ring’ may be comprised of three reproductively tions on the Mexican Plateau are spotted below, with the white isolated species (Packert¨ et al., 2005). None of the various throat unstreaked, away from Alaska and the Pacific Northw- examples of ‘ring species’ mentioned by Phillips (1959), in- est, ventral streaking typically coalesces into a central breast cluding the Mallard (Anas platyrhynchos) complex in the USA spot. Streaking or spotting is generally well defined on a whit- and Canada, seems plausible, chiefly because they do not form ish, grey, olive, or pale brown background; streak colour varies rings – there are no taxa behaving as good species at the from black to pale rufous. Broad lateral crown stripes border endpoints. Even by his own standards Mayr’s (1940, 1942) a pale central stripe, but a contrasting central crown is often additional examples – Halcyon kingfishers in Micronesia, the inconspicuous. Irides and other bare parts are dark brown to Phylloscopus collybita complex (now split into 3–4 allospe- blackish. cies), Zosterops white-eyes in the Lesser Sunda Islands, Lalage The Song Sparrow is often regarded as the most poly- trillers in the southern Celebes (Sulawesi), and Pernis honey- typic and variable species in North America (Miller, 1956) buzzards in the Philippines – require further study. Easily the and vies with the Horned Lark (Eremophilus alpestris)and best possibility for a true ring species in birds is offered by pop- Yellow Wagtail (Motacilla flava) as the most polytypic bird ulations of the Greenish Warbler (Phylloscopus trochiloides)in species in the northern hemisphere, though each is less so Asia (Ticehurst, 1938; Mayr, 1942; Irwin & Irwin, 2002), with than the Golden Whistler (Pachycephala pectoralis)ofAus- recent research showing introgression between neighbouring tralasia, the most polytypic in the world (Mayr & Diamond, populations in the ring and subspecies acting as biological spe- 2001). Variation across the Song Sparrow’s range is substan- cies at the contact point of the ring (Irwin, 2000; Irwin et al., tial and complex in both size (Aldrich, 1984) and plumage 2001a, b; Irwin & Irwin, 2002; Irwin et al., 2005). (Dickerman, 1963; Rising, 1996), with little apparent asso- We present evidence that Song Sparrow (Melospiza ciation between mitochondrial DNA (mtDNA) and morpho- melodia) populations of southwestern North America consti- logical differentiation (Zink, 1991; Zink & Dittmann, 1993; tute a ring species. The Sierra Nevada and Mojave Desert lie Fry & Zink, 1998), although recent studies using more rap- at the ring’s centre. The connecting point is between M. m. idly evolving microsatellite loci have detected a correlation heermanni and M. m. fallax in the southern Coachella Valley between morphology and genes (Chan & Arcese, 2002, 2003; (Patten et al., 2004b), which extends southeast across a steep Patten et al., 2004; Pruett & Winker, 2005; Pruett et al., 2008b). ecological gradient through the San Gorgonio Pass, a deep rift We feel that subspecies are an excellent surrogate for underly- that separates the Transverse and Peninsular Ranges of south- ing variation in the nuclear genome. ern California. This pass is the site of various other meeting Patterns of geographic variation in the Song Sparrow fol- points between coastal and desert taxa (e.g. see Patten et al., low Gloger’s rule, a common trend in North American birds 2003, 2004a). Despite differences in plumage, M. m. heer- (Zink & Remsen, 1986), with the darkest, most heavily pig- manni
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