Morphological adaptation with no mitochondrial DNA differentiation in the coastal plain Swamp Sparrow

RUSSELL GREENBERG,14 PEDRO J. CORDERO,2,5 SAM DROEGE,3 AND ROBERT C. FLEISCHER2 Smithsonian Migratory Bird Center and 2Molecular Genetics Laboratory, National Zoological Park, Smithsonian Institution, Washington, D.C. 20008, USA; and 3Biological Resources Division, US. Geological Survey, Patuxent Wildlife Research Center, Laurel, Maryland 20708, USA

ABSTRACT.-We estimated genetic differentiation between morphologically distinct tidal marsh populations of Swamp Sparrows (Melospiza georgiana nigrescens) and the more widespread inland populations (M. g. georgiana and M. g. ericrypta). The tidal marsh populations are consistently grayer with more extensive black markings (particularly in the crown), and their bills are larger. These differences are variously shared with other species of salt marsh birds and small mammals. We analyzed mitochondrial DNA sequences (5' end of control region, COII /t-lys/ATPase8, and ND2) of Swamp Sparrows and found low levels of genetic variation and no evidence of geographic structure. These results suggest a rapid and recent geographic expansion of Swamp Sparrows from restricted Pleistocene populations. Morphological differentiation has occurred without long-term genetic isolation, suggesting that selection on the divergent traits is intense. The grayer and more melanistic plumage is probably cryptic coloration for foraging on tidal mud, which tends to be grayish as a result of the formation of iron sulfides, rather than iron oxides, under anaerobic conditions. Received 14 May 1997, accepted 9 January 1998.

VERTEBRATES SHOW CONSPICUOUS ADAPTATIONS to the distinct environment of tidal marshes. For example, diurnal terrestrial species tend toward grayish or blackish coloration (Grinnell 1913, Von Bloeker 1932, Greenberg and Droege 1990). In addition, emberizid finches often have relatively large bills compared with non-tidal populations (Greenberg and Droege 1990). Tidal marsh populations often are small and geographically restricted compared with inland populations. This leads to the question of how distinct morphological features evolve in these populations in the face of potential gene flow from larger inland populations. Few studies have addressed the degree of geographic genetic structuring in species with tidal and inland forms.

Swamp Sparrows (Melospiza georgiana) breed in tidal marshes of Delaware and Chesapeake bays and in inland fresh water wetlands within formerly glaciated areas and occur only sporadically south of the glacial line, inhabiting the few suitable postglacial bogs, brushy marshes, and wet meadows. Except for a few scattered populations, a hiatus extends between the inland and coastal Swamp Sparrow populations through the Piedmont of Maryland and Pennsylvania, leaving the only potential area of significant contact in northern New Jersey and southern New York State (Greenberg and Droege 1990: figure 1).

Coastal Plain Swamp Sparrows (M. g. nigrescens) have more extensive black coloration (e.g. almost three times the area of black in the crown), are generally grayer, and have bills that average 29% greater in overall volume than Swamp Sparrows from inland populations (Greenberg and Droege 1990). In contrast to the morphological differentiation between the estuarine and the closest freshwater populations, the interior subspecies (M. g. ericrypta and M. g. georgiana) are morphologically quite uniform across their ranges, with the two recognized subspecies exhibiting only slight differences in the degree of pale markings on the back.

Three possible scenarios can account for the evolution of the nigrescens subspecies: (1) tidal marsh populations have been genetically isolated from other populations for a substantial period of time; (2) selective pressures differ and are of sufficient magnitude to cause strong and rapid morphological divergence in the face of continued gene flow from inland populations and/or despite recent range expansions that have not allowed sufficient time for mitochondrial DNA (mtDNA) divergence; and (3) morphological differences are environmentally induced (Von Bloeker 1932, James 1983, Price and Pavelka 1996). To examine these scenarios, we measured the degree of genetic differentiation in rapidly evolving regions of mtDNA between the estuarine (M. g. nigrescens) and inland populations (M. g. ericrypta and M. g. georgiana) of Swamp Sparrows.

METHODS

Field collections.-Adult and nestling M. g. nigrescens were collected during the breeding season (June and July) near Delaware Bay (Weeksville and Dividing Creek, Cumberland County, New Jersey, n = 7) and Chesapeake Bay (Black Marsh, Baltimore County, Maryland, n = 4; see Fig. 1). Members of inland populations were collected during the breeding season from Finzel Swamp, Garrett County, Maryland (M. g. georgiana, n = 5) and Clay County, Minnesota (M. g. ericrypta, n = 2) or during migration (Edgewater, Anne Arundel County, Maryland, n = 7; Dividing Creek, Cumberland County, New Jersey, n = 1; Minneapolis, Minnesota, n = 3). The subspecies identity (i.e. nigrescens versus non-nigrescens) for all migrants was verified based on the diagnostic features determined by Greenberg and Droege (1990). We could not ascertain whether migrants were M. g. ericrypta or M. g. georgiana; however, it is likely that the Maryland and Minnesota migrant samples represent birds that originated from eastern and more western parts of the breeding range, respectively. Adults were sacrificed, transported on dry ice to a freezer at -60C, and ultimately prepared as tissue samples and study skins (see Greenberg and Droege 1990); nestlings were raised in captivity and prepared as study skins when they died.