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Mitochondrial Dna Variation, Population Structure, and Evolution of the Common Grackle (Quiscalus Quiscula) ’

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Mitochondrial Dna Variation, Population Structure, and Evolution of the Common Grackle (Quiscalus Quiscula) ’ The Condor 93:318-329 0 The CooperOrnithological Society 1991 MITOCHONDRIAL DNA VARIATION, POPULATION STRUCTURE, AND EVOLUTION OF THE COMMON GRACKLE (QUISCALUS QUISCULA) ’ ROBERT M. ZINK, WILLIAM L. ROOTES, AND DONNA L. DITTMANN Museum of Natural Science, Louisiana State University, Baton Rouge, LA 70803 Abstract. The Common Grackle (Quiscalus quiscula) includes two phenotypically dif- ferentiated forms, the Purple Grackle (Q. q. quiscula), which breeds along the Atlantic and Gulf coastsof the United States, and the Bronzed Grackle (Q. q. versicolor), which occurs over the rest of eastern North America. These gracklesmeet and hybridize in a zone that stretchesfrom northeasternto the extreme southcentral United States.We used20 restriction endonucleasesto survey the level and pattern of mitochondrial DNA (mtDNA) variation within and among 35 individuals taken from eight sites. To establish the phylogenetic position of Q. quiscula, we also studiedthe Greater Antillean Grackle (Q. niger), the supposed sister taxon of Q. quiscula, the Boat-tailed Grackle (Q. major), and the Great-tailed Grackle (Q. mexicanus). A relatively high number (29) of clones was detected in Q. quiscula, of which 23 occurredin single individuals. Using resultsof simulations by Avise et al. (1988) we found times to common ancestry of the 31 clones that are much lower than predicted by neutral theory; however, it is likely that long-term effective population sizes of grackles are much lower than current population size, which potentially explains the discrepancy. Sixty-six percent of the birds were genetically most similar to an individual in another population sample, suggestingthat gene flow is high. Inspection of the distribution of in- dividual fragment profiles, composite haplotypes(clones) and a maximum parsimony phy- logenetictree of clones reveals no evidence of geographicvariation. Thus, the mtDNA gene tree is paraphyletic with respectto the “plumage” tree of Q. quiscula. The mtDNA data do not reflect the historical event that lead to the origin of either Purple or Bronzed grackles. The low diversity among clones (P = 0.28%) suggestsa recent common ancestryof clones and recent colonization of North America, which we suggestexplains the lack of geographic variation; plumageevolution must thereforehave occurredrapidly, likely enhancedby sexual selection.The separationof quiscula and niger occurred l-2 MY ago, but it is not clear that these speciesare sister taxa, whereas it is likely that major and mexicanus are. Key words: Common Grackle; Quiscalusquiscula; mitochondrial DNA; population struc- ture; gene flow. INTRODUCTION development of ideas concerning the evolution of populations (Mayr 1963). However, the degree The advent and widespread application of mo- to which morphological patterns of avian geo- lecular methods of detecting genetic variation graphic variation are genetically based is rarely have greatly facilitated empirical estimatesof the tested. It is appropriate therefore, that modem degreeof population subdivision and its relation molecular approachesbe used to describegenetic (if any) to geographic barriers, and the nature variation within and among avian populations and extent of gene flow (Avise et al. 1987). New to provide a new perspectiveon geographicvari- methods of data analysis further encourage the ation. molecular approach to genetic analysis of pop- Although ornithologists laggedbehind workers ulation structure and geographicvariation (e.g., in other fields in applying techniques of protein Slatkin and Maddison 1989). Geographic vari- (allozyme) electrophoresis to problems in geo- ation, in effecta measure of population structure, graphic variation, there is a moderate data base was previously studied by comparisons of exter- now available for birds from the New World nal morphology. Studies of geographicvariation temperate zone (Evans 1987, Zink 1988). In gen- in birds, especially, figured prominently in the eral, most allozyme studies have revealed little or no intraspecific genetic differentiation (Bar- rowclough 1983). In contrast, analysis of the ge- I Received 6 November 1990. Final acceptance24 ography of mitochondrial DNA (mtDNA) dif- January 1991. ferentiation has yielded mixed results in avian [3181 MTDNA AND POPULATION STRUCTURE 319 species.Ball et al. (1988) found little geographic wan, south to New Mexico and the eastern Unit- structure in the Red-winged Blackbird (Age&us ed States. A hybrid zone stretches from the phoeniceus), whereas Avise and Nelson (1989) northeastern United States, southward to Vir- found considerable differentiation between pop- ginia, where it is 200-400 km in width, and west- ulations of the Seaside Sparrow (Ammodramus ward to Louisiana, where it is very narrow (Hun- maritimus). In samples taken from nine geo- tington 1952, Yang and Selander 1968). Yang graphic sites in western North America, Zink (in and Selander (1968) noted that the hybrid zone press)found geographically segregatingmtDNA in Louisiana seemed to have shifted northward differences in Fox Sparrows (Passerella iliaca), between 1930 and 1965, but remained narrow, whereasin samplesof Song Sparrows(Melospiza and that introgression of genes of the Purple melodia) taken at the same sites there was some Grackle into the Bronzed Grackle was much less mtDNA differentiation, but it occurred in a geo- than the reverse. Studies of the hybrid zone re- graphically mosaic pattern. These studies reveal vealed non-assortative mating, which suggested that temperate-breeding avian speciesmight be that the forms were one biological species(Yang more genetically substructuredthan predicted by and Selander 1968). Moore and Dolbeer (1989) the bulk ofallozyme studies(Zink, in press),which studied dispersal characteristics of Q. quiscalus necessitatesadditional mtDNA surveys. and concluded that gene flow is high. Selander Another aspect of population structure that (in Yang and Selander 1968) suggestedthat the can be addressedwith mtDNA concernsneutral, Purple Grackle was closely related to grackle spe- or mutation-genetic drift, theory. Specifically, cies in the Caribbean, in particular the Greater Avise et al. (1988) concluded that under the as- Antillean Grackle (Q. niger), and postulated that sumption of selective neutrality (i.e., mutation a niger-type grackle invaded Florida and sub- and genetic drift), a rate of evolution of 2% per sequently spread into North America. The million years (MY), and a long-term effective Bronzed Grackle was therefore derived and the population size equal to current population size, Purple Grackle “ancestral.” Selander did not several vertebrate species with seemingly high specify where the bronzed phenotype arose. gene flow exhibit far shorter times to common Questions we addressedincluded: what is the ancestry (i.e., less inter-clone diversity) than ex- geographic nature of mtDNA variation among pected. They concluded that long-term effective populations, is there evidence of high gene flow population sizes were much lower than current as postulated by Moore and Dolbeer (1989), do population sizes, a conclusion independently mtDNAs of Bronzed and Purple grackles differ, reached by Barrowclough and Shields (1984) for does the distribution of times to common an- birds. Avise et al.‘s methods and analysis deserve cestry of clones conform to neutral predictions, extension to other speciesto assessthe generality and is Q. niger closer to the purple than to the of their conclusions. This is especially true be- Bronzed Grackle? If Selander’s hypothesisis cor- causethe distributions of alleles detectedby pro- rect, clonal diversity and differencesamong clones tein electrophoresis within and among avian should be greatestin the Purple Grackle because populations are consistent with neutral theory it has been in place longer, and these measures (Barrowclough et al. 1985). should decrease in the Bronzed Grackle to the We studied mtDNA variation in samples of northwest, the presumed path of colonization the Common Grackle (Quiscalusquiscula). This following glacial retreats. To test Selander’s hy- abundant speciesconsists of two forms, formerly pothesisfurther, we determined the phylogenetic consideredseparate species, the Bronzed Grackle relationships of Q. quiscula, Q. niger, and two (Q. q. versicolor),and Purple Grackle (Q. q. quis- other congeners,the Boat-tailed Grackle (Q. ma- cula). The forms differ ecologically, in plumage jor), and the Great-tailed Grackle (Q. mexican- color, and morphologically (Yang and Selander us). 1968); the Purple Grackle has a relatively stouter bill and foragesnearer the ground and on more METHODS aquatic prey. Purple Grackles occur in a fairly The following 35 specimens of Q. quisculawere narrow zone along the east coast from the north- used (general locality, n): New York (3), Wis- em United States to Louisiana, except that they consin (4), Minnesota (5), Saskatchewan (4), occur throughout Florida. Bronzed Grackles Missouri (5), northern Louisiana (3), southern range throughout eastern Canada to Saskatche- Louisiana (5), and North Carolina (6) (see Fig. 320 R. M. ZINK, W. L. ROOTES AND D. L. DITTMANN . SASK absence of sites. Some fragment profiles, those .34 derived from endonucleaseswith four-base rec- .I7 ognition sites,were too complicated for inference of sites, and thus both fragments and sites were analyzed separately.We computed genotypic di- versity, G (Nei 1987) as (n/n - 1) (1 - Z J;2), wheref; is the frequency of the ith mtDNA hap- lotype in a sample of n individuals.
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