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P0139-P0150.Pdf The Condor 99~139-150 0 The Cooper Ornithological Society 1997 MOLECULAR VARIATION AND BIOGEOGRAPHY OF ROCK SHAGS1 DOUGLAS SIEGEL-CAUSEY School of Biological Sciences and University of Nebraska State Museum, Lincoln, NE 68588-0118, e-mail: [email protected] Abstract. Molecular analysis of the presentgenetic structureof Rock Shags indicates significant population subdivision probably caused by vicariant disjunction associated with the Llanquihue Glaciation (35,00&15,000 ybp). The formerly continuouspopula- tion was forced into refugia on the Pacific and Atlantic coasts,where they remained with- out contactfor approximately 20,000 years. With amelioration of the climate and conse- quent glacial retreat, populationsrecolonized rocky shorelinesin the central portion of the present day range and introgressedconsiderably. The Chubdt and Falkland popula- tions serve as genetic sourcesfor the others, whereas the Fuegian population acts as a genetic sink. The population that is resident on Isla Chiloe is enigmatic and in nonequi- librium, possibly the result of indirect effects by a yet unsampled population. Key words: vicariance biogeography,population genetics,Fuego-Patagonia, glacia- tion, Phalacrocoracidae, Stictocarbomagellanicus. INTRODUCTION period of similar magnitude occurred at the Pliocene-Pleistocene boundary, 1.2-l .O million Vicariance biogeographic models postulate that ybp. At maximum, the Llanquihue glacial allopatric remnants of a formerly continuous sheets covered the southern Andes from ap- population are created by the interposition of a proximately 40”s latitude to the Fuegian archi- barrier to gene flow (Platnick and Nelson 1978). pelago, and east to the Atlantic coast to about The most widely studied of these vicariance 52”s latitude. During this period, the Fuegian events have been the Pleistocene glaciations of coastline (i.e., Pacific coast of southern Chile, the Northern Hemisphere (e.g., Hoffmann Tierra de1 Fuego, and the Atlantic coast of 1976). In typically studied cases, the range of a southern Argentina) probably was uninhabitable species was disrupted by the advancing ice by coastal breeding animals, because formerly- sheet which displaced the population into refu- used shoreline habitats were subsequently cov- gia of varying sizes. Once confined to a glacial ered by ice or drastically altered by changing refugium, the species experienced novel condi- sea levels (Mercer 1976, Vuilleumier 1985). tions of habitat and species mix that presented Based on geological and fossil evidence, coastal a unique set of selection pressures, likely dif- refugia existed in the Falkland Islands (Islas ferent for each refugium (Hoffmann 1981). Gla- Malvinas) as well as the adjacent Burdwood cial retreat removed the geographical barrier Bank that was exposed by lowered sea levels, and created a natural ecological experiment in the Atlantic coast of northern Argentine Patago- which populations once isolated were then re- nia, and in regions north of Isla Chiloe, Chile introduced. How isolation by vicariance may (Vuilleumier 1971). Evidence to date indicates have played a role in the present genetic struc- that the fauna of patagonian Chile, patagonian ture of species is a problem critical to under- Argentina, and Tierra de1 Fuego (i.e., Fuego- standing the role of biogeography in speciation Patagonia) experienced changes as profound as events. those studied in the northern hemisphere (Vuil- For southern South America, the Llanquihue leumier 1971, 1985, Bdz and Scillato Yane Glaciation (35,00&15,000 years before present 1979, Simpson 1979, Fjeldsg 1985, Haffer [ybp]) was the only major glaciation event of 1985, Rasmussen 1987, 1991). In order to as- the Pleistocene (Mercer 1976); the next glacial sess the magnitude and effect of the Llanquihue Glaciation on coastal animals, I analyzed the ’ ’ Received 8 December 1995. Accepted 1 October patterns of intraspecific genetic variation in 1996. Rock Shags (Phalacrocoracidae: Stictocarbo U391 140 DOUGLAS SIEGEL-CAUSEY 1936, Siegel-Causey 1986, Rasmussen 1987, Siegel-Causey and Bromley, unpubl. data). L These and other details of natural history and IN ecology suggest that the Llanquihue Glaciation had great impact upon the present genetic struc- ture of Rock Shags. There are several altema- tive hypotheses relating to a population-level response to a glacial vicariance event in south- em South America. The Llanquihue Glaciation could have forced birds onto (a) a Pacific coast refuge, (b) an Atlantic coast refuge, or (c) both Pacific and Atlantic refuges. The null hypoth- esis is (d) there were no refuges or dispersals associated with the Llanquihue Glaciation. Post-glaciation dispersal in hypotheses a, b, and c was bicoastal, because that is the present lim- its of distribution. Choosing among alternative hypotheses will require scrutiny of the gene LI 500 km flow patterns among the present populations of Rock Shags. For example, hypothesis a predicts FIGURE 1. Distribution of Stictocarbo magellani- that gene flow patterns will be unidirectional cus in the Fuego-Patagonian regions of Argentina and from Isla ChiloC through Tierra de1 Fuego to Chile in southern South America. Sampled popula- Chub&, Argentina, whereas hypothesis b pre- tions are: Chubht (stippling), Santa Cruz (diagonal dicts the opposite. Hypothesis c predicts that lines), Isla Malvinas (Falkland Islands) (light shad- ing), Tierra de1 Fuego (dark shading). The breeding gene flow patterns will be centripetal and fo- distribution of Pacific populations is largely un- cused on Tierra de1 Fuego. If there is no sig- known, except for Isla Chiloe, and putative limits are nificant pattern of gene flow, or no differences indicated by dotted lines. Sampled colonies are indi- among populations, then the null hypothesis cated by closed circles. will not be falsified. In this study, I examine the geographic variation in allozymic loci in Rock Shags collected throughout the breeding range magellanicus), an endemic seabird of Fuego- and I use various genetic measures to assessthe Patagonian marine littoral habitats (Fig. 1). magnitude and direction of putative gene flow Rock Shags are primarily cliff-nesting birds among present day populations. feeding in shallow onshore waters and are de- pendent upon suitable rocky coastlines for MATERIALS AND METHODS breeding, feeding, and roosting habitats (Mur- Tissue samples from 90 Rock Shags were col- phy 1936, Siegel-Causey 1986, Punta and Sara- lected at coastal sites in Fuego-Patagonian Ar- via 1993). The present distribution of Rock gentina and Chile from 1985 to 1987. Locali- Shags includes the region that matches pre- ties in Argentina included Puerto Melo (Chubut cisely the extent of the Llanquihue Glaciation Province), Puerto Deseado and Monte Leon plus Atlantic coastal Patagonia and the Falkland (Santa Cruz Province), and Ushuaia (Tierra de1 Islands; although Rock Shags are essentially a Fuego); in Chile, Challahue and Isla ChiloC marine bird, small freshwater populations have (Region X). Tissues from three Rock Shags been discovered on Lago Fagnano in Tierra de1 were obtained from the Falkland Islands in Fuego within flying distance of rocky marine 1984. Morphological and natural history data shores (Chebez and Gomez 1988). Rocky habi- (Siegel-Causey, unpubl. data), and preliminary tats are patchy throughout Fuego-Patagonia and genetic data using RFLP analysis (Bromley and their disappearance as a result of a growing ice Siegel-Causey, unpubl. data) indicated that sheet might extirpate Rock Shags from large birds collected from the two localities in Santa parts of its former range. Previous studies have Cruz Province were not distinct, so these were indicated regional differences in plumage, mor- analyzed together. Liver, pectoral muscle, and phology, and behavior, which suggests that heart muscle were collected, frozen in liquid ni- population subdivision is important (Murphy trogen within three hours of collection, and MOLECULARBIOGEOGRAPHYOFROCKSHAGS 141 transported by air on dry ice at liquid nitrogen e,, = Cnij - Eij) temperatures, and thereafter stored in an ultra- LJ v$ cold freezer at -70°C. Tissues were homog- enized by mortar and pestle at 4°C in a grind- where nij is the observed occurrence of a given ing buffer with a 1% NADP-mercaptoethanol genotype and E, is the expected number. An es- solution and then centrifuged at 6,000X g for 5 timate of the variance of eij can be calculated minutes. The supematant was stored at -70°C as follows (Everitt 1977): until used for electrophoresis. All supematants were analyzed within 90 days of preparation. vii= (1-E)(l -z) I surveyed 39 enzyme systems comprising 65 presumptive allozymic loci. All loci were exam- where ni+ is the row total, n+j the column to- ined for all individuals at least twice. The rep- tal, and n++ the grand total of observed values. licate runs were designed to detect possible With the estimate of the variance, vii, the stan- cryptic differences in mobility of alleles, poten- dardized residual can be transformed to a stan- tial post-translational modifications of allo- dard normal deviate with mean of zero and unit zymes caused by extended freezing and re- variance. The transformation yields an adjusted peated freeze-thaw cycles. Presumptive loci residual defined as (Ever&t 1977): were visualized using techniques and recipes summarized in Murphy et al. (1990). Electro- d, = -& phoreses were carried out on horizontal 10% starch gels or on vertical polyacrylamide slab These values are distributed as
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