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Intergradation Between the Herring Gull Larus Argentatus and the Southern Herring Gull Larus Cachinnans in European Russia E

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Intergradation Between the Herring Gull Larus Argentatus and the Southern Herring Gull Larus Cachinnans in European Russia E Russian Journal of Zoology, Vol. 3, No. 1, 1999, pp. 129–141. Translated from Zoologicheskii Zhurnal, Vol. 78, No. 3, 1999, pp. 334–348. Original Russian Text Copyright © 1999 by Panov, Monzikov. English Translation Copyright © 1999 by åÄàä “ç‡Û͇ /Interperiodica” (Russia). Intergradation between the Herring Gull Larus argentatus and the Southern Herring Gull Larus cachinnans in European Russia E. N. Panov and D. G. Monzikov Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, 117071 Russia Received January 8, 1998 Abstract—Five gull populations along a 2000-km transect, running from the Barents Sea coast in the Kola Pen- insula to Nizhegorodskaya oblast, were studied with respect to external morphology, vocalization, and DNA features. The transect crosses the easternmost part of the L. argentatus range, as well as areas of the Middle Volga basin inhabited by the gulls of cachinnans-like type. All the morphological and behavioral features proved to form a cline along the transect. Populations of the Barents Sea and the White Sea represent typical L. argentatus, while in those inhabiting the Upper and Middle Volga basin, L. cachinnans features predominate. The population of the Baltic Sea region is intermediate. Comparative DNA analysis by RAPD method has revealed introgression of L. argentatus genes southeastward, up to Nizhegorodskaya oblast, and those of L. cachinnans genes in the opposite direction, to the Baltic Sea. Two scenarios of introgression are discussed: via L. cachinnans omissus dispersal from Fennoscandia along the Volga basin and due to the expansion of the L. c. cachinans range to the north. Both processes may proceed simultaneously. INTRODUCTION In this work, the authors try to analyze another situ- ation of such a kind, namely, the example of interrela- The concept of biological species prevailing in tionships of the herring gulls Larus argentatus and modern zoology is often difficult to apply to real situa- L. cachinnans; this is a situation of allopatric species tions, notwithstanding its apparent similarity and con- sistency. The so-called “large white-headed gull com- gradually dispersing towards one another. This process plex” represents a good example of difficulties in is most evident in Western Europe. In particular, the applying this concept to demarcation of species. This southward dispersal of L. argentatus started in the late complex consists of about 20 taxa, whose range 1960s, and the northward dispersal of L. cachinnans, in embraces almost the entire Holarctics. There is no gen- 1976. At present, both species form mixed nesting col- erally accepted view on their nomenclature status. onies. Mixed argentatus × cachinnans pairs sometimes These taxa may be grouped by degree of similarity in occur, but all attempts to nest are unsuccessful (Yesou, various combinations, and the number of “good” poly- 1991; Yesou et al., 1994). typic species varies from 3 to 15 in different schemes. This is related to the fact that many taxa, well-differen- A similar tendency toward counter-dispersal of tiated morphologically and, hence, deserving the status these species takes place in Eastern Europe. Rapid of “taxonomic species,” are not closed genetic systems, expansion of L. argentatus southwards from Fennos- because they are connected to other taxa by more or candia and in the Baltic was documented in detail in the less intensive gene flows (Panov, 1989). first quarter of the 20th century (see Mierauskas et al., The pairs of forms, which are completely isolated 1991, for a review). Earlier (Monzikov and Panov, reproductively in some areas (i.e., representing “good 1996a, 1996b), we provided evidence for the hypothe- biological species”) but freely hybridize in others, rep- sis of current dispersal of L. cachinnans upstream along resent the main problem for the concept of biological the Volga basin. In general, the situation in Eastern species. These taxa illustrate the situation of secondary Europe differs from that described for western France. “species fusion” (Mayr, 1969). The gulls Larus argen- There is no direct secondary contact between geneti- tatus and L. hyperboreus provide a good example of cally pure populations of L. argentatus and L. cachin- such a type of relationships within the complex of her- ring gulls. These clearly differentiated species are sym- nans. However, our data allow us to suppose that allo- patric and reproductively isolated over vast areas of the patric autochthonous populations of these species are Subarctic. They hybridize intensively only in two dis- connected by gene flows through a chain of intermedi- tant regions, Iceland and northeastern Alaska (Ingolfs- ate hybrid populations. The purpose of this work is to son, 1970, 1987; Spear, 1987). test this hypothesis. 129 130 PANOV, MONZIKOV MATERIALS AND METHODS ties of attribution of all signals from the groups 2–5 to the vocalization type of L. argentatus or L. cachinnans. To test this hypothesis, we undertook a comparative In addition, we undertook discriminant analysis for six analysis of morphobiological peculiarities of gulls in and seven groups. In the last case, it was the sample the following transect: Ainovy Islands, Barents Sea from population 5, Nizhegorodskaya oblast, which was (population 1); Kandalaksha Bay of the White Sea, a priori divided into two subgroups, including signals Murmansk oblast (population 2); Remisaar Island, the typical for L. argentatus and L. cachinnans, respec- Gulf of Finland of the Baltic Sea, Leningradskaya tively. Group numbers (1–6 and 1–7) were used as an oblast (population 3); Rybinsk Reservoir, Yaroslavl independent variable. The resulting Machalanobis dis- oblast (population 4); Sitniki Village, Nizhegorodskaya tance matrix between groups was used for classification oblast (population 5). The transect length was ca. of groups with use of different methods of cluster anal- 2000 km. ysis: full relations, unweighted method of mean rela- For comparison, we used materials on the geneti- tion, and the Ward method. In addition, we made clus- cally pure populations of L. cachinnans from the Cas- terization of all 170 cases, i.e., particular phonograms, pian Sea (population 6) and Black Sea. Phenotypic fea- without their a priori classification, i.e., without pre- tures of 78 live mature birds and 87 chicks were ana- liminary attribution to one of the six or seven groups. In lyzed. Blood samples were taken for DNA analysis by this analysis, We used the above-mentioned methods modified PCR method. Adult gulls were caught from with different metrics (Euclidean and Pearson coeffi- their nests by narcotization of birds using baits with cient). α-chloralose, 33 mg per a bird weighing 800–1500 g. The analysis of DNA polymorphism was conducted We visually examined phenotypic composition of all using RAPD (modified method of polymerase chain the colonies visited and data obtained on nesting biol- reaction with random primer). This method allows us to ogy of all populations, as well as phonograms and vid- compare taxon-specific sets of “bands” (patterns) eos characterizing the specificity of signal behavior of obtained as products of DNA amplification with a ran- the gulls of the Ainovy Islands, Kandalaksha Bay, and dom primer. For identification of taxa, the RAPD Rybinsk Reservoir. The sounds were recorded using method was modified by us for future labeling of Realistic and Sony TCM-121 portable tape recorders, amplification products and their separation in polyacry- and videos were made using a CCD-TR570E camera. lamide gel with subsequent radiography. This provides We used A-PC Avisoft–Sonagraph software for the for higher resolution of this method applied to amplifi- analysis of phonograms. In addition, we analyzed gull cation products of similar lengths, owing to the better collections in the Zoological Museum of Moscow State separation of fragments. The zone of differences University, totalling 276 specimens. When analyzing between “pure” L. argentatus and L. cachinnans is in morphometric features, We used different methods of the area of 280–300 and 550–600 nucleotides, respec- cluster analysis: agglomerative methods (singular and tively. Our collection for genetic analysis included full relations, unweighted mean relation, and the Ward blood samples from 19 taxa (species and subspecies) method, all with Euclidean distance) and iterative from the family Laridae (257 specimens). We analyzed methods (the k-mean method). Calculations were based blood samples from 17 individuals from 3 autochtho- on standardized data. Due to a lack of data on males nous populations of L. argentatus, 19 individuals from from the population from the Rybinsk Reservoir, clus- the autochthonous population of L. cachinnans from tering was done by female samples from all the popula- the Sea of Azov, and 52 individuals from the Baltic tions studied. region and the Volga basin. The analysis of geographic variation in the “long The blood obtained from the wing vein was mixed call” acoustic signal was done on the basis of 170 pho- with conservation buffer containing 50 mM EDTA, 1% nograms using 7 independent variables: durations of NaF, and thymol and was stored without freezing at the last “long syllable” in the initial part of the signal; temperatures not lower than 4°ë. We studied the total second and fifth short syllables; pauses between “long” DNA extracted by phenol-chloroform method without and the first short syllables, between the first and sec- preliminary sedimentation of nuclei. Each polymerase ond and the fourth and fifth short syllables (all in ms); chain reaction (PCR) was performed using one ran- as well as the value of interharmonic interval, in kHz. domly chosen primer. We used two 10-nucleotide prim- The total sample was divided into 6 groups by the num- ers, designated below as primer 29 (5'–CCGGCCT- ber of geographic localities, or local populations, where TAC-3') and 45 (5'-GCCGTCCGAG-3'). The PCR pro- the phonograms were obtained. Sample size ranged cedure was made up of two steps. The first, without from 16 to 52 phonograms.
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