Cheeked Ground Squirrels (Spermophilus 9 10 10 11 Erythrogenys Sensu Lato) Suggest Taxonomic Delineation 11 12 12 13 13 14 Vera A
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Integrative Zoology 2019; 14: 341–353 doi: 10.1111/1749-4877.12383 1 ORIGINAL ARTICLE 1 2 2 3 3 4 4 5 5 6 6 7 Phylogenetic relationship and variation of alarm call traits of 7 8 8 9 populations of red-cheeked ground squirrels (Spermophilus 9 10 10 11 erythrogenys sensu lato) suggest taxonomic delineation 11 12 12 13 13 14 Vera A. MATROSOVA,1 Anastasia D. IVANOVA,1,2 Elena V. VOLODINA,3 Ilya A. VOLODIN,2,3 14 15 4 2 5 15 16 Dmitry Yu. ALEXANDROV, Olga V. SIBIRYAKOVA and Oleg A. ERMAKOV 16 17 1Engelhardt Institute of Molecular Biology, RAS, Moscow, Russia, 2Lomonosov Moscow State University, Moscow, Russia, 17 18 3Moscow Zoo, Moscow, Russia, 4Severtsov Institute of Ecology and Evolution, RAS, Moscow, Russia and 5Department of Zoology 18 19 19 and Ecology, Penza State University, Penza, Russia 20 20 21 21 22 22 23 Abstract 23 24 24 Distribution area and taxonomic borders within the species complex Spermophilus erythrogenys sensu lato re- 25 25 main questionable. Early evidence suggests that red-cheeked ground squirrels of Southeast Kazakhstan are re- 26 26 markably different in terms of the acoustic structure of their alarm calls from the red-cheeked ground squirrels 27 27 of the Kurgan region in Russia. In this study, we analyzed the differences in the acoustic structure of the alarm 28 28 call and mitochondrial DNA (complete control region, 1005–1006 bp and complete cytochrome b gene, 1140 29 29 bp) in 3 populations of red-cheeked ground squirrels (Tara, Altyn-Emel and Balkhash), all located within ar- 30 30 eas isolated by geographical barriers in Southeast Kazakhstan. We found that the alarm call variables were sim- 31 31 ilar between the 3 study populations and differed by the maximum fundamental frequency (8.46 ± 0.75 kHz) 32 32 from the values (5.62 ± 0.06 kHz) reported for the red-cheeked ground squirrels from the Kurgan region of Rus- 33 33 sia. Variation in mtDNA control region was only 3% and variation in cytochrome b gene was only 2.5%. Phylo- 34 34 genetic trees based on cytochrome b gene polymorphism of 44 individuals from the study area and adjacent ter- 35 35 ritories indicated 3 clades with high (98–100%) bootstrap support: “intermedius,” “brevicauda” and “iliensis”). 36 36 We conclude that the 3 study populations in Southeast Kazakhstan belong to the clade intermedius and suggest 37 37 a taxonomical revision of the species complex Spermophilus erythrogenys sensu lato, including analyses of nu- 38 38 clear DNA and alarm calls for populations of the brevicauda and iliensis clades. 39 39 40 Key words: alarm call, control region, cytochrome b, mitochondrial DNA, vocal communication 40 41 41 42 42 43 43 44 44 45 INTRODUCTION 45 46 46 Correspondence: Vera A. Matrosova, Russian Academy of 47 Red-cheeked ground squirrels of Southeast Kazakh- 47 48 Sciences, Division Department of Structural and Functional stan, commonly considered within taxon Spermophi- 48 49 Genomics, Engelhardt Institute of Molecular Biology, Vavilova lus erythrogenys sensu lato, represent an excellent mod- 49 50 str., 32, Moscow 119991, Russia. el for studying biogeographic speciation (Nikol’skii & 50 51 Email: [email protected] Rumyantsev 2004). Southeast Kazakhstan is a geo-mor- 51 © 2019 International Society of Zoological Sciences, Institute of Zoology/ 341 Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd V. A. Matrosova et al. 1 phologically heterogeneous region with deep rivers, tions of ground squirrels from this area include both 1 2 mountains and lowlands providing numerous eco-geo- bioacoustical analyses (Nikol’skii & Rumyantsev 2004) 2 3 graphical barriers for ground squirrels, including the ar- and genetic analyses (Ermakov et al. 2015). 3 4 eas that are unfit for habitation although seem surmount- Considering the acoustic structure of the alarm call 4 5 able (Fig. 1). Studying populations of red-cheeked (primarily based on frequency modulation pattern of the 5 6 ground squirrels from this region might cast new light alarm call notes), Nikol’skii and Rumyantsev (2004) 6 7 on their geographical divergence (Harrison et al. 2003; subdivided the alarm calls recorded in 13 populations of 7 8 Herron et al. 2004; Thorington & Hoffmann 2005; Hel- ground squirrels (distributed over the large area shown 8 9 gen et al. 2009) and raise new questions about the by the dotted line in Fig. 1) into 4 clusters, potentially 9 10 mechanisms by which populations diverged (Zachos corresponding to the 4 species (S. erythrogenys, Sper- 10 11 2018). mophilus brevicauda, Spermophilus carruthersi and 11 12 Geographical boundaries between ranges of differ- Spermophilus major) with non-overlapping distribution 12 13 ent species and forms of ground squirrels from South- areas; the boundaries between the clusters corresponded 13 14 east Kazakhstan are presently unknown. Approaches to large zoogeographic barriers (Fig. 1). Among them, 14 15 for identifying taxonomical ranks of different popula- most distinctive were 4 individual red-cheeked ground 15 16 squirrels from the Altyn-Emel area: their alarm calls 16 17 were unusually high-frequency, with the maximum fun- 17 18 damental frequency of over 8 kHz compared to values 18 19 below 7 kHz in ground squirrels in other studied popu- 19 20 lations. The authors hypothesized that animals from the 20 21 Altyn-Emel area belong to the form “carruthersi” with- 21 22 in S. erythrogenys sensu lato; however, unequal sam- 22 23 ples of animals from different populations (from 1 to 9) 23 24 and small numbers of alarm calls available for analyses 24 25 (1 per individual) along with their unknown genetic sta- 25 26 tus prevented more decisive conclusions about their tax- 26 27 onomical position (Nikol’skii & Rumyantsev 2004). To 27 28 date, the alarm call acoustics of ground squirrels from 28 29 the Altyn-Emel area have not been studied in detail. 29 30 30 A recent barcoding study (Ermakov et al. 2015), 31 31 based on polymorphism of cytochrome c oxidase sub- 32 32 unit 1 (COI) of all Eurasian species of ground squir- 33 33 rels, showed a paraphyly of S. erythrogenys, S. brevi- 34 34 cauda and Spermophilus pallidicauda. Moreover, on the 35 35 basis of mtDNA polymorphism, 5 individuals of sup- 36 36 posed S. erythrogenys turned out to be 3 genetically dis- 37 37 tant forms, for which a putative species level rank was 38 38 proposed: (i) S. erythrogenys (right bank of the Irtysh 39 39 River); (ii) another, previously unknown, form from the 40 40 right bank of the Ob’ River (Kuznetsk Depression); and 41 41 (iii) S. carruthersi (Zaysan Depression, the Dzungar- 42 42 ian Alatau). Thus, although it has been suggested that 43 43 ground squirrels inhabiting the area of the Dzungarian 44 44 Figure 1 Map showing the study area (a) and data collection Alatau including the Altyn-Emel area should be consid- 45 45 localities (b). Sites of matched alarm call and DNA sampling ered as S. carruthersi, the available genetic and acoustic 46 46 are marked in white; sites of DNA only sampling are marked in data are not sufficient to support this suggestion. 47 black (see Table 1 for details). Stars designate type localities: 47 Formerly, taxon S. erythrogenys sensu lato was inter- 48 “bre” – S. brevicauda Brandt, 1843; “int” – S. intermedius 48 preted as a single wide-range polymorphic species com- 49 Brandt, 1843; “car” – S. carruthersi (Thomas, 1912); “ili” – S. 49 plex involving all ground squirrels from Kazakhstan 50 e. iliensis (Belyaev, 1945). The dotted line delineates the study 50 51 area by Nikol`skii & Rumyantsev (2004). to Central Mongolia from west to east and all ground 51 342 © 2019 International Society of Zoological Sciences, Institute of Zoology/ Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd Ground squirrels of Southeast Kazakhstan 1 squirrels from Southwest Siberia to Tien Shan from into the phylogeography of the ground squirrels inhabit- 1 2 north to south (Belyaev 1955; Gromov et al. 1965; Vasi- ing this area. 2 3 lyeva 1968; Kryštufek & Vohralík 2013). From anoth- 3 4 er point of view, S. erythrogenys sensu lato includes a MATERIALS AND METHODS 4 5 few morphologically different forms considered as sepa- 5 6 rate species (Afanas’ev et al. 1953; Ognev 1963; Sluds- Study sites, animals and dates 6 7 kiy et al. 1969). Recently, these forms with unclear tax- 7 8 onomic status were separated into 3 species based on Alarm call and DNA samples of red-cheeked ground 8 9 cytochrome b gene (cyt b) polymorphism: S. erythroge- squirrels were collected in Southeast Kazakhstan from 9 10 nys, inhabiting the northern part of the area; S. brevicau- 10 to 24 June 2015 in the 3 natural colonies which are 10 11 da, inhabiting the southern part of the area and S. pallid- representative of the 3 study populations, “Tara,” “Al- 11 12 icauda, inhabiting the eastern part of the area (Harrison tyn-Emel” and “Balkhash” (Table 1). All the 3 habi- 12 13 et al. 2003; Herron et al. 2004; Thorington & Hoffmann tats represented a dry grazing steppe. We examined 38 13 14 2005; Helgen et al. 2009). living subjects: 30 live-trapped and 8 free-ranging; 10 14 were from the Tara, 10 from the Altyn-Emel and 18 15 In rodents, vocalizations are not learned but inherit- 15 from the Balkhash population. Of the 38 living subjects, 16 ed genetically (Kikusui et al. 2011). Ground squirrels 16 22 provided matched samples of the alarm calls and 17 have species-specific alarm calls (Nikol’skii 1979, 1984; 17 DNA, whereas 16 individuals from the Balkhash pop- 18 Schneiderová & Policht 2011; Matrosova et al.