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The Genus Myotis (Chiroptera, Vespertilionidae)

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The Genus Myotis (Chiroptera, Vespertilionidae) Original Article ISSN 1517-6770 the genus Myotis (Chiroptera, Vespertilionidae) in Brazil: phylogeny, distribution, and cytogenetics Michel Barros Faria1,2* & Maria Clara Santos Ribeiro2 1Universidade do Estado de Minas Gerais Unidade Carangola, Carangola, Minas Gerais, Brazil. Professor do Departamento do curso de Ciências Biológicas. E-mails: *[email protected], [email protected]. 2Museu de Zoologia Newton Baião de Azevedo Abstract. Myotis is the largest genus of the Vespertilionidae, showing a cosmopolitan geographical distribution and is considered an example of adaptive radiation. Nine species occurs in Brazil and this study synthesized aspects of the geographic distribution, karyotype, and phylogeny. A search in bibliographic databases was carried out using keywords. The phylogeny study was based on the sequencing of a specimen of Myotis ruber collected in a fragment of the Altantic Forest of Minas Gerais; this specimen was deposited at the Newton Baião de Azevedo Museum of Zoology. The genus showed to be widely distributed in the Brazilian territory, with Myotis nigricans being the most widespread. In addition, high karyotypic conservatism was observed in all species of the genus. The phylogenetic analyses using themt-Cytb gene corroborated the monophyletic aspect of the genus and the Myotis ruber species. Keywords: Geographic potential, karyotype, phylogenetic systematics, Vespertilionidae. Resumo. O gênero Myotis (Chiroptera, Vespertilionidae) no Brasil: filogenia, distribuição e citogenética. Myotis é o maior gênero de Vespertilionidae, apresentando distribuição cosmopolita e sendo um excelente exemplo de radiação adaptativa. Nove espécies ocorrem no Brasil e este estudo sintetizou aspectos da distri- buição geográfica, cariótipo e filogenia. Foi realizada uma pesquisa em bancos de dados bibliográficos, utili- zando palavras-chave. O estudo de filogenia baseou-se no sequenciamento de um espécime de Myotis ruber, coletado em um fragmento de Mata Atlântica do Estado de Minas Gerais; e depositado no Museu de Zoologia Newton Baião de Azevedo. O gênero mostrou ser amplamente distribuído no território brasileiro, sendo Myo- tis nigricans a espécie mais representativa. Além disso, observou-se alto conservadorismo cariotípico em todas as espécies do gênero. As análises filogenéticas utilizando o gene mitocondrial citocromo-b corroboraram o aspecto monofilético do gênero e da espécie Myotis ruber. Palavras-Chave: Potencial geográfico, cariótipo, sistemática filogenética, Vespertilionidae. Introduction man, 1993; Ruedi & Mayer, 2001; Simmons, 2005; Tavares et al., 2008). Its species exhibit Myotis Kaup, 1829 is the most rep- great similarities in forms and seldom display resentative genus among the Vespertilionidae specialized features (LaVal, 1973; Ruedi et al., and has a wide distribution (LaVal, 1973; Koop- Revista Brasileira de Zoociências 19(3): 161-175. 2018 162. Faria & Ribeiro 1990; Gannon et al., 2001; López-González et Geoffroy, 1806);Myotis simus (Thomas, 1901). al., 2001; Ruedi & Mayer, 2001; Stadelmann et Regarding the genus taxonomic com- al., 2004), hindering the process of identification plex of species that occur in Brazil, Myotis dinel- and the systematic organization of the group. lii was described as a subspecies of Myotis levis Tate (1941) divided the genus into by LaVal (1973) based on the allopatric distribu- seven subgenera by grouping species within each tion of organisms and their morphological sim- subgenus according to their morphological simi- ilarities. Subsequently, because sympatric traits larity: Selysius, Isotus, Paramyotis, Myotis, Chrys- were recorded in the spatial distribution of M. opteron, Leuconoe, and Rickettia. Findley (1972) levis levis and M. l. dinellii (see Passos et al., analyzed 48 external and cranial characters 2010) in Southern Brazil, they could no longer be grouping the species only in the three subgenera described as species and subspecies. Miranda et Selysius, Myotis, and Leuconoe, also according to al (2013) performed morphological and morpho- the specimens’ morphological affinities related metric studies on these organisms and detected to different flight and feeding modes. A fourth differences in the sexual dimorphism of both spe- subgenus, Cistugo, was described by Koopman cies, with M. levis showing separation between (1993), and as containing species restricted to males and females, and differences in color and South Africa. Cistugo is now recognized as a dis- size. Myotis levis showed more similarity with M. tinct genus from Myotis (Lack et al., 2010). The ruber while M. dinellii presented similarity to M. other subgenera are currently considered an albescens and M. nigricans. ecomorphological group, that is, all Myotis of Myotis lavali and M. izecksohni were the New World are grouped into one single sub- described from the M. nigricans complex based genus yet without a formally known name (Wil- on morphological and morphometric traits for son, 2008). Despite being a broad and diverse species differentiation among themselves, and genus, Myotis is karyotypically one of the most for the differentiation of M. nigricans species, conserved (Baker & Jordan, 1970); in general, during a study about qualitative evaluations of phylogenetic studies classify the genus as being this species (Moratelli et al., 2011b). monophyletic (Stadelmann et al., 2007). Although there are a volume There are only nine species recorded in considerable work describing the ecology of in- Brazil (Nogueira et al., 2014): Myotis albescens dividuals of the genus, systematic and phyloge- (É. Geoffroy, 1806); Myotis dinelli Thomas, 1902; netic aspects remain poorly understood. There- Myotis izecksohni Moratelli et al., 2011a; Myotis fore, through bibliographic review and molecular levis (É. Geoffroy, 1824); Myotis lavali Moratel- study of Myotis ruber, this work brought togeth- li et al., 2011a; Myotis nigricans (Schinz, 1821); er, briefly, data on the geographic distribution of Myotis riparius Handley, 1960; Myotis ruber (É. Revista Brasileira de Zoociências 19(3): 161-175. 2018 The genus Myotis in Brazil .163 the genus Myotis in Brazil and to find out the cy- A specimen of Myotis ruber was collected togenetic and phylogenetic status, pointing out during a bat survey in an Atlantic Forest remnant the main problems involved in these studies. of Minas Gerais, located in Reserva Particular do Patrimônio Natural Santuário Ecológico Mata Materials and Methods dos Jacus (RPPN SEMJ) (42°02’51” W; 20°29’01” The phylogenetic analyses were based S; DATUM SIRGAS 2000), in municipality the Alto on cytochrome-b (cyt-b) sequences of My- Jequitibá. The ranges of temperature vary from otis obtained from GenBank and proper 1,150 to 1,470 mm, the climate type is Cwb, wet sequencing (Table 1). The mitochondrial cyto- tropical, with dry winter and temperate summer, chrome b (cyt-b) gene was chosen for the study according to the classification of Köppen (ALVA- because it is widely used in systematic studies of RES et al., 2013). The specimen was prepared and mammals, alone or in combination and because deposited at the Newton Baião de Azevedo Mu- it has a database of good taxonomic coverage de- seum of Zoology (voucher MZNB 378; see Faria posited in GenBank. et al. 2017). Hepatic tissue DNA was extracted Table 1. List of species analyzed with name, GenBank or feld number (number), locality and reference. Taxa ID GenBank Reference Myotis ruber - This study Myotis ruber AF376867 Ruedi & Mayer, 2001 Myotis simus AM262336 Stadelmann et al., 2007 Myotis simus JX130506 Larsen et al., 2012 Myotis riparius JX130571 Larsen et al., 2012 Myotis riparius JX130570 Larsen et al., 2012 Myotis riparius JX130569 Larsen et al., 2012 Myotis riparius JX130568 Larsen et al., 2012 Myotis nigricans AF376864 Ruedi & Mayer, 2001 Myotis nigricans JX130535 Larsen et al., 2012 Myotis nigricans JX130530 Larsen et al., 2012 Myotis nigricans JX130529 Larsen et al., 2012 Myotis albescens JX130504 Larsen et al., 2012 Myotis albescens JX130503 Larsen et al., 2012 Myotis albescens JX130522 Larsen et al., 2012 Myotis levis JX130475 Larsen et al., 2012 Myotis levis AF376853 Ruedi & Mayer, 2001 Myotis gracilis AB243030 Kawai et al., 2006 Revista Brasileira de Zoociências 19(3): 161-175. 2018 164. Faria & Ribeiro using the phenol/chloroform protocol accord- The ML topology was obtained with the PhyML ing to Sambrook et al. (1989). The DNA quality 3.0 software (Guindon & Gascuel, 2003) using was verified by 0.8% agarose gel electrophoresis the following parameters: optimized sequence and ultraviolet (UV) transilluminator visualization balance, proportion of estimated variable sites, and quantified in a Nanodrop spectrophotome- estimated α, initial BioNj tree, topology of sizes ter (ND-1000™). The gene was amplified through of optimized branches, and the aLRT-SH support polymerase chain reactions (PCR; Axygen model values obtained on the basis of 1,000 replicates Maxygene II) standardized with specific primers. (Anisimova & Gascuel, 2006; Guindon et al., 2010). The incomplete mitochondrial cyto- chrome b gene (733bp; cyt-b) was amplified with Bibliographic searches were conduct- the primers L14724 (Irwin et al., 1991) and CIT- ed in databases such as Web of Science (http:// REV (Casado et al., 2010). Amplicons were pu- www.webofknowledge.com/) and SciElo (http:// rifed using the GFX PCR DNA and Gel Band Pu- www.scielo.br/) to obtain data on taxonomy, rifcation Kit (GE Healthcare) and labelled with geographic distribution, and cytogenetics. The
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