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Hymenoptera, Apidae): Incongruence Between Morphology and Mitochondrial DNA Henrique Batalha-Filho, Ana M

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Hymenoptera, Apidae): Incongruence Between Morphology and Mitochondrial DNA Henrique Batalha-Filho, Ana M Phylogeography and historical demography of the neotropical stingless bee Melipona quadrifasciata (Hymenoptera, Apidae): incongruence between morphology and mitochondrial DNA Henrique Batalha-Filho, Ana M. Waldschmidt, Lucio A.O. Campos, Mara G. Tavares, Tânia M. Fernandes-Salomão To cite this version: Henrique Batalha-Filho, Ana M. Waldschmidt, Lucio A.O. Campos, Mara G. Tavares, Tânia M. Fernandes-Salomão. Phylogeography and historical demography of the neotropical stingless bee Melipona quadrifasciata (Hymenoptera, Apidae): incongruence between morphology and mitochon- drial DNA. Apidologie, Springer Verlag, 2010, 41 (5), 10.1051/apido/2010001. hal-00892084 HAL Id: hal-00892084 https://hal.archives-ouvertes.fr/hal-00892084 Submitted on 1 Jan 2010 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie 41 (2010) 534–547 Available online at: c INRA/DIB-AGIB/EDP Sciences, 2010 www.apidologie.org DOI: 10.1051/apido/2010001 Original article Phylogeography and historical demography of the neotropical stingless bee Melipona quadrifasciata (Hymenoptera, Apidae): incongruence between morphology and mitochondrial DNA* Henrique Batalha-Filho1,AnaM.Waldschmidt2, Lucio A.O. Campos3, Mara G. Tavares 3,TâniaM.Fernandes-Salomao˜ 3 1 Universidade de São Paulo, Departamento de Genética e Biologia Evolutiva, 05508090, São Paulo, São Paulo, Brazil 2 Universidade Estadual de Sudoeste da Bahia, Departamento de Ciências Biológicas, 45200000, Jequié, Bahia, Brazil 3 Universidade Federal de Viçosa, Departamento de Biologia Geral, 36570000, Viçosa, Minas Gerais, Brazil Received 19 August 2009 – Revised 28 October 2009 – Accepted 23 November 2009 Abstract – The stingless bees are among the most abundant and ecologically important social inverte- brates in tropical communities. The Neotropical stingless bee Melipona quadrifasciata has two subspecies: M. quadrifasciata quadrifasciata and M. quadrifasciata anthidioides. The main difference between sub- species are the yellow metassomal stripes, which are continuous in M. q. quadrifasciata and discontinuous in M. q. anthidioides. Recently, two populations were described with continuous stripes and inhabiting clearly disjunct areas in relation to M. q. quadrifasciata. We sequenced 852 bp of the mtDNA COI gene from 145 colonies from 56 localities, and for the first time performed a detailed phylogeographic study of a neotropical stingless bee. Phylogenetic analyses revealed the existence of two clades exhibiting a south to north distribution: southern populations comprise the subspecies M. q. quadrifasciata, and northern pop- ulations are composed of M. q. anthidioides and two disjunct populations with continuous stripes. The divergence time of these two phylogroups was estimated between 0.233 and 0.840 million years ago in the Pleistocene, a period of climatic changes and geomorphological alterations in the Neotropical region. No evidence of genetic structure in relation to the tergal stripes was found, indicating that the morpho- logical trait regarding the pattern of stripes on tergites is not an accurate diagnostic for the subspecies of M. quadrifasciata. biogeography / coalescence / tergal stripes / Melipona quadrifasciata / subspecies 1. INTRODUCTION 1950). Traditionally, two subspecies have been recognized, M. quadrifasciata anthidioides The stingless bee Melipona quadrifasci- and M. quadrifasciata quadrifasciata, based ata, popularly known as “mandaçaia”, is dis- upon yellow stripes on the second to fifth ter- tributed along the eastern part of Brazil from gites, which are continuous in M. q. quadri- Rio Grande do Sul to Paraíba (Moure and Kerr, fasciata and interrupted in M. q. anthidioides (Ducke, 1916;Schwarz,1932). Corresponding author: H. Batalha-Filho, M. q. quadrifasciata is found in southern [email protected] São Paulo, Paraná, Santa Catarina, and Rio * Manuscript editor: Marina Meixner Grande do Sul (Kerr, 1951; Moure, 1975), Online material is available at: whereas M. q. anthidioides ranges from north- http://www.apidologie.org ern and northeastern São Paulo, along eastern Article published by EDP Sciences Phylogeography of Melipona quadrifasciata 535 Brazil, to Paraíba (Kerr, 1951). Kerr (1951) stripes, were analyzed by Waldschmidt et al. and Moure (1975) show a hybridization zone (2000, 2002) and they were genetically sim- between the two subspecies in the state of São ilar to M. q. anthidioides. However, in those Paulo and southern Minas Gerais, where in- studies the relationship between the pattern of termediary patterns of yellow tergal stripes are tergal stripes and genetic similarity was not ad- detected. Recently, Batalha-Filho et al. (2009) dressed and the sampling was limited. described the range distribution of the two Here we analyze a large number of sam- populations with continuous stripes and in- pling sites which cover, for the first time, most habiting clearly disjunct areas in relation to of the species range, including localities sam- the main distribution of the subspecies M. q. pled for the first time. Furthermore, the popu- quadrifasciata: one in northern Minas Gerais lations with continuous tergal stripes recently and another in northeastern Bahia and Sergipe. described by Batalha-Filho et al. (2009)were According to Batalha-Filho et al. (2009), also included. the geographic distribution of M. quadrifas- Some molecular population genetics ciata is associated with regions higher than studies have been conducted with bees 500 meters above sea level, except for its (Tanaka et al., 2001; Soucy and Danforth, southern range limit where lower elevation is 2002; Dick et al., 2004;Cruzetal.,2006; counterbalanced by higher latitude. Such re- Quezada-Euán et al., 2007; Kraus et al., 2008). lationship can be exemplified by the distri- However, none of the studies have applied bution of this species in the state of Espírito coalescent and more recent phylogeographic Santo, where M. quadrifasciata is found only methods. in the upper mountain portion of the state, be- The goal of the present study was to elu- ing unreported on northern sites, such as the cidate the phylogeographic pattern and de- Atlantic rainforest in Bahia. The populations mographic history of M. quadrifasciata.We of M. quadrifasciata bearing continuous tergal address two main questions: (i) is there corre- stripes on northeastern Bahia and Sergipe are lation between the distribution of tergal stripes associated with the São Francisco river mouth pattern and the maternal mitochondrial lin- in low elevation regions. eage? In other words, do populations with Some molecular studies have been carried continuous tergal stripes form a monophyletic out in M. quadrifasciata. Waldschmidt et al. group? (ii) What demographic event(s) in (2000) analyzed the subspecies of M. quadri- Neotropical region explain the observed phy- fasciata and detected a RAPD-PCR marker logeographic pattern? The present results will exclusive to M. q. quadrifasciata and ab- contribute to our knowledge about the biogeo- sent in M. q. anthidioides. Waldschmidt et al. graphic and evolutionary patterns of this taxon (2002), also using RAPD markers in popu- and the Neotropical region. lations of M. quadrifasciata, observed two genetically distinct groups, one being com- posed of M. q. quadrifasciata and other by 2. MATERIAL AND METHODS M. q. anthidioides.Different mtDNA restric- tion patterns were detected between both sub- 2.1. Sampling and DNA extraction species by Moreto and Arias (2005). Souza Samples (N = 145 colonies, one worker per et al. (2008) analyzed 155 colonies of both colony) were collected between 2002 and 2008 subspecies of M. quadrifasciata using RFLP in 56 localities in the Brazilian states of Bahia in the cytochrome b gene and found an as- (BA), Espírito Santo (ES), Minas Gerais (MG), sociation between the RFLP pattern and the Rio de Janeiro (RJ), São Paulo (SP), Paraná (PR), ff di erence in tergal stripes of each subspecies. Rio Grande do Sul (RS), Santa Catarina (SC), and Populations exhibiting continuous abdominal Sergipe (SE) (Tab. S1 available in online material stripes from northern Minas Gerais, Sergipe, and Fig. 1). The samples were stored in absolute and northeastern Bahia, however, were not in- ethanol at –80 ◦C until DNA extraction. cluded in that study. Two colonies from north- Samples were divided into four groups based ern Minas Gerais, exhibiting continuous tergal on the pattern of tergal stripes: (i) subspecies M. 536 H. Batalha-Filho et al. Figure 1. Map of the geographic distribution of the 56 sampling sites of M. quadrifasciata. The white squares with black points indicate individuals of M. q. quadrifasciata, the black hexagons indicate individ- uals of M. q. anthidioides, the white squares indicate the individuals with continuous tergal stripes from northern Minas Gerais, and the white triangles indicate the specimens with continuous tergal stripes from Sergipe and northeastern Bahia. The grey area represents the geographical range of M. quadrifasciata as determined by Batalha-Filho et al. (2009). The dashed line represents
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