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ArticleTitle Combining phylogeography and future climate change for conservation of Bombus morio and B. pauloensis (: ) Article Sub-Title Article CopyRight Springer Nature Switzerland AG (This will be the copyright line in the final PDF) Journal Name Journal of Conservation Corresponding Author Family Name Françoso Particle Given Name Elaine Suffix Division Instituto de Biociências Organization Universidade de São Paulo Address Rua do Matão, 277 sala 320, São Paulo, SP, CEP 05508-090, Brazil Phone +551130917587 Fax Email [email protected] URL ORCID

Author Family Name Zuntini Particle Given Name Alexandre Rizzo Suffix Division Instituto de Biologia Organization Universidade Estadual de Campinas Address Rua Monteiro Lobato, 255, Campinas, SP, CEP 13083-970, Brazil Phone Fax Email URL ORCID Author Family Name Arias Particle Given Name Maria Cristina Suffix Division Instituto de Biociências Organization Universidade de São Paulo Address Rua do Matão, 277 sala 320, São Paulo, SP, CEP 05508-090, Brazil Phone Fax Email URL ORCID

Received 16 April 2017 Schedule Revised Accepted 26 November 2018

Abstract A worldwide decline of many bee species has been reported, but conversely some species seems to be in expansion. Nonetheless species truly in expansion may be overestimated, especially when they are considered as a whole, and information about intraspecific lineages is lacking. The objective of this study was to test whether the species Bombus morio and B. pauloensis will be safe under future climate changes. Specifically, test if these bees will suffer geographic decline or expansion; test whether each phylogeographic lineage within B. pauloensis will respond differently in modeling of future geographic distribution given climate change; find stable areas holding high genetic diversity based on predicted future climatic changes; and test whether these areas are covered by existing protected areas. To reach the objectives we performed analyses using phylogeographic data already available and climate change information to model the demography of the panmictic B. morio and the phylogeographic lineages in B. pauloensis. Our results suggest that both species will suffer a reduction in suitable area and that the reduction in distribution is masked for B. pauloensis. When each clade was separately analyzed, the ones in the edge of the species distribution are the most likely to decline. We found a large future refuge in eastern state of São Paulo and state of Rio de Janeiro for B. morio and for the clades of B. pauloensis. This refuge seems to show high levels of species richness and endemism for different taxa. Thus, by protecting this area we will be preserving not only the pattern of biodiversity but also the processes that generate and maintain them for many other species. Keywords (separated by '-') Phylogeographic lineages - Future distribution modeling - Conservation - Bumblebee - Brazil Footnote Information Electronic supplementary material The online version of this article (https://doi.org/10.1007/ s10841-018-0114-4) contains supplementary material, which is available to authorized users. Journal of Insect Conservation https://doi.org/10.1007/s10841-018-0114-4

1 ORIGINAL PAPER

2 Combining phylogeography and future climate change 3 for conservation of Bombus morio and B. pauloensis (Hymenoptera: 4 Apidae)

5 Elaine Françoso1 · Alexandre Rizzo Zuntini2 · Maria Cristina Arias1

6 Received: 16 April 2017 / Accepted: 26 November 2018 7 © Springer Nature Switzerland AG 2018

8 Abstract 9 A worldwide decline of many bee species has been reported, but conversely some species seems to be in expansion. None- 10 theless species truly in expansion may be overestimated, especially when they are considered as a whole, and information 11 about intraspecific lineages is lacking. The objective of this study was to test whether the bumblebee species Bombus morio 12 and B. pauloensis will be safe under future climate changes. Specifically, test if these bees will suffer geographic decline or 13 expansion; test whether each phylogeographic lineage within B. pauloensis will respond differently in modeling of future geo- 14 graphic distribution given climate change; find stable areas holding high genetic diversity based on predicted future climatic 15 changes; and test whether these areas are covered by existing protected areas. To reach the objectives we performed analyses 16 using phylogeographic data already available and climate change information to model the demography of the panmictic 17 B. morio and the phylogeographic lineages in B. pauloensis. Our results suggest that both species will suffer a reduction in 18 suitable area and that the reduction in distribution is masked for B. pauloensis. When each clade was separately analyzed, 19 the ones in the edge of the species distribution are the most likely to decline. We found a large future refuge in eastern state 20 of São Paulo and state of Rio de Janeiro for B. morio and for the clades of B. pauloensis. This refuge seems to show high 21 levels of species richness and endemism for different taxa. Thus, by protecting this area we will be preserving not only the 22 pattern of biodiversity but also the processes that generate and maintain them for many other species. AQ1

23 Keywords Phylogeographic lineages · Future distribution modeling · Conservation · Bumblebee · Brazil

24 Introduction et al. 2006; Olesen et al. 2007; Pauw 2007; Potts et al. 2016). 30 Unfortunately recent reports have indicated a worldwide 31 25 Currently there are more than 20,000 species of bees bee decline (Cane and Tepedino 2001; Biesmeijer et al. 32 26 accepted in the world (Ascher and Pickering 2014). The 2006; De la Rúa et al. 2009). Moreover, a regional Red List 33 27 ecological services they provide through pollination are assessment indicates that 9% of bees are threatened (Potts 34 28 unquestionable and have high ecologic and economical et al. 2016). Although this assessment is available only for 35 29 impacts (Kremen et al. 2008; Fontaine et al. 2006; Vamosi Europe, it should be considered as an alert in a global sce- 36 nario. The cause of the decline in general may be associated 37 to extrinsic factors as habitat loss and fragmentation, agri- 38 A1 Electronic supplementary material The online version of this culture intensification, excessive use of pesticides, patho- 39 A2 article (https​://doi.org/10.1007/s1084UNCORRECTED​1-018-0114-4) contains gens, industrialization, PROOF invasive alien species, and global 40 A3 supplementary material, which is available to authorized users. climatic changes. Also intrinsic genetic and ecological fac- 41 A4 * Elaine Françoso tors as haplodiploidy and complementary sex determination 42 A5 [email protected] (related to production of unviable or sterile diploid males), 43 social behavior and specialist feeding habit may be involved 44 A6 1 Instituto de Biociências, Universidade de São Paulo, Rua do 45 A7 Matão, 277 sala 320, São Paulo, SP CEP 05508‑090, Brazil (Zayed 2009, and references therein; Potts et al. 2016). Specifically, are important pollinators of 46 A8 2 Instituto de Biologia, Universidade Estadual de Campinas, 47 A9 Rua Monteiro Lobato, 255, Campinas, SP CEP 13083‑970, natural flora and crops (Corbet et al. 1991; Kevan 1991; A10 Brazil Memmott et al. 2004; Pywell et al. 2006; Velthuis and Doorn 48

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49 2006; Goulson et al. 2008; Goulson 2010). They present Future changes in climate are likely to affect species 102 50 important and sometimes advantageous features when com- range, distribution of the biological diversity, and taxa 103 51 pared to honeybees, e.g., a greater capacity for foraging in evolutionary history (Thuiller et al. 2011). The geographic 104 52 cold and rainy conditions, visiting crops with longer flowers distribution modeling based on future projections has been 105 53 due to their long tongue, and performing buzz pollination, used to predict how species will respond to climatic changes 106 54 important for plants with poricidal anthers, as Solanaceae (Hannah et al. 2002; Kramer et al. 2010; Loiselle et al. 2010; 107 55 (Goulson 2010, and references therein). Nevertheless, many Pearman et al. 2010; Maiorano et al. 2011; Saupe et al. 2011; 108 56 studies have documented a recent decline of bumblebees Taubmann et al. 2011; Watt et al. 2011; Giannini et al. 2012; 109 57 species, mainly in areas that suffered high habit modifica- D`Amen et al. 2013). Giannini et al. (2012), using two dif- 110 58 tion by anthropic actions related to agriculture intensifica- ferent scenarios for future projections, an optimistic and a 111 59 tion and urbanization (Williams 1982, 1986; Carvell 2002; pessimistic, to the years 2050 and 2080, concluded that 9 112 60 Goulson 2006; Batra 1995; Ellis et al. 2006; McFrederick of 10 species of Brazilian bees would have their suitable 113 61 and LeBuhn 2006; Pywell et al. 2006; Fitzpatrick et al. 2007; areas decreased. While a number of causal factors may be 114 62 Kosior et al. 2007; Colla and Packer 2008; Goulson et al. involved, the response of different species to habitat loss 115 63 2008; Grixti et al. 2009; Williams et al. 2009; Williams and is likely a key component of this phenomenon (Lozier and 116 64 Osborne 2009; Cameron et al. 2011; Morales et al. 2013). Cameron 2009). Lozier et al. (2011) observed expansion in 117 65 Shifts in pollinator diversity and ranges are well docu- some bumblebee species in North America, despite recent 118 66 mented in Europe and North America bumblebees (Pfeiffer habitat fragmentation. The authors discuss the role of mar- 119 67 and Foster 2015; Potts et al. 2016), but there is little infor- ginal habitats, such as patches of weedy flowers adjacent 120 68 mation for Latin America, Africa and Asia (Potts et al. to highways and agricultural fields, or gardens in heavily 121 69 2016). While European species appear mainly affected by urbanized areas, as potential food resources for bumblebees. 122 70 a change-over in agricultural practices impacting food and Furthermore, the high capacity for dispersal (Macfarlane 123 71 nest resources (Williams and Osborne 2009), in the United 1995; Buttermore 1997; Kraus et al. 2009; Lepais et al. 124 72 States, species decline has been associated with a high 2010) may maintain population structure via immigration 125 73 prevalence of the microsporidian pathogen Nosema bombi (Francisco et al. 2016; Françoso et al. 2016a, b). Although 126 74 (Cameron et al. 2011). In Chile and southern Argentina the the decline of bees is global and currently discussed, many 127 75 introduced species Bombus ruderatus and Bombus terrestris species of Bombus are not affected and remain constant or 128 76 have replaced Bombus dahlbomii, formerly the most abun- even in expansion (Goulson et al. 2008). Nevertheless, spe- 129 77 dant pollinator (Morales et al. 2013). Today, B. dahlbomii is cies truly in expansion may be overestimated. Normally the 130 78 absent in many areas, including those where the two intro- species are analyzed as a unit, lacking important informa- 131 79 duced species were first recorded (Morales et al. 2013). In tion about lineages. That is, one lineage may be expanding 132 80 Brazil, a recent report indicated that B. bellicosus has suf- but an overall loss of genetic diversity may be accounting 133 81 fered drastic decline and extinction in the northern portion of in other lineages. The infra-specific genetic data are crucial 134 82 its distribution range, probably due to habitat loss, pollution, for the preservation of the historical components of diversity 135 83 and climate change (Martins and Melo 2010; Martins et al. and to maintain the potential for species to mount adaptive 136 84 2015). responses to environmental changes (D’Amen et al. 2013). 137 85 In Brazil there are just eight species of bumblebees Françoso et al. (2016a, b), encompassing the two most 138 86 recognized: B. applanatus, B. bahiensis, B. bellicosus, B. widely distributed bumblebee species in Brazil, B. morio 139 87 brasiliensis, B. brevivillus, B. morio, B. pauloensis, and B. and B. pauloensis, provided valuable contributions on the 140 88 transversalis, being the first two species recently described demography, distribution, and genetic structure. Their 141 89 (Santos et al. 2015; Françoso et al. 2016a, b). They are results suggest no genetic structure for B. morio by mito- 142 90 important pollinators of several crops: blueberry (da Silveira chondrial and microsatellite data, except for very distinct 143 91 et al. 2011); Brazil nut (Maués 2002; Giannini et al. 2015); samples from Teodoro Sampaio city that likely reflect a new 144 92 eggplant (D`Avila and Marchini 2005; Montemor and Souza species or subspecies corroborating previous data obtained 145 93 2009; GianniniUNCORRECTED et al. 2015); gabiroba, guava, jurubeba, sweet by Francisco et al. (2016PROOF). On the other hand, B. pauloensis 146 94 passion fruit, squash, urucum (Giannini et al. 2015), tomato has three conspicuous lineages with deep phylogeographic 147 95 (Aldana et al. 2007; Giannini et al. 2015); yellow passion division according to mitochondrial data and morphology: 148 96 fruit (Yamamoto et al. 2012; Giannini et al. 2015); beans central (C), north (N), and south (S) clades. These lineages 149 97 (D’Avila and Marchini 2005); and sunflowers (D’Avila and differ in the climates they experience and have substantial 150 98 Marchini 2005; Giannini et al. 2015). Nonetheless, little is geographic separation (Françoso et al. 2016a, b; Fig. 1). As 151 99 known about their conservation status, and consequently the phylogeographic data provide an important set, and once 152 100 there is no policy for the protection and management of the genetic structure of B. morio and B. pauloensis is known, 153 AQ2101 these bees. our main goal is to test whether both species and the lineages 154

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Fig. 1 Phylogeographic patterns found in Bombus morio (a) and region of Cytochrome C Oxidase II and ATPase 8 genes, and ­tRNAlys Bombus pauloensis (b) by using molecular data concerning 1570 bp and ­tRNAasp). Grey areas in the map correspond to altitudes above of mitochondrial DNA (Cytochrome C Oxidase I, Cytochrome B, 750 m. Main main clade, TS Teodoro Sampaio clade, C central clade, the large ribosomal RNA subunit, and cluster 4 of tRNA, covering a N north clade, S south clade. Adapted from Françoso et al. (2016a, b)

155 of B. pauloensis will be safe under future climate changes, of relative contributions of the environmental variables to 179 156 considering the existing protected areas. Specifically the the Maxent model and the jackknife test of variable impor- 180 157 objectives were to test: (i) whether these bee species will tance. The environmental variables were analyzed separately 181 158 suffer geographic decline or expansion; (ii) whether each and excluded if verified: (1) low contribution and lower gain 182 159 phylogeographic lineage within B. pauloensis will respond when in isolation, and (2) increase or no change in the gain 183 160 differently in modeling of future geographic distribution when omitted. If the area under the curve (AUC) value was 184 161 given climate change; (iii) whether there are stable areas decreased, the environment variable was kept; conversely, 185 162 with high genetic diversity based on predicted future cli- if the AUC value increased, the environment variable was 186 163 matic changes; and (iv) whether these areas are covered by definitely excluded. Maxent generates models using only 187 164 existing protected areas. These objectives were addressed by presence records. We developed present-day models (5 km 188 165 performing geographic distribution modeling and projected resolution) and then projected them into the future condi- 189 166AQ3 future climate change. tions (2050 and 2070). Global climate model (GCM) data at 190 191 2.5 min spatial resolution from CMIP­ 5 (IPCC Fifth Assess- 192 ment) for four representative scenarios based on ­CO2 con- 167 Methods centration pathways (RCP2.6, RCP4.5, RCP6.0 and RCP8.5) 193 data was downscaled and calibrated (bias corrected) using 194 168 Modeling future geographic distribution WorldClim 1.4 as baseline “current” climate according to 195 WorldClim (http://www.world​clim.org/cmip5​_2.5m). Each 196 169 For input locality data, we used the same points described RCP differs greatly in the rate of radiative forcing and emis- 197 170 in Françoso et al.UNCORRECTED (2016a, b): 102 different georeferenced sions, being RCP2.6 PROOF the scenario with lower emissions; 198 171 occurrence records for B. morio and 71 for B. pauloensis. and RCP8.5 the scenario with higher emissions. Four GCM 199 172 Distribution models were based on the top contributing bio- models were used: BCC-CSM1-1, CCSM4, HadGEM2-AO, 200 173 climatic variables (Table 1) from the WorldClim data set and MIROC5. We modeled averages of ten replicates using 201 174 (Hijmans et al. 2005) using Maximum Entropy algorithm the “crossvalidate” option for each model and scenario. 202 175 in Maxent, v.3.3.3k (Phillips et al. 2006; Phillips and Dudik Model performance was evaluated using the AUC calculated 203 176 2008), a method that performed well in comparison to alter- by Maxent. AUCs > 0.75 are typically considered adequate 204 177 native approaches (Elith et al. 2006). The top contribution for species distribution modeling applications (Pearce and 205 178 bioclimatic variables were chosen according to the estimates Ferrier 2000). The average of the four GCM models with 206

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Table 1 Contribution of each climatic variable in the geographic dis- Fig. 2 Current and future distribution modeling for Bombus morio ◂ tribution of B. morio and B. pauloensis (main clade) and Bombus pauloensis (all clades together, and Cen- tral, North, and South clades separately, according to Françoso et al. Species Variable Con- 2016a, b), obtained using the average of four GCM models (BCC- tribu- CSM1-1, CCSM4, HadGEM2-AO, and MIROC5), each under four tion representative ­CO2 concentration pathways (RCP26, RCP45, RCP60 (%) and RCP85). Suitability range is represented by the grey scale on the projections, in which lighter and darker gray means minimum and B. morio Max. temperature of warmest month 29.1 maximum probabilities, respectively. Graphs represent the distri- Precipitation of warmest quarter 24.2 butional area reduction from modern day to 2050 and 2070 for each Temperature seasonality 24.2 model and scenario combination of predicted presence. The axes of Mean temperature of coldest quarter 12 ordinates show the occupied area in a normalized ratio Precipitation of wettest month 5.3 Isothermality 3.9 Maptools (Bivand and Lewin-Koh 2013), Raster (Hijmans 219 Precipitation of driest quarter 1.3 2014a, b), rgdal (Bivand et al. 2013), and rgeos (Bivand and 220 B. pauloensis Max. temperature of warmest month 32.4 Rundel 2014). 221 Temperature seasonality 25.3 Precipitation of warmest quarter 22.3 Conservation 222 Annual precipitation 9.4 Mean temperature of wettest quarter 5.8 The cell values obtained in the distribution modeling were 223 Temperature annual range 3.1 extracted under the different simulations (current, 2050 224 Precipitation of driest month 1.7 and 2070) to measure the predicted reduction in suitable 225 B. pauloensis C clade Precipitation of warmest quarter 36.9 area. The intersection of 2070 distribution models from 226 Precipitation of coldest quarter 23.7 both species (including the C, N, and S clades of B. pau- 227 Isothermality 13.1 loensis) was used to find future stable areas (i.e., refuges) 228 Max. temperature of warmest month 9.4 with high genetic diversity. The simulations were performed 229 Mean temperature of wettest quarter 8 firstly considering B. morio and B. pauloensis, and secondly 230 Mean temperature of driest quarter 6.4 considering B. morio and the three clades of B. pauloen- 231 Temperature seasonality 2.4 sis. These areas were compared to current protected areas, 232 B. pauloensis N clade Mean temperature of coldest quarter 27.9 including Full Protection Conservation Units (FPCU) and 233 Precipitation of wettest quarter 20.9 Sustainable Use Conservation Units (SUCU) (Supplemen- 234 Precipitation of wettest quarter 19.8 tary Material 1; available from http://siscom.ibama​ .gov.br​ ). 235 Precipitation of coldest quarter 15.9 Max. temperature of warmest month 15.5 B. pauloensis S clade Precipitation of warmest quarter 22.1 Results 236 Isothermality 21.3 Mean temperature of driest quarter 20.4 We verified high AUC values for all projections for both spe- 237 Precipitation of driest month 17.8 cies (> 0.97). The current modeling and future projections 238 Mean temperature of warmest 16 of distribution using the average of four GCM models, each 239 quarter one with four scenarios, as well the reduction in distribu- 240 Min. temperature of coldest quarter 2.4 tion area for each GCM model and scenario for B. morio, 241 B. pauloensis and its three clades are represented in Fig. 2. 242 The simulations performed separately for each GCM model 243 207 each one of the four scenarios of carbon emission were used with each scenario presented a high variation, which means 244 208 for final considerations. they are very distinct from each other (graphics in Fig. 2 and 245 209 We classified the suitability for each species and for the Supplementary Material 2). In 2070, according to the four 246 210 clades in B. pauloensisUNCORRECTED into three thresholds: maximum suit- GCM models together PROOF (average), the prediction is a strong 247 211 ability, corresponding to a predicted suitability higher than reduction in the distribution area, nearly 45%, for B. morio, 248 212 75%; medium suitability, with values above 50%; and mini- 49% for B. pauloensis (all clades together), and 37, 71 and 249 213 mum suitability, representing suitability above 25%. Based 60% for the C, N, and S B. pauloensis clades, respectively, 250 214 on this information, we evaluated the percent reduction of with suitability above 50% (Fig. 3). 251 215 suitable area for each species and infra-specific clade based Bombus morio and B. pauloensis (analyzed as a whole) 252 216 on the predicted future climate change. would face a reduction in their distribution on the northern 253 217 All maps and the data summarization were made in R portions of their ranges, mainly in the state of Minas Gerais. 254 218 (R Core Team 2013), using Geosphere (Hijmans 2014a, b), The B. pauloensis clades would be affected differentially 255

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Fig. 4 1.0 Bombus morio Intersection of current and future (2070) distribution mod- ◂ B. pauloensis eling of Bombus morio and Bombus pauloensis (whole species and clade C the threes clades separately: Central, North, and South clades) in dif- clade N clade S ferent levels of suitability, overlapped with conservation unit layers. 0.8 Suitability ranges in maximum, medium, and minimum probabilities (greater than 75%, 50–75%, and 25–50%, respectively) of predicted presence. The intersection of 2070 distribution models from both spe- B. pauloensis 0.6 cies (including the C, N, and S clades of ) was used to find future stable areas (red dashes). The two figures below represent the diversity of clades (B. morio, C, N and S clades of B. pauloensis) in the distribution for 2070 projections 0.4

with medium suitability proper for the four clades together, 286 0.2 located inside the large future refuge in the states of São 287 Paulo and Rio de Janeiro. Compared with current protected 288 areas, these future refuges apparently seem to be protected, 289 0.0 especially the large one, since the Serra do Mar region is 290 Current 2050 2070 covered by a mosaic of conservation units (Fig. 4). 291

Fig. 3 Distributional area reduction from modern day, 2015 and 2070, in suitability higher than 50% (medium probability) of Bombus Discussion 292 morio (main clade) and Bombus pauloensis (all clades together, Cen- tral, North, and South clades separately) According to future projections, until 2070 both B. morio 293 and B. pauloensis will have a distribution decrease of nearly 294 256 according to future predictions. Clade C should be the most 50% in the distribution in areas of medium suitability. This 295 257 stable, while clade N will suffer the stronger reduction from reduction will may not affect so drastically B. morio, since 296 258 the south of state of Minas Gerais until the north of state of it has high dispersal capacity (Moure and Sakagami 1962); 297 259 São Paulo, and clade S will be reduced mainly from west to and does not present genetic differentiation through its geo- 298 260 east of its original distribution. In general, north areas will graphic distribution indicating panmixia (Francisco et al. 299 261 face a reduction in the suitability, while the opposite will 2016; Françoso et al. 2016a, b). Therefore, the panmixia 300 262 happen in south areas. could be ensured and the genetic diversity would be easily 301 263 To investigate whether the current protect areas are proper recovered. However, the reduction in the distribution of B. 302 264 to protect both species of bumblebees in current days and in pauloensis considered as a unit was masked in comparison 303 265 the future, the suitability intersection under current and 2070 to the predictions performed for each clade separately. While 304 266 projections using both species together, and both species the clade C will likely be less affected by future climatic 305 267 but considering the internal clades of B. pauloensis were changes (reduction of 37%), clades N and S will suffer a 306 268 stacked with the protected areas (Fig. 4). The intersection reduction of ca. 71 and 60%, respectively. 307 269 area using B. morio and the clades of B. pauloensis is deeply Models that do not distinguish infra-specific units often 308 270 smaller in comparison to the whole species. According to fail to identify potential risks of climate changes to line- 309 271 the simulations using both species together, from current ages (Pearman et al. 2010; D`Amen et al. 2013). In fact, 310 272 days to 2070 there will be a reduction in area of 48% and the clades of B. pauloensis will respond very differently to 311 273 74% under medium and maximum suitability, respectively. future changes. The clade C showed to be the most stable in 312 274 The intersection of B. morio and the clades of B. pauloensis future projections analysis. Probably its current geographic 313 275 distribution modeling in 2017 showed three common areas distribution region may represent the species center of ori- 314 276 that can be named as future refuges. Two of these areas are gin and diversity. Yet, the two other clades within B. pau- 315 277 close in distanceUNCORRECTED and are located in the coast of southeast of loensis seem to have PROOF been originated in eastern São Paulo 316 278 Brazil, mainly in the east of states of São Paulo and Rio de state (Françoso et al. 2016a, b). According to Françoso et al. 317 279 Janeiro, and will be referred here as “large future refuge”. (2016a, b) the clade C is in Hardy–Weinberg equilibrium, 318 280 The third area is very small and located in the south of state i.e., microsatellite data indicated random mating and no 319 281 of Espírito Santo, and will be name here as “small future selective pressure among the genotypes from generation to 320 282 refuge”. generation. These data reinforce the hypothesis of popula- 321 283 The number of clades (B. morio and B. pauloensis clades tion stability and no expansion. In contrast, the clades N 322 284 C, N and S) in the distribution was performed for current and and S will suffer a remarkable decline, especially clade N. 323 285 2070 projections (Fig. 4). In 2070, there will be two areas These clades have been originated recently (Last Glacial 324

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325 Maximum and Last Inter Glacial in the Pleistocene, respec- bumblebees can survive in marginal and very disturbed habi- 375 326 tively), are in expansion, and present homozygote excess tats as agricultural fields (Lozier et al.2011 ) or urbanized 376 327 (Françoso et al. 2016a, b). Furthermore, they encompass the areas. This way, the guidelines for conservation suggested 377 328 edges of the species distribution, which are areas most likely by Ribeiro et al. (2009) must be considered, which includes 378 329 to change. Populations at the edge of the species distribu- prioritizing conservation of large mature forest fragments; 379 330 tion, even if not necessarily related to low genetic variabil- management of smaller fragments to maintain functionally 380 331 ity (Lira-Noriega and Manthey 2013), probably have a high linked mosaics; managing the matrix surrounding fragments 381 332 chance of extinction (Doherty et al. 2003). Reduced levels of to minimize edge effects and improve connectivity; and take 382 333 genetic diversity, which is expected in declining species, is restoration actions, particularly in certain key areas. 383 334 not necessarily observed (Lozier and Cameron 2009; Lozier 335 et al. 2011) since diversity loss through genetic drift in small The importance of phylogeographic lineages 384 336 effective populations can be replenished by migrants (Cam- in conservation 385 337 eron et al. 2011), unless a severe bottleneck there has been. 338 Williams (1986, 1988) to explain the pattern of species loss The uniqueness of a population (in terms of its allelic com- 386 339 in the United Kingdom, at least in part, argued that each position) and its diversity levels are criteria for the selection 387 340 bumblebee species occupies a particular climatic range. In of priority populations to be conserved (Petit et al. 1998). 388 341 the center of this range the species should be able to forage Considering the criteria for recognition of management units 389 342 most profitably, and persist in a range of habitats including (MU) as populations with a significant genetic diversity 390 343 those that are not ideal. If the quality of a habitat declines, (Moritz 1994), we suggest that the three phylogeographic 391 344 the populations near the edge of their climatic range are the groups of B. pauloensis should be treated as different MUs. 392 345 first to become extinct.Bombus bellicosus is a good exam- Therefore, significant well-preserved natural areas contain- 393 346 ple. The species distribution ranges from Argentina to state ing representative genetic diversity should be identified in 394 347 of Paraná, Brazil, and was abundant until the early 1980s. In each of the three groups to evaluate the current system of 395 348 recent surveys conducted from 2002 to 2005, no specimens conservation units. 396 349 were recovered in state of Paraná, at sites they used to occur Preserving central populations in a species’ niche may 397 350 (Martins and Melo 2010). protect populations with higher genetic diversity rather 398 than those populations that are environmentally peripheral 399 (Lira-Noriega and Manthey 2013). The protection of this 400 351 Future refuge large future refuge will be preserving not only the pattern 401 of biodiversity but also the processes that generated and 402 352 The large future refuge, located in the east of the states of maintained it (Smith et al. 2001), and not only for B. morio 403 353 São Paulo and Rio de Janeiro, has been already suggested and B. pauloensis, but also for many other species. Fur- 404 354 for 9 of 14 species analyzed, including spiders, harvestmen, thermore, we strongly recommend that population genetics 405 355 scorpions, amphibians, birds, and mammals (Porto et al. and conservation studies should consider the center and 406 356 2013). Furthermore this area is also very important by the edge of distribution and the diversity of species, since a 407 357 high level of species richness and endemism of different population in decline or expansion can just be in the edge 408 358 taxa including mammals (Costa et al. 2000), birds (da Silva or center of the species distribution. Studies focusing on 409 359 et al. 2004), and harvestmen (Pinto-da-Rocha et al. 2005). phylogeography, geographic distribution modeling, and 410 360 This stable area was firstly identified through the intersection the suitability values of distribution are useful tools to 411 361 of three distribution models for each species under differ- improve our understanding on process and population spe- 412 362 ent climatic scenarios: current, 6000 and 21,000 years ago cies dynamics. 413 363 (Porto et al. 2013). In addition, we found two common areas Acknowledgements 364 composed by Atlantic Forest inside the large future refuge We would like to thank J. Richard Abbott for 414 English review of the earlier version of the manuscript, the Missouri 415 365 in the states of São Paulo and Rio de Janeiro, suitable for B. Botanical Garden (Saint Louis, MO, USA) where this manuscript was 416 366 morio and theUNCORRECTED three clades of B. pauloensis together. PROOF 417 written, Flavio de Oliveira Francisco for comments, and Susy Coe- 367 Although this large future refuge apparently seems to lho for the laboratory maintenance. Financial support was provided 418 368 be protected, the Atlantic Forest is extremely degraded. Its by Fundação de Amparo à Pesquisa do Estado de São Paulo (Proc. 419 10/50597-5 and 13/12530-4; Ph.D. and scholarship to EF 2009/07124- 420 369 natural reserves protect only 9% of the remaining forest and 1, 2010/20548-2 and 2013/03961-1) and by Conselho Nacional de 421 370 1% of the original forest (Ribeiro et al. 2009). Unfortunately, Desenvolvimento Científico e Tecnológico (research fellowship to 422 371 most of these areas are small, the distance between frag- MCA). 423 372 ments is large, and are near to large cities, as São Paulo. 373 Therefore, there is no guarantee that these reserves will be 374 sufficient to protect this important refuge, even knowing that

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424 Author contributions EF, did the research and wrote the manuscript; da Silva JMC, de Sousa MC, Castelletti CHM (2004) Areas of end- 482 425 ARZ, assistance in data analysis, R scripts and advice; and MCA, emism for passerine birds in the Atlantic forest, South America. 483 426 advice, guidance and support in preparing the manuscript. Glob Ecol Biogeogr 13:85–92 484 da Silveira TMT, Raseira MCB, Nava DE, Couto M (2011) Blueberry 485 pollination in southern Brazil and their influence on fruit quality. 486 427 Compliance with ethical standards Rev Bras Frutic 33:81–88 487 De la Rúa P, Jaffé R, Dall’Olio R, Muñoz I, Serrano J (2009) Biodi- 488 Conflict of interest 428 The authors declare no potential conflict of inter- versity, conservation and current threats to European honeybees. 489 429 ests. Apidologie 40:263–284 490 Doherty PF, Boulinier T, Nichols JD (2003) Local extinction and turno- 491 ver rates at the edge and interior of species’ ranges. 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