<I>Centris</I> and <I>Epicharis</I>
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ORIGINAL ARTICLE doi:10.1111/evo.12689 Gain and loss of specialization in two oil-bee lineages, Centris and Epicharis (Apidae) Aline C. Martins,1,2 GabrielA.R.Melo,2 and Susanne S. Renner1,3 1Department of Biology, University of Munich, 80638, Munich, Germany 2Department of Zoology, Federal University of Parana,´ PB 19020, Curitiba, PR 81531-980, Brazil 3E-mail: [email protected] Received October 17, 2014 Accepted May 21, 2015 It is plausible that specialized ecological interactions constrain geographic ranges. We address this question in neotropical bees, Centris and Epicharis, that collect oils from flowers of Calceolariaceae, Iridaceae, Krameriaceae, Malpighiaceae, Plantaginaceae, or Solanaceae, with different species exploiting between one and five of these families, which either have epithelial oil glands or hair fields. We plotted the level of oil-host specialization on a clock-dated phylogeny for 22 of the 35 species of Epicharis and 72 of the 230 species of Centris (genera that are not sister genera) and calculated geographic ranges (km2) for 23 bee species based on collection data from museum specimens. Of the oil-offering plants, the Malpighiaceae date to the Upper Cretaceous, whereas the other five families are progressively younger. The stem and crown groups of the two bee genera date to the Cretaceous, Eocene, and Oligocene. Shifts between oil hosts from different families are common in Centris, but absent in Epicharis, and the direction is from flowers with epithelial oil glands to flowers with oil hairs, canalized by bees’ oil-collecting apparatuses, suitable for piercing epithelia or mopping oil from hair fields. With the current data, a link between host specialization and geographic range size could not be detected. KEY WORDS: Bees, geographic ranges, molecular clock dating, oil flowers, phylogenetics, plant–insect interactions. Individual phytophagous insect species rarely use the full range and fatty oil. The oil is produced by epithelial glands or oil hairs of their food plants, and the relationship between the range sizes found in the flowers of 2000 species in well over 100 genera of insects and their food plants is not a simple linear one (Stewart in 11 families on all continents except Antarctica (Vogel 1974, et al. 2015). Range expansion may be facilitated by temporary 1988; Rasmussen and Olesen 2000; Machado 2004; Renner and escape from natural enemies, by the exploitation of novel food Schaefer 2010). In the New World, the oil bee/oil plant “system” plants that permit a broader set of habitats to be used, or by cli- extends from the southern United States to Patagonia and involves mate change, making changes in distributions difficult to attribute seven plant families and four groups of bees, Centris (Fig. 1A– to particular factors. A testable expectation in this context is that C), Epicharis, Tapinotaspidini, and Tetrapedia (Rasmussen and foraging specialization should limit range expansions and should Olesen 2000; Sigrist and Sazima 2004; Martins et al. 2013). be associated with narrower ranges than occupied by related less Considering that there are only 450 oil-bee species world- specialized species. Bees are phytophagous insects because they wide in few genera and subfamilies and yet 2000 species of plants feed their larvae with the gamete-containing pollen grains of flow- in numerous genera and 11 families with oil-offering flowers, ering plants. Plants have evolved numerous strategies to reduce colonization of new floral oil hosts by bees over evolutionary the proportion of their pollen that ends up in larval guts, includ- time is the expected scenario, and this is supported by molec- ing offering additional or alternative rewards (Simpson and Neff ular clock dated bee and plant phylogenies indicating very few 1981). One such alternative reward is floral oil, which is collected ancient oil-flower lineages and numerous younger ones (Ren- by the females of some 450 species of bees in 18 genera in Ap- ner and Schaefer 2010). Selection by bees on preadapted flowers inae and Melittinae that provision their cells with a mix of pollen that could be “recruited” as new oil sources would have involved C 2015 The Author(s). Evolution C 2015 The Society for the Study of Evolution. 1835 Evolution 69-7: 1835–1844 ALINE C. MARTINS ET AL. Figure 1. Oil-producing flowers of the Neotropics and Centris females collecting oil. (A) Centris aenea on oil-offering Byrsonima (Malpighiaceae). (B) Centris tarsata on oil-offering Krameria (Krameriaceae). (C) Centris trigonoides on oil-offering Angelonia inte- gerrima (Plantaginaceae). (D) Nierembergia species (Solanaceae). (E) Cypella herbertii (Iridaceae). (F) Calceolaria species (Calceolariaceae). Photos: (A)–(E) Antonio Aguiar, (F) Oscar Perez.´ oil-host broadening and polyphagous stages, possibly correlated Epicharis with 35 species occurring from 23° in the north to 34° with geographic range expansion, similar to what has been sug- in the south (Fig. 2A), both in the Apidae (Martins et al. 2014a). gested for phytophagous butterflies (Janz et al. 2006; Janz and Females in both genera feed on nectar from many kinds of flow- Nylin 2008; Nylin et al. 2013). ers, but feed their brood with pollen mixed with oil from a limited Here we address the question of host breadth evolution, in- number of flower types (Vinson et al. 1996, 1997; Aguiar and creasing specialization, and its possible relation to range size in Gaglianone 2003). The pollen and oil come from the flowers of two genera of Neotropical oil bees, Centris with 230 species oc- Malpighiaceae (Figs. 1A), Calceolariaceae (Fig. 1F), Iridaceae curring from 39° in the north to 47° in the south (Fig. 2B) and (Fig. 1E), Krameriaceae (Figs. 1B), Orchidaceae, Plantaginaceae 1836 EVOLUTION JULY 2015 GAIN AND LOSS OF SPECIALIZATION IN TWO OIL-BEE LINEAGES, CENTRIS AND EPICHARIS (APIDAE) known, the family assignments of their oil flowers are known from field observations (Table S1). For a species to be able to exploit a particular oil flower, it has to have the right type of oil- collecting apparatus, suitable either for piercing epithelia under which floral oil has accumulated or for mopping up oil from fields of minute hairs that secrete it. Epithelial glands exist in Malpighi- aceae, Krameriaceae, and Orchidaceae; oil-producing hair fields in Calceolariaceae, Iridaceae, Plantaginaceae, and Solanaceae. Bees that collect oil from epithelial glands have rigid setae on the tarsi of their forelegs and middle legs to break the epithelium. Bees that collect oil from oil-producing hair fields instead have spoon-like setae on the foreleg tarsi, quite different from the setae required for piercing epithelia (Vogel 1974; Neff and Simpson 1981). By combining data on the actual oil host of different species with clock-dated phylogenies for Centris and Epicharis as well as their main oil-host clades, we here reconstruct the evolutionary direction of oil-host use and the evolution or loss of specialization (i.e., oil foraging on one, two, three, or more plant families). For a subset of species, we infer whether the number of oil hosts relates to geographic range size. Material and Methods TAXON SAMPLING AND MOLECULAR CLOCK DATING We sampled 64 species of Centris with pointed or spoon-shaped setae on four legs, the condition found in the majority of species in this genus, four of the 10 species with setae on only the forelegs (C. hyptidis, C. thelyopsis, C. cineraria, C. anomala), and four species that have no oil-collecting apparatuses. All Epicharis have oil combs on both pairs of front legs, and we sampled 22 species of this genus. We also included 20 corbiculate bee species. The DNA data matrix is from Martins et al. (2014a), and includes 4300 aligned nucleotides from four ribosomal and protein-coding nuclear markers; namely, 28S, LW-Rhodopsin, elongation factor 1α-F2-copy, and RNA polymerase II. Divergence times were es- timated using the Bayesian approach implemented in BEAST 1.7 (Drummond et al. 2012), with a Yule tree prior as appropriate for species-level work, the GTR + G substitution model, which best fit the data as found with jModelTest v. 2 under the AIC (Darriba et al. 2012), and the uncorrelated lognormal (UCLN) re- Figure 2. Geographic ranges of Epicharis, Centris, and subclades laxed clock model. We used two calibration fossils. One was Apis of Centris discussed in the text. (A) Epicharis;(B)Centris; (C) range lithohermaea from the Middle Miocene Chojabaruˆ formation in of the Wagenknechtia clade (labeled in Fig. 4); (D) range of the Japan (it dates to the Langhian, a geological stage with an age hyptidis clade (Fig. 4). of 13.8–16 Mya). This is the oldest fossil assigned to the crown group of Apis, specifically the dorsata group (Engel 2006). We (Fig. 1C), and/or Solanaceae (Fig. 1D). For the purpose of this used this fossil to constrain the crown age of A. dorsata and A. study, specialists are species taking oil from only one family, cerana using a log-normal prior with a median of 1.26, SD of 0.5, whereas generalists are capable of exploiting the oil glands of and an offset of 15 Mya, which let ages fall between 13.8 and 16 more than one plant family. Although the nectar, pollen, and oil Mya. The other fossil was Kelneriapis eocenica, a stingless bee sources used by individual species Centris or Epicharis are not from Eocene Baltic Amber (Lutetian, with an age of 41.2–47.8 EVOLUTION JULY 2015 1837 ALINE C. MARTINS ET AL. Mya), and we used this fossil to constrain the stem age of the topologies compared with the published phylogenetic assessments African Meliponini (in our sampling: Hypotrigona, Meliponula, based on the same data. Except for minor differences in unsup- Plebeina, Axestotrigona) to 44 million years, using a log-normal ported nodes, trees were similar to the previously published ones prior with a median of 1.67, SD of 0.5, and an offset of 45 Mya, (Figs.