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The Evolution of a Pollen Diet: Host Choice and Diet Breadth of Andrena Bees (Hymenoptera: Andrenidae)*

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The Evolution of a Pollen Diet: Host Choice and Diet Breadth of Andrena Bees (Hymenoptera: Andrenidae)* Apidologie 39 (2008) 133–145 Available online at: c INRA/DIB-AGIB/ EDP Sciences, 2008 www.apidologie.org DOI: 10.1051/apido:2007064 Original article The evolution of a pollen diet: Host choice and diet breadth of Andrena bees (Hymenoptera: Andrenidae)* Leah L. Larkin1,3, John L. Neff2,BerylB.Simpson1 a Section of Integrative Biology, The University of Texas at Austin, Austin, Texas 78712, USA b Central Texas Melittological Institute, Austin, TX 78731, USA c Present address: Department of Biology and Museum of Southwestern Biology, MSC 03 2020, University of New Mexico, Albuquerque, NM 87131, USA Received 18 June 2007 – Revised 1 November 2007 – Accepted 14 November 2007 Abstract – We investigate of two aspects of pollen diet of Andrena bees: the evolution of diet breadth within nearctic representatives of the genus, which includes both polylectic and oligolectic species; and host choice within an oligolectic clade of Andrena. We also evaluate phenology. Traits were mapped onto a molecular phylogeny to identify the ancestral character states. Overall, oligolecty appears to be the basal state within Andrena, and broader diets have evolved a number of times, suggesting that specialization is not a “dead end”. Within the oligolectic clade studied, host shifts occur predominantly between members of the same plant tribe, indicating a phylogenetic constraint to host-usage; however, shifts to other tribes are not uncommon, and may lead to adaptive radiation. Additionally, some lineages retain the ability to use pollen from an ancestral host-plant tribe. Finally, we find a correlation between using host plants in the family Asteraceae and fall emergence. Andrena / diet breadth / host choice / pollen / specialization 1. INTRODUCTION pollen (Guirguis and Brindley, 1974; Levin and Haydak, 1957; Williams, 2003) suggests Bee larvae feed mainly on pollen, a plant that not all pollen is created (chemically) tissue, and are thus herbivores. Bees, however, equal. are usually omitted from discussions of the Like other herbivores, bees exhibit a range evolution of host choice among phytophagous of diet breadth, from broadly generalist insects (e.g., Jaenike 1990; Mayhew, 1997; (polylectic) to narrowly specialist (oligolec- but see Bernays, 1988). This neglect may be tic). Why some bees restrict their diets while attributed to the often mutualistic nature of others are nearly catholic in their tastes has pollination and the apparent lack of chem- long intrigued bee biologists (Cruden, 1972; ical defenses in pollen, both of which dis- Linsley, 1958; Robertson, 1925; Wcislo and tinguish pollen collecting from the clearly Cane, 1996) who have proposed a variety of antagonistic interaction of phytophagy. How- ff models to explain the evolution of host choice. ever, even e ective pollinators, if suboptimal, The few pioneering studies which have at- may be viewed as competing with both the tempted to address the evolution of pollen plant and the optimal pollinator for pollen ff specificity are not backed by rigorous phy- (Thomson et al., 2000). Also, di erential per- logenetic hypotheses (e.g., Moldenke, 1979a; formance of some bees on alternate types of Müller, 1996; see Larkin, 2002, Appendix D). Corresponding author: L.L. Larkin, Perhaps half of all bees are oligolec- [email protected] tic (Michener, 2007). True oligolectic bees * Manuscript editor: Bryan Danforth collect pollen from a limited number of Article published by EDP Sciences and available at http://www.apidologie.org or http://dx.doi.org/10.1051/apido:2007064 134 L.L. Larkin et al. phylogenetically related host plants, either recognize and manipulate multiple hosts, may within a genus, tribe or family, across the explain specificity better than the quality of geographic range of the bee species. Only the chosen food (Bernays, 2001). In these con- when the host plant is locally scarce, as in texts, generalist behavior should be derived. years of drought or towards the end of the Only one study has addressed the evolution flowering season, will oligolectic bees utilize of diet breadth in a modern phylogenetic con- other plants (Linsley and MacSwain, 1958; text: Müller (1996) reported four shifts from JLN, personal observation). In the extreme, oligolecty to polylecty within 72 Old World and rare, case of monolecty, only one host anthidiine species (two additional shifts could species is visited (e.g., Cane et al., 1996). In not be polarized), as well as eight transitions contrast, polylectic species collect from a wide to new host taxa within oligolectic lineages. range of unrelated host plants, although they However, a re-analysis of his data set (Larkin, may specialize in the short term (e.g., fidelity 2002, Appendix D) resulted in a tree with little in honey bees and bumblebees); this behav- resolution, such that polarization could not be ior should not be confused with true oligolecty ascertained. In both Müller’s original analysis (Faegri and van der Pijl, 1979). and Larkin’s reanalysis, diet breadth at the root Little is truly known about the evolution of the tree was equivocal. of diet breadth in bees. The traditional view In the only other study to address host of floral host choice and feeding behavior in choice phylogenetically, Sipes and Wolf general has been that it evolved unidirection- (2001) investigated host shifting within ally, from generalist to specialist (Michener, an oligolectic genus of emphorine bees, 1954; Linsley, 1958; MacSwain et al., 1973; Diadasia, known to use hosts in five dis- Iwata, 1976; Moldenke, 1979a, b; Hurd et al., tantly related families. They found that four 1980) and that subsequent host shifts are to independent shifts to novel hosts occurred closely related plants. Rarer shifts to dis- from an ancestral host in the Malvaceae. As tantly related plants are thought to lead to Diadasia belongs to the tribe Emphorini, adaptive radiations. Some data supports this. whose members are entirely oligolectic, the Oligolecty appears twice in a phylogeny of authors did not attempt to assess whether Lasioglossum (Danforth et al., 2003), in L. oligolecty was an ancestral or derived trait (Hemihalictus) lustrans and again in the two overall. L. (Sphecodogastra) species. In both cases it is The genus Andrena (Andrenidae) is an derived. Moldenke (1979a) found no evidence excellent group with which to study the for evolution of polylecty from oligolecty. On evolution of pollen diet because it includes the other hand, Kratochwil (1984, 1991) and both polylectic and oligolectic taxa, the latter Cane and Eickwort (unpublished manuscript) specializing on many plant taxonomic groups, suggested that oligolecty may be the primitive including Asteraceae, Brassicaceae, Cor- condition in higher bee taxa. Wcislo and Cane naceae, Cucurbitaceae, Ericaceae, Fabaceae, (1996) supported the idea of multiple evolu- Hydrophyllaceae, Malvaceae, Onagraceae, tionary origins of oligolecty but were unable Portulacaceae, Salicaceae and Solanaceae in to polarize the evolution of diet breadth with- North America. The genus includes nearly out a phylogeny of bees as a whole. Michener 1400 described species and is essentially Ho- (2007) aired the merits of both viewpoints. larctic in distribution. Adults are usually Thus, the idea of evolution toward feeding univoltine, emergent for only about six weeks specificity is predominantly a theoretical con- per year, although a few Old World species struct. are bivoltine. Species in North America are Studies of other phytophagous insects in- predominantly vernal, although some groups dicate that avoidance of competition and/or have switched to autumnal emergence. Spe- predators may mediate host choice as much as cialists must time their emergence to coincide nutritional content of the host itself (Bernays, with the flowering period of their hosts, thus 1988; Bernays and Chapman, 1994), or that changes in phenology may be correlated with neurological limitations, such as the ability to a host shift or a change in diet breadth. Evolution of diet in Andrena 135 One group of specialists within Andrena groups included Ancylandrena larreae in the sub- is the subgenus Callandrena sensu lato family Andreninae, Protoxaea gloriosa in the Ox- Cockerell, consisting of 85 described species aeninae, and six panurgine species. The ML tree which are unusual among North American An- was found via an iterative search strategy using pro- drena for the preponderance of a fall flight gressively more thorough branch swapping algo- season. All but one specialize exclusively on rithms (Danforth et al., 1999). pollen of plants in the Asteraceae, particu- larly in the tribes Heliantheae, Astereae, Lac- tuceae, and Helenieae. Together, these four 2.1. Evolution of diet breadth and tribes account for 87% of museum collections phenology attributed to subgenus Callandrena s. l. for which a host has been identified. No mem- Diet breadth (oligolectic versus polylectic) and ber of subgenus Callandrena s. l. is polylec- phenology for each species in our phylogeny was tic, but members of the group exhibit host based on reports from the literature and on host shifts and differences in diet breadth, from nar- records from museum specimens. Diet breadth was rowly to broadly oligolectic. Thus, subgenus not determined for outgroup taxa. Phenology was Callandrena s. l. is an ideal system in which to coded for Ancylandrena, as all five known species study the evolution of these parameters. Only are spring emergent, but not for the panurgine out- group species. Characters of phenology (spring,
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