Playing with Extremes Origins and Evolution of Exaggerated Female

Molecular Phylogenetics and Evolution 115 (2017) 95–105 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Playing with extremes: Origins and evolution of exaggerated female forelegs MARK in South African Rediviva bees ⁎ Belinda Kahnta,b, , Graham A. Montgomeryc, Elizabeth Murrayc, Michael Kuhlmannd,e, Anton Pauwf, Denis Michezg, Robert J. Paxtona,b, Bryan N. Danforthc a Institute of Biology/General Zoology, Martin-Luther-University Halle-Wittenberg, Hoher Weg 8, 06120 Halle (Saale), Germany b German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany c Department of Entomology, Cornell University, 3124 Comstock Hall, Ithaca, NY 14853-2601, USA d Zoological Museum, Kiel University, Hegewischstr. 3, 24105 Kiel, Germany e Dept. of Life Sciences, Natural History Museum, Cromwell Rd., London SW7 5BD, UK f Department of Botany and Zoology, Stellenbosch University, Matieland 7602, South Africa g Laboratoire de Zoologie, Research institute of Biosciences, University of Mons, Place du Parc 23, 7000 Mons, Belgium ARTICLE INFO ABSTRACT Keywords: Despite close ecological interactions between plants and their pollinators, only some highly specialised polli- Molecular phylogenetics nators adapt to a specific host plant trait by evolving a bizarre morphology. Here we investigated the evolution Plant-pollinator interaction of extremely elongated forelegs in females of the South African bee genus Rediviva (Hymenoptera: Melittidae), in Ecological adaptation which long forelegs are hypothesised to be an adaptation for collecting oils from the extended spurs of their Greater cape floristic region Diascia host flowers. We first reconstructed the phylogeny of the genus Rediviva using seven genes and inferred Trait evolution an origin of Rediviva at around 29 MYA (95% HPD = 19.2–40.5), concurrent with the origin and radiation of the Melittidae Succulent Karoo flora. The common ancestor of Rediviva was inferred to be a short-legged species that did not visit Diascia. Interestingly, all our analyses strongly supported at least two independent origins of long legs within Rediviva. Leg length was not correlated with any variable we tested (ecological specialisation, Diascia visitation, geographic distribution, pilosity type) but seems to have evolved very rapidly. Overall, our results indicate that foreleg length is an evolutionary highly labile, rapidly evolving trait that might enable Rediviva bees to respond quickly to changing floral resource availability. 1. Introduction Several bee taxa have developed specialised pilosity for collecting pollen. Central European bees of various families have convergently Since most pollinator species visit a broad range of host plant spe- evolved highly specialised facial hair adapted to gather pollen from cies (Bosch et al., 2009; Waser et al., 1996), morphological traits in nototribic flowers in the families Lamiaceae and Scrophulariaceae pollinators are only rarely thought to have evolved in direct response to (Müller, 1996). Other bees collecting pollen from the narrow flowers of a specific host plant morphology (Feinsinger, 1983; Vázquez and Aizen, Boraginaceae and Primulaceae have a highly modified leg and 2004). However, specialist pollinators that are highly dependent on a mouthpart pilosity for effectively extracting pollen from the hidden particular host taxon might exhibit remarkably bizarre morphological anthers of their host-plants (Muller, 1995). Particularly fascinating are adaptations to their host plants. For example, some fly species within adaptations of bees for collecting floral oil (Buchmann, 1987). Oil the Nemestrinidae and Tabanidae have developed an extremely elon- collecting behaviour has been documented in (i) the tribes Centridini, gated proboscis in order to obtain nectar from the long, narrow, tubular Tetrapedini, Ctenoplectrini and Tapinotaspini of the family Apidae flowers of their host plants (Goldblatt and Manning, 2000). As flies with (Buchmann, 1987; Cocucci et al., 2000; Houston et al., 1993; Neff and tongues matching the tubes of their hosts are likely to gain more floral Simpson, 1981; Steiner and Whitehead, 2002) and in (ii) two of the reward, morphological adaptation to the host is probably associated genera of Melittidae: Macropis and Rediviva (Michez et al., 2009). with a fitness advantage (Pauw et al., 2009). However, we note that the While the majority of bees are adapted to oil collection by posses- phenotypic adaptations in the bee may not necessarily translate into sing highly specialised hairs on either their legs or abdomen fitness benefits and enhanced pollination of the plant. (Buchmann, 1987), females of the melittid genus Rediviva have evolved ⁎ Corresponding author at: Institute of Biology/General Zoology, Martin-Luther-University Halle-Wittenberg, Hoher Weg 8, 06120 Halle, Germany. E-mail address: [email protected] (B. Kahnt). http://dx.doi.org/10.1016/j.ympev.2017.07.025 Received 28 December 2016; Received in revised form 22 June 2017; Accepted 26 July 2017 Available online 27 July 2017 1055-7903/ © 2017 Elsevier Inc. All rights reserved. B. Kahnt et al. Molecular Phylogenetics and Evolution 115 (2017) 95–105 remarkably long forelegs for accessing floral oils within the elongate within the genus Rediviva by sequencing six nuclear genes and one floral spurs of their principal host-plants (Vogel, 1974, 1984; Steiner mitochondrial gene and reconstructing tree topologies using Bayesian and Whitehead, 1990, 1991). Apart from Rediviva, elongated forelegs approaches. We then mapped leg length onto the hypothesised phylo- have only been described for Centris hyptidis (Apidae) and Tapinotaspis geny and estimated the tempo of leg length evolution. We also mapped species (Apidae) that regularly visit Angelonia (Scrophulariaceae, other characteristics potentially associated with leg length variation, Machado et al., 2002), Nierembergia (Solanaceae, Cosacov et al., 2008) such as foreleg pilosity, bee distribution (winter vs. summer rainfall and Sisyrinchium (Iridaceae, Cocucci et al., 2000). This suggests con- area), and the use of Diascia hosts, onto the phylogeny and tested if vergent evolution of long legs for the purpose of oil collection. these traits are related to the evolution of leg length. Moreover, we also In order to collect floral oil, a female Rediviva inserts its forelegs into investigated if long legged bees are more specialised than short legged the Diascia floral spurs, rubs against the spur walls that are covered species. Our study not only provides the first thorough phylogeny for with oil-secreting trichome elaiophores, and absorbs the oil with spe- the genus Rediviva but is also the first to address the evolution of leg cialised hairs on the tarsal segments (Buchmann, 1987; Steiner and length across Rediviva bees. Whitehead, 1988; Vogel, 1984). The oil is then transferred to the bee's hindlegs (Vogel, 1984) and transported to the nest, where it serves as 2. Materials and methods larval food and probably in brood cell lining (Pauw, 2006; Kuhlmann, 2014). During oil collection, pollen attaches to a species-specific part of 2.1. Phylogenetics and evolution of Rediviva the bee’s body (Pauw, 2006; Waterman et al., 2011). About half of the Diascia species described are self-incompatible and highly dependent on 2.1.1. Taxon sampling and sequencing Rediviva bees for reproduction (Steiner and Whitehead, 1988). Flowers Rediviva belongs to the family Melittidae, a small, relictual family of other Scrophulariaceae (Alonsoa, Colpias, Hemimeris), Iridaceae, that forms the sister group to all other extant bee families based on Stilbaceae (Anastrabe, Bowkeria, Ixianthes) and Orchidaceae also serve molecular data ((Brady et al., 2011; Branstetter et al., 2017; Hedtke as sources of oil for several Rediviva species (Kuhlmann and Hollens, et al., 2013; Kahnt et al., 2015; Peters et al., 2017). Melittidae is esti- 2015; Manning et al., 2002; Manning and Brothers, 1986; Pauw, 2006, mated to have originated in the late Cretaceous (Cardinal and Danforth, 2005; Waterman et al., 2011; Whitehead et al., 2008; Whitehead and 2013; Branstetter et al., 2017; Peters et al., 2017). The monophyly of Steiner, 2001, 1996) and some of these plant species seem to depend Melittidae has been under dispute for a long time since morphological solely on Rediviva for pollination (Steiner and Whitehead, 2002, 1991). synapomorphies are lacking and molecular studies either fail to support In addition, all Rediviva species visit a range of local flowers for pollen or only weakly support monophyly (Danforth et al., 2006a, 2006b, or nectar (Whitehead et al., 2008; Whitehead and Steiner, 2001) and 2013; Michener, 2007). However, recent studies were able to provide thereby likely pollinate them. From a conservation perspective, Rediviva substantial support for a monophyletic Melittidae (Branstetter et al., bees are therefore probably of great importance for maintaining plant 2017; Hedtke et al., 2013). Rediviva might also be rendered para- diversity in southern Africa (Pauw and Bond, 2011; Pauw and Hawkins, phyletic due to the inclusion of the closely related genus Redivivoides 2011). (Michez et al., 2009). Female Rediviva species vary in foreleg length from 6.5 mm (R. al- The genus Rediviva is restricted to southern Africa, as are the ap- bifasciata) to an extreme of up to 26 mm (R. emdeorum; Whitehead and proximately 73 species of its host plant genus Diascia (Steiner, 2011). Steiner,

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