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Sexual Dimorphism of the Sensory Systems in Bees (Hymenoptera, Apoidea) and the Evolution of Sex-Specific Adaptations in the Context of Mating Behavior

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Sexual Dimorphism of the Sensory Systems in Bees (Hymenoptera, Apoidea) and the Evolution of Sex-Specific Adaptations in the Context of Mating Behavior Sexual dimorphism of the sensory systems in bees (Hymenoptera, Apoidea) and the evolution of sex-specific adaptations in the context of mating behavior Sensorischer Geschlechtsdimorphismus bei Bienen (Hymenoptera, Apoidea) und die Evolution geschlechtsspezifischer Anpassungen im Kontext des Paarungsverhaltens Dissertation zur Erlangung des naturwissenschaftlichen Doktorgrades der Julius-Maximilians-Universität Würzburg vorgelegt von Martin Streinzer aus Wien, Österreich Würzburg, 2013 Eingereicht am: ....................................................................................................................... Mitglieder der Promotionskommission: Vorsitzender: Prof. Dr. Wolfgang Rössler (University Würzburg) Gutachter : Prof. Dr. Johannes Spaethe (Universität Würzburg) Gutachter: Prof. Dr. Thomas Schmitt (Universität Würzburg) Tag des Promotionskolloquiums: ............................................................................................. Doktorurkunde ausgehändigt am: ............................................................................................ This thesis is based on the following manuscripts: Manuscript I: Streinzer, M., Brockmann, A., Nagaraja, N., Spaethe, J. (2013). Sex and caste- specific variation in compound eye morphology of five honeybee species. PLoS One 8(2):e57702. doi: 10.1371/journal.pone.0057702 Manuscript II: Streinzer, M., Spaethe, J. (under review). A scientific note on peripheral compound eye morphology of small and normal-sized honeybee drones. Journal of Apicultural Research Manuscript III: Streinzer, M., Spaethe, J. (under review). The evolution of elaborate male visual systems in bumblebees (Hymenoptera, Apidae, Bombus). Zoological Journal of the Linnean Society Manuscript IV: Streinzer, M., Spaethe, J. (in preparation) Visual ecology of long-horned bee males (Eucera berlandi, Hymenoptera: Apidae): Adaptations of the visual system and mate detection. Manuscript V: Streinzer, M., Kelber, C., Pfabigan, S., Kleineidam, CJ., Spaethe, J. (in press). Sexual dimorphism in the olfactory system of a solitary and a eusocial bee species. Journal of Comparative Neurology. doi: 10.1002/cne.23312 STATEMENT OF AUTHOR CONTRIBUTIONS Manuscript I Streinzer, M., Brockmann, A., Nagaraja, N., Spaethe, J. (2013). Sex and caste-specific variation in compound eye morphology of five honeybee species. PLoS One 8(2):e57702. doi: 10.1371/ journal.pone.0057702 Contribution Author initials; decreasing order of responsibility Idea & study design MS AB JS Material & data collection MS NN Data analysis & interpretation MS Manuscript writing MS AB JS Manuscript II Streinzer, M., Spaethe, J. (under review). A scientific note on peripheral compound eye morphology of small and normal-sized honeybee drones. Journal of Apicultural Research Contribution Author initials; decreasing order of responsibility Idea & study design MS Material & data collection MS Data analysis & interpretation MS Manuscript writing MS JS Manuscript III Streinzer, M., Spaethe, J. (under review). The evolution of elaborate male visual systems in bumblebees (Hymenoptera, Apidae, Bombus). Zoological Journal of the Linnean Society Contribution Author initials; decreasing order of responsibility Idea & study design MS JS Material & data collection MS Data analysis & interpretation MS Manuscript writing MS JS Manuscript IV Streinzer, M., Spaethe, J (in preparation). Visual ecology of long-horned bee males (Eucera berlandi, Hymenoptera: Apidae): Adaptations of the visual system and mate detection Contribution Author initials; decreasing order of responsibility Idea & study design MS JS Material & data collection MS JS Data analysis & interpretation MS Manuscript writing MS JS Manuscript V Streinzer, M., Kelber, C., Pfabigan, S., Kleineidam C.J., Spaethe, J. (in press). Sexual dimorphism in the olfactory system of a solitary and a eusocial bee species. Journal of Comparative Neurology. doi: 10.1002/cne.23312 Contribution Author initials; decreasing order of responsibility Idea & study design MS CJK JS Material & data collection MS CK SP Data analysis & interpretation MS CJK JS Manuscript writing MS CJK JS TABLE OF CONTENTS 1. Summary 1 2. Zusammenfassung 3 3. Introduction 6 3.1. Bees (Hymenoptera:Apoidea:Apiformes) 6 3.2. Sexual dimorphism in bees 6 3.3. Bee mating 7 3.3.1. Mating systems 7 3.3.2. Signals and cues 8 3.4. Sensory systems investigated 9 3.4.1. Visual sense 9 3.4.1.1. Visual system 9 3.4.1.2. Adaptations of the compound eyes in bees 10 3.4.2. Olfactory sense 11 3.4.2.1. Olfactory system 11 3.4.2.2. Adaptations of the olfactory system in bees 13 3.5. Choice of study species 14 3.5.1. Honeybees (Hymenoptera: Apidae: Apinae: Apini: Apis LINNÉ) 14 3.5.2. Bumblebees (Hymenoptera: Apidae: Apinae: Bombini: Bombus LATREILLE) 15 3.5.3. The long-horned bee Eucera berlandi (DUSMET) 1926 (Hymenoptera: Apidae: Apinae: Eucerini) 16 4. Outline of the thesis 24 4.1. Aims and questions 24 4.2. Overview of manuscripts 25 5. Manuscript I: Sex and caste-specific variation in compound eye morphology of five honeybee species 30 6. Manuscript II: A scientific note on peripheral compound eye morphology of small and normal-sized honeybee drones 40 7. Manuscript III: The evolution of elaborate male visual systems in bumblebees (Hymenoptera, Apidae, Bombus) 45 8. Manuscript IV: Visual ecology of long-horned bee males (Eucera berlandi, Hymenoptera: Apidae): Adaptations of the visual system and mate detection 75 9. Manuscript V: Sexual dimorphism in the olfactory system of a solitary and a eusocial bee species 92 10. Discussion 116 10.1. Visual system 116 10.1.1. Females and workers 116 10.1.2. Queens 117 10.1.3. Males 118 10.1.4. Evolution of elaborate visual systems in Bombus 119 10.1.5. Spatial vision in Eucera mating behavior and Ophrys pollination 119 10.2. Olfactory system 120 10.2.1. Sex-specific olfactory systems 120 10.2.2. Olfaction in bumblebee mating and foraging behavior 121 10.3. Degree of sexual dimorphism 122 11. Erklärungen 128 12. Danksagung 129 SUMMARY 1. SUMMARY Bees have had an intimate relationship with humans for millennia, due to their importance as pollinators of fruit, vegetable and other crops, as well as suppliers of honey, wax and other products. This relationship has led to an extensive understanding of their ecology and behavior that has attracted researchers from such diverse fields as ecology, economics, sensory ecology, neurobiology, sociobiology and many others. One of the most comprehensively understood species is the Western honeybee, Apis mellifera. Its behavioral repertoire is rich, often attributed to its social lifestyle, and its learning skills, memory and mating behavior have intrigued many researchers. The pronounced caste and sexual dimorphism has facilitated the study of the causes and consequences of sex differences on the evolutionary and developmental levels. Our understanding of sex-specific investment in bees, in general, has continued to increase, but has remained phenomenological and superficial in many respects. Signals and cues employed in bee foraging and mating behavior are reasonably well understood in only a handful of species. Functional adaptations are described in some species, but the knowledge, especially on male- specific adaptations, is fragmentary. In this thesis I explored the variety of sensory adaptations for sex-specific behaviors in three model systems within the bees. Females share a similar ecology, engaging in nest construction, parental care and foraging, and therefore similar functional morphologies are to be expected. Males, however, engage mainly in mating behavior. A variety of male mating strategies has been described which differ in their spatiotemporal features and in the signals and cues involved, and thus selection pressures. As a consequence, males’ sensory systems are more diverse than those of females. In the first part of this thesis I studied adaptations of the visual system in honeybees. As a starting point I compared sex and caste-specific eye morphology among 5 species (Apis andreniformis, A. cerana, A. dorsata, A. florea, A. mellifera). While A. mellifera has been investigated in great detail, the Asian congeners have only recently received scientific interest. I found a strong correlation between body size and eye size in both female castes. Queens have a relatively reduced visual system which is in line with the reduced role of visual perception in their life history. Workers differed in eye size and functional morphology, which corresponds to known foraging differences among species. In males, the eyes are conspicuously enlarged in all species, but a disproportionate enlargement was found in two species. While it can be attributed to nocturnal mating activity in A. dorsata, the role of the eye enlargement in A. florea mating behavior is currently unknown. In addition, I demonstrate a correlation between male visual parameters and mating flight time, and propose that light intensities play an important role in the species-specific timing of mating flights. In the second study I investigated eye morphology differences among two phenotypes of drones in the Western honeybee. Besides normal-sized drones, smaller drones are reared in the colony, and suffer from reduced reproductive success. My results suggest that the smaller phenotype does not differ in spatial resolution of its visual system, but suffers from reduced light and contrast sensitivity which may exacerbate the reduction in reproductive success caused by other factors. In the third study I investigated
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