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Causes and Consequences of Cuticular Hydrocarbon Divergence in Parabiotic Ants

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Causes and Consequences of Cuticular Hydrocarbon Divergence in Parabiotic Ants Causes and consequences of cuticular hydrocarbon divergence in parabiotic ants Dissertation Zur Erlangung des Grades Doktor der Naturwissenschaften Am Fachbereich Biologie Der Johannes-Gutenberg Universität Mainz Philipp Peter Sprenger geb. am 23.03.1991 in Dernbach Mainz, 2020 Dekan: 1. Berichterstatter: 2. Berichterstatter: Tag der mündlichen Prüfung: 24.04.2020 Table of contents Zusammenfassung ………………….…………………………………...………………………… 3 Summary .…...………………………………………………………………………………………. 5 General introduction …………….………………………………………………………………... 7 Species interactions and their potential influence on cuticular hydrocarbon divergence Chapter 1 …………………………………………………………………………………………. 21 Cuticular hydrocarbons as potential mediators of cryptic species divergence in a mutualistic ant association Chapter 2 ……………………………………………………………………………………….. 57 Influence of mutualistic lifestyle, mutualistic partner, and climate on cuticular hydrocarbon profiles in parabiotic ants Chapter 3 ...................................................................................................................................... 95 Identification of candidate genes involved in cuticular hydrocarbon differences between cryptic, parabiotic ant species Chapter 4 ……………………………………………………………...………………………… 119 Nestmate recognition in the cryptic species of Crematogaster levior Chapter 5 ……………………………………………………………………………...………… 139 Dinner with the roommates: Trophic niche differentiation and competition in a mutualistic ant-ant association Chapter 6 ………………………………………………………………………………...……… 159 Cuticular hydrocarbons in ants and other insects: How and why they differ among individuals, colonies and species Perspectives ……………………………………………………………………….…………….… 193 How and why cuticular hydrocarbons could be important in species divergence Author contributions ………………………………………………………………………….…. 205 Acknowledgements ……………………………………………………………..…...…………... 207 References ………………………………………………………………………………………… 209 Curriculum vitae …………………………………………………………………………………. 239 1 2 Zusammenfassung Interaktionen zwischen Arten wie Konkurrenz, Antagonismus und Mutualismus werden oft als Gründe für die Diversifizierung phänotypischer Merkmale angeführt und tragen somit signifikant zur Artenvielfalt auf der Erde bei. Kutikuläre Kohlenwasserstoffe (engl. CHCs) sind die Hauptkomponenten der Wachsschicht, die fast alle terrestrischen Arthropoden besitzen. Die Profile dieser CHCs können als komplexes phänotypisches Merkmal betrachtet werden. Sie haben vielfältige Funktionen, insbesondere schützen sie Insekten vor Austrocknung, sind aber auch wichtig für die chemische Kommunikation. Diese Kom- munikationsfunktion ist besonders wichtig für soziale Insekten wie Ameisen, Bienen, Wespen oder Termiten. Um den Erfolg einer Kolonie zu sichern ist es von größter Wichtigkeit Informationen wie die Kolonie- und Kastenzugehörigkeit, Anwesenheit und Fruchtbarkeit der Königin oder das Alter einzelner Individuen auszutauschen. Weiterhin benutzen Ameisen CHC Profile um mutualistische Partnerspezies zu identifizieren. Eine besondere Form eines solchen Mutualismus ist die Parabiose, sprich zwei Ameisenarten, die sich friedlich ein Nest teilen. In dieser Arbeit untersuche ich die Ursachen und Folgen der Divergenz von CHC Profilen in den parabiotischen Ameisenarten Crematogaster levior und Camponotus femoratus aus dem tropischen Regenwald Südamerikas. In Kapitel 1 untersuche ich den Artstatus chemisch verschiedener Formen beider oben erwähnter Gattungen und diskutiere welche Rolle CHCs in der Speziation spielen könnten. Ich demonstriere schlüssig, dass beide, Cr. levior und Ca. femoratus, eigentlich aus zwei kryptischen Arten bestehen, welche sich trotz nur geringer morphologischer Unterschiede stark in ihren CHC Profilen, dem genetischen Hintergrund und in Cr. levior auch in auf der Kutikula nachweisbaren Sekundärmetaboliten unterscheiden. Durch eine detaillierte Unter- suchung der CHC Unterschiede innerhalb und zwischen den kryptischen Arten von Cr. levior und Ca. femoratus, identifiziere ich mehrere ultimate Ursachen für die Variation in den CHC Profilen in Kapitel 2. Besonders die parabiotische Lebensweise führt zu starken Veränderungen wie beispielweise der Verlängerung der Kohlenstoffketten der CHCs in beiden Ca. femoratus Arten, jedoch nur einer der Cr. levior Arten. Dies scheint innerhalb der Crematogaster Arten einen phylogenetisch fortschrittlichen Zustand darzustellen. Obwohl die kryptischen Arten nah verwandt sind, zeigen sie stark verschiedene CHC Profile. Daher untersuchte ich weiterhin in Kapitel 3 ob Genexpressionsunterschiede am Ort der CHC Biosynthese diese Unterschiede erklären könnten. In diesem Kapitel identifiziere ich mehrere Kandidatengene und ihre Expressionsmuster als proximate Ursachen für die CHC Unter- schiede. In vielen Fällen konnte ich hier zeigen, dass die Genexpressionsunterschiede sich in den Unterschieden im CHC Profil widerspiegeln. Die starken Unterschiede in den CHC Profilen haben vermutlich Folgen für die Nest- genossenerkennung und das Aggressionsverhalten der Ameisen, weshalb ich die Erkennung innerhalb und zwischen den kryptischen Arten von Cr. levior in Kapitel 4 untersuchte. 3 Hierbei versuchte ich herauszufinden, welche Substanzen oder strukturelle Substanzklassen für die Erkennung eine Rolle spielen. Übereinstimmend mit der Hypothese das die Verlängerung der Kohlenstoffketten die Kohlenwasserstoffmoleküle schwieriger wahr- zunehmen macht, fand ich, dass CHC Extrakte der Cr. levior Art mit kürzeren Kohlenwasser- stoffketten scheinbar besser wahrnehmbar waren und daher aggressiver behandelt wurden. Weil die Divergenz der CHC Profile und die Aufspaltung in zwei kryptische Arten übereinstimmen, scheint es wahrscheinlich, dass dies weitere ökologische Folgen haben könnte. In Kapitel 5 untersuchte ich daher ob die Artaufspaltung von Partitionierung in der Nahrungsnische zwischen a) den mutualistischen Partnern und b) den kryptischen Arten von Cr. levior und Ca. femoratus begleitet wurde. Die Ergebnisse implizieren, dass die Mutualisten um Nahrung konkurrieren und die Konkurrenz möglicherweise durch einen Trade-off zwischen Nahrungsauffindung und Dominanz verringert wird. Die Unterschiede zwischen den kryptischen Arten jedoch waren sehr subtil, was darauf hindeutet, dass ent- weder Partitionierung in Nischendimensionen stattfindet, die wir bisher nicht untersucht haben oder dass die kryptischen Arten ein Beispiel für „neutrale Arten“ sind. In Kapitel 6 verschaffe ich einen Überblick über die Ebenen und das Ausmaß der Variation von CHCs bei Ameisen aber auch anderen Insekten. Durch die Aufarbeitung aktueller Literatur biete ich einen detaillierten Einblick in Quellen für fixierte und plastische Variation auf individueller, kolonieweiter, populationsweiter und artspezifischer Ebene. Weiterhin dis- kutiere ich welche Faktoren zu adaptiven CHC Änderungen führen und wie diese durch biosynthetische und biophysikalische Mechanismen eingeschränkt werden. Zusammenfassend zeigt diese Arbeit die Existenz kryptischer Arten mittels integrativer Taxonomie, bietet Einblicke in die komplexen Selektionsdrücke, die die Evolution von CHC Profilen beeinflussen und identifiziert mehrere Kandidatengene, die in die Divergenz der CHC Profile involviert sein könnten. Diese Divergenz in CHC Profilen könnte eine wichtige Rolle bei der Speziation einnehmen. Es ist jedoch bisher unklar ob die chemischen Unter- schiede zur Partnerwahl und damit zu präzygotischer reproduktiver Isolation beitragen, oder ob die Profilunterschiede erst nach der Speziation verstärkt wurden. Während CHC Divergenz, wenn sie zu assortativer Paarung führte, sympatrische Artbildung erlauben würde, würden allopatrische Populationen durch Prozesse wie Isolation-by-distance, genetische Drift oder lokale Anpassung in ihren CHC Profilen divergieren. Weiterhin zeigt diese Arbeit, dass die kryptischen Arten der parabiotischen Ameisen ein interessantes Modell sein könnten um zu untersuchen wie ökologisch ähnliche Arten einen Konkurrenzausschluss vermeiden können und möglicherweise auch für die Untersuchung „neutraler Prozesse“, die Artenkoexistenz in tropischen Ökosystemen ermöglichen. 4 Summary Species interactions such as competition, antagonism and mutualism are thought to promote diversification in phenotypic traits and thus significantly contribute to species diversity on Earth. Cuticular hydrocarbons (CHCs) are the major components of the waxy layer covering basically all terrestrial arthropods. They can be seen as a complex phenotypic trait and have multiple functions, most importantly protecting insects from desiccation and acting as agents of chemical communication. The communication functions of CHCs are especially important in social insects, such as ants, bees, wasps or termites. To successfully run a colony, they need to exchange information such as colony or caste membership, queen presence and fertility or age of an individual. Furthermore, ants use CHC profiles to identify mutualistic partner species. A special form of such a mutualism is parabiosis, i.e. two ant species mutualistically sharing the same nest. In this thesis, I investigate the causes and consequences for the divergence of CHC profiles in the parabiotic ant species Crematogaster levior and Camponotus femoratus from the South American rainforest. In Chapter 1, I elucidate the species status of chemically diverged morphs of the ants of both genera mentioned above and discuss which role CHCs could have mediating speciation. I conclusively demonstrate that both, Cr. levior and Ca. femoratus,
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