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«DISSERTATION vorgelegt an der Fakultät für Biologie der Ludwig-Maximilians-Universität München Christina Muck Seewiesen, September 2011 Die ...»

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BEHAVIOURAL AND HORMONAL

ASPECTS OF THE BREEDING ECOLOGY

IN SEX-ROLE REVERSED POLYANDROUS BIRDS

DISSERTATION

vorgelegt an der Fakultät für Biologie der

Ludwig-Maximilians-Universität München

Christina Muck

Seewiesen, September 2011

Die mündliche Prüfung fand am 19. November 2012 statt.

Gutachter der Dissertation PD. Dr. Wolfgang Goymann (Erstgutachten) Prof. Dr. Matthias Starck (Zweitgutachten) Prof. Dr. Wilfried Gabriel (Rigorosum) PD. Dr. Volker Witte (Rigorosum) Prof. Dr. Susanne Renner (Umlauf) Prof. Dr. Lutz Wiegrebe (Umlauf) Declaration Ehrenwörtliche Versicherung Ich versichere hiermit ehrenwörtlich, dass die von mir vorgelegte Dissertation von mir selbstständig und ohne unerlaubte Hilfe angefertigt ist.

München, den _____________ _________________________

Christina Muck Erklärung Hiermit erkläre ich, dass die Dissertation nicht ganz oder in wesentlichen Teilen einer anderen Prüfungskommission vorgelegt worden ist, und dass ich mich anderweitig einer Doktorprüfung ohne Erfolg nicht unterzogen habe.

München, den _____________ _________________________

Christina Muck Christina Muck PhD Thesis Table of Contents Statutory declaration and statement……………………………………...... 3 Content…………………………………………………………………………... 5 Declaration of contribution as co-authors………………………………… 7 Summary, English version…………………………………………………… 9 Summary, German version……...…………………………………………… 13 General Introduction………………………………………………………….. 17 Chapter One Paternity in the classical polyandrous black coucal (Centropus grillii) - a cuckoo accepting cuckoldry?

Chapter Two Testosterone does not directly modulate aggression but increases mate guarding in sex-role reversed female barred buttonquails………………….. 89 Chapter Three Hormones mirror personality – a mirror image stimulation test in male stonechats………………………………………………………………………... 115 Chapter Four Throat patch size and darkness co-varies with testosterone in females of a sex-role reversed species…………………………………………………….. 145

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Author Contributions Chapter One: Paternity in the classical polyandrous black coucal (Centropus grillii) - a cuckoo accepting cuckoldry?

C.M. contributed to the fieldwork, data analysis, and writing of the manuscript.

B.K. conducted the parentage analysis and contributed to the writing of the manuscript.

S.K. conducted the genotyping.

M.V. conducted the home range analysis.

W.G. designed the study and contributed to the fieldwork and to writing of the manuscript.

Chapter Two: Testosterone does not directly modulate aggression but increases mate guarding in sex-role reversed female barred buttonquails C.M. contributed to the study concept and design, practical work (simulated territorial intrusion experiments, blood sampling), data analysis, and writing of the manuscript.

W.G. contributed to the study concept and design, practical work (blood sampling), and discussion and writing of the manuscript.

Chapter Three: Hormones mirror personality – a mirror image stimulation test in male stonechats C.M. contributed to the study concept and design, practical work (simulated territorial intrusion experiments, blood sampling and hormone analysis), data analysis, and writing of the manuscript.

W.G. contributed to the study concept, and discussion and writing of the manuscript.

–  –  –

Chapter Four: Throat patch size and darkness co-varies with testosterone in females of a sex-role reversed species C.M. contributed to the study concept and design, practical work, plumage scoring, data analyses, and writing of the manuscript.

W.G. contributed to the study concept, practical work, and discussion and writing of the manuscript.

___________________________ ___________________________

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Summary In most vertebrate species, intra-sexual competition over resources and mates is higher among males than females. The strong mate-competition among males drives sexual selection to the development of male secondary sexual traits such as sexual ornaments and weaponry, a larger body size, and increased aggression, while females are the more choosy sex and take over parental care.

These conventional sex-roles are reversed in a small number of land vertebrate species. In such species, females typically establish, and vigorously defend, breeding and/or feeding territories and show a stronger intra-sexual competition than males. Males, on the contrary, incubate and take care for the young, often without any help by the female. In birds, exclusive male parental care is mostly associated with sequential or simultaneous polyandry.

The proximate mechanisms behind sex-role reversal and a polyandrous mating system remain an open question. Nevertheless, there are indications that steroid hormones such as testosterone, which is closely linked to the expression of ‘male’ characteristics in conventional sex-roles, may be involved in the reversal of behavioural, physiological and morphological characteristics in classically polyandrous species.





In my present thesis I, investigated three aspects that are characteristic for sex-role reversed polyandrous species, or may even be involved in the evolution of this mating system. These aspects were mate fidelity (i.e. extra-pair paternity rates), female aggression, and female secondary sexual traits (plumage colouration). I

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testosterone in their expression, in my study species. Furthermore, I explored the role of testosterone in male aggression and the potential connection of the birds’ personality to their behavioural and hormonal response during a territorial challenge, i.e. to their male typical behaviour.

In Chapter One I showed that promiscuity occurred at astonishingly high levels in a classically polyandrous species, the African black coucal. These results contradict theoretical models of the relationship between paternity and parental care, which imply low levels of extra-pair paternities for males to take over most of the parental duties. The high extra-pair paternity rates in black coucals seem to result from a low mate guarding ability of males, which is due to the dense habitat they live in, and due to the onset of incubation before clutch completion. Classical polyandry therefore may develop despite disadvantageous breeding conditions for the male.

In Chapter Two I found that experimentally elevated testosterone levels did not trigger an aggressive response during a territorial challenge in sex-role reversed polyandrous female barred buttonquails. Instead, high levels of testosterone affected female mate-guarding behaviour, which can be seen as a part of territorial defence, as well. In this species, circulating testosterone levels may therefore regulate behaviour involved in female-female competition. Moreover, considering the maletypical correlation of testosterone and mate-guarding intensity, testosterone may indeed be involved in the reversal of the sex-roles in barred buttonquails.

In Chapter Three I demonstrated that monogamous male stonechats responded agitated and/or aggressive towards their own mirror reflection and also towards a decoy, but not to a control glass panel. Yet none of these three challenges elicited a testosterone response related to the observed aggression. Interestingly,

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males showed one of two distinct patterns of aggression towards their own reflection in the mirror, and these patterns were related to hormone levels. Individuals which showed strong and physical aggression towards the mirror had characteristically higher testosterone and lower corticosterone levels, and males which did not exhibit aggression but only agitation behavior towards the mirror were characterized by relatively lower testosterone and higher corticosterone levels. Individual differences in hormone levels were consistent between the three experimental tests. From these results I hypothesize that in captive male stonechats the behavioral and hormonal response during competitive fights is not provoked by the stimulus alone but mainly modulated by the birds’ personality. Similarly, personality may be play a role in the development of sex-role reversed behaviour in polyandrous species – an hypothesis that has scarcely been investigated.

In Chapter Four I describe a highly significant correlation between testosterone and the expression of a melanin-based throat patch in classically polyandrous female barred buttonquails. In males, no such relationship was apparent despite comparable testosterone levels between the sexes, suggesting that females may have an enhanced sensitivity for testosterone or its metabolites. These results are unique as they reveal that even un-manipulated testosterone levels may trigger ‘male’ characteristics in polyandrous females, suggesting that a hormonal mechanism may be involved in sex-role reversal in barred buttonquails.

Despite the variety of subjects and species investigated in my thesis, the results of all four chapters demonstrate that the development of sex-role reversed characters and behaviour in polyandrous species is dependent on a variety of ecological and physiological aspects which may differ between species. While

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Zusammenfassung Bei den meisten Wirbeltieren ist die intra-sexuelle Konkurrenz über Resourcen und Paarungsmöglichkeiten stärker bei den Männchen als bei den Weibchen ausgeprägt. Durch sexuelle Selektion führt dieser starke Konkurrenzdruck unter den Männchen zu der Entwicklung von sekundären Geschlechtsmerkmalen, die typisch für die Männchen und ihre Rolle in einer Paarbindung sind. So weisen Männchen oft Ornamente und Waffen auf, haben einen kräftigeren Körperbau, und verhalten sich aggressiver als Weibchen. Diese wiederum sind wählerischer als Männchen und übernehmen meist die Aufzucht der Jungen.

Diese konventionelle Verteilung der Geschlechterrollen ist bei einigen wenigen Landwirbeltieren vertauscht. Bei diesen Arten erkämpfen und verteidigen Weibchen die Brut- und Futterhabitate, und auch die intra-sexuelle Konkurrenz um Partner ist bei den Weibchen stärker als bei den Männchen. Die Männchen hingegen brüten und kümmern sich um die Nachkommen, oft ohne jegliche Hilfe des Weibchens. Bei Vögeln ist diese extreme Form von väterlicher Brutpflege meist mit einem polyandrischen Paarungssystem verbunden.

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geschlechtstypischen Verhaltens und Merkmale in klassisch polyandrischen Arten spielen. Das Hormon Testosteron zum Beispiel ist sehr nah mit der Ausprägung von “männlichen” Charakteristika in konventionellen Geschlechterrollen verbunden, und beeinflusst möglicherweise auch „männliche“ Züge bei Weibchen.

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In meiner Dissertation habe ich drei Aspekte untersucht, die charakteristisch für Geschlechterrollentausch in polyandrischen Arten sind, oder sogar bei der Evolution dieses Paarungssystems eine Rolle spielen. Diese Aspekte sind Promiskuität

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Schwerpunkt zum einen im Auftreten dieser Aspekte und zum anderen in deren möglicher Testosteronabhängikeit bei den von mir untersuchten Arten. Zusätzlich

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Auseinandersetzungen zwischen Männchen beeinflusst werden und eventuel von deren Persönlichkeit abhängt.

Im Ersten Kapitel konnte ich zeigen, dass Promiskuität ein erstaunlich oft auftretendes Phänomen bei einer klassisch polyandrischen Vogelart, dem

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theoretischen Modellen über das Verhältnis von Vaterschaft und väterlicher Fürsorge für die Nachkommen. Diese Modelle setzen eine sehr niedrige Häufigkeit von ausserehelichen Vaterschaften als Bedingung für die Entwicklung von ausgiebiger Brutpflege der Männchen voraus. Die jedoch relativ hohe Rate an ausserehelichen Vaterschaften beim Grillkuckuck scheint darauf zu beruhen, dass die Männchen nur sehr schwer ihre Partnerinnen bewachen und vor anderen Männchen beschützen können. Dies wiederum liegt einerseits an der sehr dichten und hohen Vegetation des Bruthabitats, andererseits daran, dass die Männchen mit dem Brüten beginnen, sobald das erste Ei im Nest liegt, und die Weibchen somit freien Spielraum haben. Klassische Polyandrie kann demnach auch dann entstehen, wenn die Brutbedingungen für die Männchen unvorteilhaft sind.

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Bindenlaufhühnchen-Weibchen experimentell erhöhte Testosteronwerte keine aggressive Reaktion während territorialer Auseinandersetzungen hervorrufen.

Stattdessen intensivieren die hohen Testosteronwerte bei den Weibchen das Bewachen/Beschützen der Partner, was auch eine Art von Territoriumsverteidigung sein kann. Daher scheint bei Bindenlaufhühnchen Testosteron tatsächlich das Konkurrenzverhalten zwischen Weibchen zu beeinflussen oder gar zu regulieren.

Wenn man bedenkt, dass eine Korrelation zwischen Testosteron und Partnerbewachendem Verhalten eher bei Männchen bekannt ist, könnten diese Ergebnisse ein Hinweis darauf sein, dass Testosteron eine Rolle beim Geschlechterrollentausch der Bindenlaufhühnchen spielt.

Das Dritte Kapitel beschreibt die Reaktion von männlichen, monogamen Schwarzkehlchen auf ihr eigenes Spiegelbild oder auf einen ausgestopften Lockvogel. Beide Reize simulieren eine territoriale Bedrohung und lösten beunruhigtes oder aggressives Verhalten bei den Testvögeln hervor. Eine gleichzeitige Erhöhung der Testosteronwerte blieb jedoch aus. Interessanterweise verhielten sich die Männchen während der Spiegelbilddemonstration auffällig nach

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