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The Evolution of Social Dominance in Mouse Lemurs (Microcebus Spp.): the Effect of Sex and Species on Social Interaction

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The Evolution of Social Dominance in Mouse Lemurs (Microcebus Spp.): the Effect of Sex and Species on Social Interaction University of Veterinary Medicine Hannover Institute of Zoology The evolution of social dominance in mouse lemurs (Microcebus spp.): the effect of sex and species on social interaction THESIS Submitted in partial fulfilment of the requirements for the degree DOCTOR OF PHILOSOPHY (PhD) awarded by the University of Veterinary Medicine Hannover by Rina Evasoa Mamy Antananarivo, Madagascar Hannover, Germany 2018 Supervisor: Prof. Dr. Elke Zimmerman Prof. Dr. Ute Radespiel Supervision Group: Prof. Dr. Elke Zimmerman Prof. Dr. Ute Radespiel PD. Dr. Heike Hadrys Prof. Dr. Julia Ostner 1st evaluation: Prof. Dr. Elke Zimmerman University of Veterinary Medicine Hannover, Institute of Zoology Prof. Dr. Ute Radespiel University of Veterinary Medicine Hannover Institute of Zoology PD. Dr. Heike Hadrys University of Veterinary Medicine Hannover Institute for Animal Ecology and Cell Biology Prof. Dr. Julia Ostner Department of Behavioral Ecology Georg-August-University Göttingen 2nd evaluation: Prof. Dr. Cristina Giacoma University of Torino. Dept. of Life Sciences and System Biology, V. Accademia Albertina, 13. 10123 Torino, Italy Date of final exam: 29.10.2018 Part of the thesis has been published previously in: American Journal of Primatology Sponsorship: DAAD Great is our Lord, and of great power: his understanding is infinite. Psalms 147:5 To my parents my husband my sister my brother my nephew Table of contents Table of contents …………………………………………………………………………….. i List of figures………………………………………………………………………………… iii List of tables………………………………………………………………………………….. iv Previously published excerpts of this thesis…………………………………………………. v Summary……………………………………………………………………………………... vii Zusammenfassung……………………………………………………………………………. ix Chapter 1 – General introduction 1 1.1 Background……………………………………………………………………………. 1 1.2 Social tolerance and social relationship in primates…………………………………... 2 1.2.1 Affiliation …………………………………………………………………………....... 2 1.2.2 Agonistic behavior …………………………………………………………………...... 3 1.3 The evolution of social dominance…………………………………………………….. 3 1.4 The evolution of social tolerance and female dominance……………………………… 4 1.5 Mouse lemurs (Microcebus spp.)……………………………………………………..... 6 1.6 Anthropogenic pressures and threats acting on mouse lemur populations and species... 11 1.7 Aims and hypotheses………………………………………………………………….. 12 Chapter 2 - Variation in reproduction of the smallest‐bodied primate radiation, the mouse lemurs (Microcebus spp.): A synopsis 14 Chapter 3 – Determinants of interspecific variation in social tolerance in mouse lemurs (Microcebus spp.) 15 3.1 Introduction…………………………………………………………………………... 16 3.2 Results ………………………………………………………………………………... 19 3.2.1 Variation of affiliation during the encounters among dyad types and species ………. 19 3.2.2 Variation in rates of agonism and number of conflicts among dyad types and species.. 23 3.2.3 Variation in social dominance among dyad types and species……………………….. 26 3.3 Discussion…………………………………………………………………………….. 28 3.3.1 Influence of phylogeny on social tolerance…………………………………………... 29 3.3.2 Influence of habitat type on social tolerance…………………………………………. 31 3.3.3 Influence of reproductive activity on social tolerance………………………………... 32 3.3.4 Interspecific variability in social tolerance and implications for social diversity mouse lemurs………………………………………………………………………….. 33 3.4 Conclusions…………………………………………………………………………… 36 3.5 Methods……………………………………………………………………………….. 36 3.5.1 Study sites and study species…………………………………………………………. 36 3.5.2 Capture and selection of study animals……………………………………………….. 37 3.5.3 Experimental set-up and data collection……………………………………………… 38 3.5.4 Behavioral observations………………………………………………………………. 38 3.5.5 Statistical modelling…………………………………………………………………... 40 3.6 Declarations…………………………………………………………………………… 41 3.6.1 Ethics approval………………………………………………………………………... 41 i 3.6.2 Consent for publication………………………………………………………………. 41 3.6.3 Availability of data and material……………………………………………………… 41 3.6.4 Competing interests…………………………………………………………………… 41 3.6.5 Funding………………………………………………………………………………... 41 3.6.6 Author’s contributions………………………………………………………………… 42 3.7 Acknowledgements…………………………………………………………………….. 42 3.8 References……………………………………………………………………………… 42 3.9 Additional files ………………………………………………………………………… 48 Chapter 4- General discussion 64 4.1 Reproductive plasticity in mouse lemurs……………………………………………… 65 4.2 Social plasticity in mouse lemurs…………………………………………………….. 67 4.3 Plasticity in female dominance among mouse lemurs ………………………………. 69 4.4 Implications for taxonomy……………………………………………………………. 72 4.5 Implications for conservation………………………………………………………… 72 4.6 Outlook………………………………………………………………………………… 72 Chapter 5 – References for introduction and discussion 73 Acknowledgments 84 AFFIDAVIT 88 ii List of figures Figure 1.1 Distribution map for Microcebus spp………………………………………… 8 Figure 1.2 Picture of six study species (Microcebus spp.)………………………………. 9 Figure 3.1 Species comparison of the joint use of sleeping box………………………… 20 Figure 3.2 Species comparison of joint space use per dyad type ………………………. 22 Figure 3.3 Species comparison of total body contact per dyad type ………………….. 23 Figure 3.4 Aggression rates in mf-dyads for each species and sex separately………… 24 Figure 3.5 Aggression rates in mm-dyads for each forest type…………………………. 25 Figure 3.6 Species comparison of the total number of conflicts per dyad type. ………. 26 Figure 3.7 Map with northern half of Madagascar showing study sites of six study species………………………………………………………………………… 37 Figure 3.8 Encounter cage with eight compartments (A-H) and four extra locations (Ro, T, S, FS)………………………………………………………. 38 Figure 4.1 Evolution of seasonality and aseasonality reproduction pattern in lemur species………………………………………………………………………… 67 Figure 4.2 Partial clade showing evolution of female dominance in lemurs…………….. 71 iii List of tables Table 1.1 Distribution of different types of female dominance among lemur……………… 5 Table 3.1 Number of won conflicts for males and females in male-female dyads and their statistical comparison …………………………………………………………..... 27 Table 3.2 Number of male-male-dyads with significant male-male dominance per species 27 Table 3.3 Summary of findings on parameters that explained variation in social tolerance and its outcome …………………………………………………………………. 30 Table 3.4 Descriptive data of study species ………………………………………………... 48 Table 3.5 Statistical model for staying together in the sleeping box………………………. 49 Table 3.6 Statistical models for joint space use……………………………………………. 50 Table 3.7 Statistical models for total body contact………………………………………… 53 Table 3.8 Statistical model for aggression rate……………………………………………... 55 Table 3.9 Statistical models for number of conflicts……………………………………….. 57 Table 3.10 Summary of decided conflicts…………………………………………………. 60 iv Previously published excerpt of this thesis Chapter 2 of this thesis was published in the scientific peer-reviewed journal American Journal of Primatology. Publications: Chapter 2 was published on 16th August 2018 in the journal “American journal of primatology” entitled “Variation in reproduction of the smallest‐bodied primate radiation, the mouse lemurs (Microcebus spp.): a synopsis.” by Mamy Rina Evasoa, Ute Radespiel, Alida Frankline Hasiniaina, Solofonirina Rasoloharijaona , Blanchard Randrianambinina , Romule Rakotondravony , Elke Zimmermann (Volume 80 issue 7; DOI: 10.1002/ajp.22874). It was first published online on 16th May 2018. The copyright is held by John Wiley and Sons. The American journal of primatology is the original source of publication which can be accessed on https://onlinelibrary.wiley.com/doi/abs/10.1002/ajp.22874. The format of the chapter was adapted to the style of this thesis. The conception and design of the study presented in chapter 2 were performed by MRE, EZ and UR. The data were collected by MRE and AFH. The interpretation of the data was done by MRE, EZ and UR. The article was drafted by MRE, EZ, and critically revised by all authors. All authors approved the publication of the final version. Chapter 3 represents a manuscript, which is submitted to a scientific peer-reviewed journal of publication in BMC Ecology by Mamy Rina Evasoa, Elke Zimmermann, Alida Frankline Hasiniaina, Solofonirina Rasoloharijaona, Blanchard Randrianambinina, Romule Rakotondravony and Ute Radespiel. The conception and design of the study presented in chapter 3 was performed by MRE, EZ and UR. EZ and UR conceived and designed the study. MRE and AFH collected the data. MRE and UR analyzed the data and drafted the manuscript. All authors participated in the interpretation of the data. All authors read and approved the final manuscript. v Poster/ Presentations at scientific meetings: Rina Evasoa M., Hasiniaina A. F., Rasoloharijaona S., Randrianambinina B., Radespiel U., & Zimmermann E. (2017). “Variation in Intra-and Intersexual relationships in closely related species of a nocturnal primate radiation”. (Microcebus spp.). 7th European Federation for Primatology (EFP) meeting. University of Strasbourg, France. August 21-25, 2017. Rina Evasoa M., Hasiniaina A. F., Randrianambinina B., Rasoloharijaona S., Radespiel U., & Zimmermann E. (2017). “Reproductive variation in the large radiation of the smallest primates, mouse lemurs (Microcebus ssp.)”. Inaugural Madagascar Primatological Society Congress, Madagascar. December 13 – 16, 2017. Rina Evasoa M., Zimmermann E., Hasiniaina A. F., Randrianambinina B., Rasoloharijaona S., &. Radespiel U. (2018). “Is there a relationship between aggression levels, reproductive
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