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The Case of Feather Mites

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The Case of Feather Mites On the diversification of highly host-specific symbionts: the case of feather mites Jorge Doña On the diversification of highly host-specific symbionts: the casePhD Thesis of feather mites Recommended citation: Doña, J. (2018) On the diversification of highly host-specific symbionts: the case of feather mites. PhD Thesis. Universidad de Sevilla. Spain. On the diversification of highly host-specific symbionts: the case of feather mites Memoria presentada por el Licenciado en Biología y Máster en Genética y Evolución Jorge Doña Reguera para optar al título de Doctor por la Universidad de Sevilla Fdo. Jorge Doña Reguera Conformidad de los directores: Director Director Fdo.: Dr. Roger Jovani Tarrida Fdo.: Dr. David Serrano Larraz Tutor Fdo.: Dr. Manuel Enrique Figueroa Clemente 4 List of works derived from this Ph.D. thesis: - Chapter 1: Doña, J.*, Proctor, H.*, Mironov, S.*, Serrano, D., and Jovani, R. (2016). Global associations between birds and vane-dwelling feather mites. Ecology, 97, 3242. - Chapter 2: Doña, J., Diaz‐Real, J., Mironov, S., Bazaga, P., Serrano, D., & Jovani, R. (2015). DNA barcoding and mini‐barcoding as a powerful tool for feather mite studies. Molecular Ecology Resources, 15, 1216-1225. - Chapter 3: Vizcaíno, A.*, Doña, J.*, Vierna, J., Marí-Mena, N., Esteban, R., Mironov, S., Urien, C., Serrano, D., Jovani, R. Enabling large-scale feather mite studies: An Illumina DNA metabarcoding pipeline (under review in Experimental and Applied Acarology). - Chapter 4: Doña, J., Potti, J., De la Hera, I., Blanco, G., Frias, O., and Jovani, R. (2017). Vertical transmission in feather mites: insights into its adaptive value. Ecological Entomology, 42, 492-499. - Chapter 5: Doña, J., Proctor, H., Serrano, D., Johnson, KP., Oddy-van Oploo, A., Ascunce, MS., Huguet-Tapia, JC., Jovani, R. (2018). Feather mites play a role in cleaning host feathers: New insights from DNA metabarcoding and microscopy. Molecular Ecology, in press. - Chapter 6: Doña, J., Sweet, AD., Johnson, KP, Serrano, D., Mironov, SV., Jovani, R. (2017). Cophylogenetic analyses reveal extensive host-shift speciation in a highly specialized and host-specific symbiont system. Molecular Phylogenetics and Evolution, 115, 190-196. - Chapter 7: Doña, J., Proctor, H., Mironov, S., Serrano, D., Jovani, R. (2017). Host-specificity, infrequent major host-switching and the diversification of highly host-specific symbionts: the case of feather mites. Global Ecology and Biogeography, 27, 188-198. - Chapter 8: Doña, J., Serrano, D., Mironov, S., Montesinos-Navarro, A, Jovani, R. Chasing host-switches: A DNA metabarcoding study on the eco-evolutionary scenario of host-shift speciation of host-specific symbionts (under review in Molecular Ecology —invited article). - Appendix 1: Vierna, J.*, Doña J.*, Vizcaíno, A., Serrano D and Jovani, R. (2017). PCR cycles above routine numbers do not compromise high-throughput DNA barcoding results. Genome, 60, 868-873. - Appendix 2: Mironov, S., Doña, J., Jovani, R. (2015). A new feather mite of the genus Dolichodectes (Astigmata: Proctophyllodidae) from Hippolais polyglotta (Passeriformes: Acrocephalidae) in Spain. Folia Parasitologica, 62, 32. 5 - Appendix 3: Esteban, R., Doña, J., Vierna, J., Vizcaíno, A., Serrano, D., Jovani, R. (2018). The complete mitochondrial genome of the feather mite Trouessartia rubecula Jablonska, 1968 (Astigmata: Analgoidea: Trouessartiidae). Mitochondrial DNA Part B: Resources, 3, 652-654. - Appendix 4: Jovani, R., Doña J., Labrador, M and Serrano D. (2017). Opening the doors of parasitology journals to other symbionts. Trends in Parasitology, 33, 578-579. Other works published during this Ph.D. thesis: - Doña, J.*, Ruiz-Ruano, FJ.*, Jovani, R. (2015). DNA barcoding of Iberian Peninsula and North Africa Tawny Owls Strix aluco suggests the Strait of Gibraltar as an important barrier for phylogeography. Mitochondrial DNA, 27, 4475-4478. - Doña, J.*, Moreno-García M.*, Criscione CD., Serrano, D., Jovani, R. (2015). Species mtDNA genetic diversity explained by infrapopulation size in a host-symbiont system. Ecology and Evolution, 5, 5801-5809. - Carlson, C., Burgio, K., Dougherty, E., Phillips, A., Bueno, V., Clements, C., Castaldo, C., Dallas, T., Cizauskas, C., Cumming, C., Doña, J., Harris, N., Jovani, R., Mironov, S., Muellerklein, O., Proctor, H., Getz, W. Parasite biodiversity faces extinction and redistribution in a changing climate. Science advances, 3, e1602422. - De Rojas, M., Doña, J., Jovani, R., Dimov, I., Zurita, A., Callejón, R., Rodríguez-Plá, M., Evidence of cryptic species in the genus Tinaminyssus (Acari: Rhinonyssidae) based on morphometrical and molecular data. Experimental and Applied Acarology, in press. * Authors contributed equally to this work 6 Table of Contents Abstract ...................................................................................................... 9 Resumen .................................................................................................. 11 Introduction ............................................................................................... 13 Objectives ................................................................................................. 19 Chapter 1. Global associations between birds and vane- dwelling feather mites ................................................................................................................... 21 Chapter 2. DNA barcoding and minibarcoding as a powerful tool for feather mite studies. ........................................................................................................ 59 Chapter 3. Enabling large-scale feather mite studies: An Illumina DNA metabarcoding pipeline ........................................................................................ 77 Chapter 4. Vertical transmission in feather mites: insights on its adaptive value ............................................................................................................................ 97 Chapter 5. Feather mites play a role in cleaning host feathers: New insights from DNA metabarcoding and microscopy. ........................................................ 139 Chapter 6. Cophylogenetic analyses reveal extensive host-shift speciation in a highly specialized and host-specific symbiont system ...................................... 139 Chapter 7. Host specificity, infrequent major host switching and the diversification of highly host-specific symbionts: The case of vane-dwelling feather mites ................................................................................................................. 139 Chapter 8. Chasing host-switches: A DNA metabarcoding study on the eco- evolutionary scenario of host-shift speciation of host-specific symbionts............. 165 7 Appendix 1. PCR cycles above routine numbers do not compromise high- throughput DNA barcoding results ..................................................................... 191 Appendix 2. A new feather mite of the genus Dolichodectes (Astigmata: Proctophyllodidae) from Hippolais polyglotta (Passeriformes: Acrocephalidae) in Spain ................................................................................................................. 203 Appendix 3. The complete mitochondrial genome of the feather mite Trouessartia rubecula Jablonska, 1968 (Astigmata: Analgoidea: Trouessartiidae). ......................................................................................................................... 219 Appendix 4. Opening the Doors of Parasitology Journals to Other Symbionts ......................................................................................................................... 223 Discussion .............................................................................................. 191 Conclusions ............................................................................................ 237 Bibliography ............................................................................................. 239 Agradecimientos | Acknowledgements .................................................... 281 8 Abstract One of the most relevant and poorly understood topics in Evolutionary Ecology is symbiont evolutionary diversification. Since Fahrenholz's rule (1913), the idea of symbionts speciating following hosts speciation (i.e., cospeciating) has been pervasive. Recent studies, however, have shown that host-shift speciation (speciation after switching to a new host) is almost as relevant as cospeciation in explaining symbiont diversification. Also, these studies have revealed that methodological biases have favored cospeciation. Nonetheless, most symbiont groups, especially those highly host-specific and specialized in which cospeciation is expected to be the rule, such as the feather mites of birds, were yet to be studied. Symbionts are the most abundant and diverse organisms on Earth, and thus essential components of ecosystems. However, symbionts have attracted historically less attention than other organisms and their study entails numerous methodological challenges, so surprisingly little is understood about the basic biology and ecology of many symbiont groups, especially the non-parasitic. By studying vane-dwelling feather mites living permanently on the surface of flight feathers of birds (Acariformes: Astigmata: Analgoidea and Pterolichoidea), this thesis is a contribution to fill this gap. This thesis is divided into three parts: 1) First, resources and molecular tools enabling large-scale studies
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