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Behavioural, Neural and Genetic Patterns Related to Age Or Lifespan in Companion Dogs

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Behavioural, Neural and Genetic Patterns Related to Age Or Lifespan in Companion Dogs dc_1507_17 Magyar Tudományos Akadémia Behavioural, neural and genetic patterns related to age or lifespan in companion dogs Életkorral, élethosszal összefüggő viselkedési, agyi és genetikai mintázatok kutyákban Enikő Kubinyi DSc thesis Akadémiai doktori értekezés 2019 Powered by TCPDF (www.tcpdf.org) dc_1507_17 Acknowledgement The dissertation represents a collaboration between people with different expertise but common interest: the love of dogs or more precisely, the love of studying the behaviour of dogs. I am very grateful to the members of the Senior Family Dog Project, Dóra Szabó, Borbála Turcsán, Lisa Wallis, Patrizia Piotti, Sára Sándor, Dávid Jónás, Kálmán Czeibert, Ivaylo Iotchev, Zsófia Bognár, Kitti Tátrai and Soufiane Bel Rhali for coming up with new ideas and realising the research on dog aging. I want to thank the founders of the Family Dog Project at the Department of Ethology, Eötvös Loránd University: Vilmos Csányi, Ádám Miklósi, József Topál, and Antal Dóka for their continuous and friendly support. Among them, Ádám Miklósi was my mentor during the PhD and postdoc period and originally it was József Topál who suggested me to study cognitive aging. Special thanks go for my long-time colleagues, Márta Gácsi, Zsófia Virányi, Péter Pongrácz, Attila Andics, Boglárka Morvai, Dorottya Ujfalussy, Tamás Faragó, Ákos Pogány, Vera Konok, Judit Vas, Gabriella Lakatos, Flóra Szánthó, Anna Gergely, Borbála Győri, and all students and employees of the Department of Ethology. I truly appreciate the contribution of my co-authors and collaborators from different institutes. On the studies of this thesis I had the pleasure and honour to work with Tamás Vicsek, Máté Nagy, Zsuzsa Ákos, Róbert Beck (ELTE, Dept. of Biological Physics), Anna Kis (Institute of Cognitive Neuroscience and Psychology), Rachel S. Carson (Kalamazoo College), Petrouchka Hulsboch (Katholieke Universiteit Leuven), Örs Petneházy (University of Kaposvár), Pauline Marty (École Nationale Vétérinaire de Toulouse). I owe thanks to my former and present PhD, MSc, BSc, and internship students for their work, dog owners for their voluntary and enthusiastic participation in the behaviour tests, and especially for those owners who donated the body of their beloved dogs to the Canine Brain and Tissue Bank. My husband, Attila Dávid Molnár has helped me a lot in my career since 1994, and we could count on the support of the grandparents in supervising our three children, Vanda, Vilja, and András when their parents were busy with work. Financially the research presented in the dissertation was supported by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (Grant Agreement No. 680040), the János Bolyai Research Scholarship of the Hungarian Academy of Sciences, the Bolyai+ ÚNKP-18-4 New National Excellence Program of the Ministry of Human Capacities, the Hungarian Brain Research Program 2017-1.2.1-NKP- 2017-00002, FP7/215554, and the Hungarian Scientific Research Fund (PD48495, OTKA K84036). 2 Powered by TCPDF (www.tcpdf.org) dc_1507_17 Contents I. General introduction .............................................................................................................. 4 1 Four questions about aging ................................................................................................ 5 2 Healthy, typical and pathological aging ............................................................................ 7 3 Conventional model organisms of aging ........................................................................... 8 4 Canine aging .................................................................................................................... 10 5 Aims ................................................................................................................................. 20 II. Experimental studies .......................................................................................................... 25 6 Ethics Statement .............................................................................................................. 25 7 The prevalence of age-related cognitive decline in companion dogs across the entire adult lifespan .................................................................................................................... 26 8 Demographics of companion dogs across age groups and identifying the key variables associated with health status ............................................................................................ 37 9 Developing a behaviour test for assessing discrimination and reversal learning ............ 51 10 Positivity effect in dogs: do old dogs experience less negative emotions? ..................... 61 11 Age-related effects in looking at faces of humans and conspecifics ............................... 72 12 Age-related changes in human-based personality traits and associations with owner and dog demographics ............................................................................................................ 85 13 Interventions to increase play and training motivation may alleviate the negative effects of aging .......................................................................................................................... 103 14 The relationship between age, personality, dominance and leadership in a group of dogs ....................................................................................................................................... 123 15 Dominance status and age in companion dogs sharing the same household ................. 135 16 Age related differences in the spindling activity of the sleeping brain ......................... 151 17 The genetic background of longevity based on whole-genome sequence data of two methuselah dogs ............................................................................................................. 158 III. General discussion .......................................................................................................... 170 18 Theses: Novel scientific achievements .......................................................................... 170 19 Putting things together ................................................................................................... 174 20 Perspectives ................................................................................................................... 177 21 References ...................................................................................................................... 186 22 List of the experimental studies in the dissertation (Part II.) ......................................... 223 23 Publications related to the theses ................................................................................... 224 3 Powered by TCPDF (www.tcpdf.org) dc_1507_17 “I have sometimes thought of the final cause of dogs having such short lives and I am quite satisfied it is in compassion to the human race; for if we suffer so much in losing a dog after an acquaintance of ten or twelve years, what would it be if they were to live double that time?” Sir Walter Scott I. General introduction Aging is a naturally occurring complex biological process, and it is one of the most relevant problems to understand how active and healthy aging can be achieved. Currently, 8-10% of the human population is over the age of 60 years, but in 2050 it is expected to be 22%, resulting in a significant challenge for health care (Bloom et al., 2015). With the rapidly aging population, related research is a priority. The study of dog aging is significant from at least two perspectives. First, dogs’ increased lifespan is a direct consequence of sharing their life with humans. Roughly, one-third of all family households maintain one or more pet dogs around the world, with many reporting that their dog is considered as part of their family. Despite the growing number of aged dogs in present day populations, very little is known about the actual prevalence and risk factors of age-related changes in dogs (Azkona et al., 2009; Neilson, Hart, Cliff, & Ruehl, 2001; Osella et al., 2007; Salvin, McGreevy, Sachdev, & Valenzuela, 2010). The relatively extended lifespan in dogs artificially enhances the proportion of dogs with cognitive decline in the population which is a serious welfare concern. Research could facilitate the early recognition and treatment of certain conditions, as well as provide a way (e.g. feeding, physical and mental exercises) for a preventive and predictive approach. Second, according to several authors (e.g. Chapagain et al. 2018; Cotman and Head 2008; Gilmore and Greer 2015; Head 2013; Milgram et al. 1999; Overall 2000; Szabó, Gee, and Miklósi 2016; Waters 2011) dogs provide a good model for human aging which has unprecedented advantages in terms of general validity to the human case. Pet dogs share our environment more than any other species and develop homologues of the most prevalent age- related human diseases. As companion animals, the same environmental factors affect them as people (chemicals, air pollution, noise pollution, lack of exercise, etc.) which are suspected risk factors of cognitive decline in humans. Pet dogs also excel in displaying socio-cognitive skills in interaction with humans compared to other animals. To achieve the goal to increase the population of healthy agers, our research aims to describe the causal factors contributing to the emergence of cognitive decline and to
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