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The Genetics of Burrowing Behavior in Peromyscus Mice in the Lab and the Field The Genetics of Burrowing Behavior in Peromyscus Mice in the Lab and the Field The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Bedford, Nicole L. 2019. The Genetics of Burrowing Behavior in Peromyscus Mice in the Lab and the Field. Doctoral dissertation, Harvard University, Graduate School of Arts & Sciences. Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:42029821 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA The genetics of burrowing behavior in Peromysc mice in the lab and the field a dissertation presented by Nicole L. Bedford to The Department of Organismic and Evolutionary Biology in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the subject of Organismic and Evolutionary Biology Harvard University Cambridge, Massachusetts February 2019 ©2019 – Nicole L. Bedford all rights reserved. Thesis advisor: Professor Hopi E. Hoekstra Nicole L. Bedford The genetics of burrowing behavior in Peromysc mice in the lab and the field Abstract Striking variation in animal behavior has repeatedly evolved among closely-related species over short evolutionary timescales. However, the proximate and ultimate mechanisms that give rise to behav- ioral diversity remain poorly understood. Here, we leverage variation in burrow architecture among deer mice (genus Peromysc), which ranges from short and simple to long and complex. First, we discover that complete, adult-like burrowing behavior emerges earlier in postnatal development in a complex-burrowing species. We then identify a genetic region associated with both precocious burrowing in juveniles and burrow length in adults. Second, we find that the complex-burrowing species digs cooperatively with both same- and opposite-sex partners. However, opposite-sex pairs are more socially cohesive and more likely to engage in simultaneous, coordinated digging, thereby producing longer burrows than same-sex pairs. Third, we design and implement a custom radio frequency identification (RFID) system to non-invasively monitor burrow use in the wild. We find that, in nature, mice frequent the burrows of close genetic relatives and may receive inclusive fitness benefits by maintaining a network of shared burrows. Last, we develop a novel phenotyping plat- form for the high-throughput quantification of multiple components of burrowing behavior. Using this video-recorded assay, we uncover variation in the temporal dynamics of burrow construction that contribute to interspecific variation in overall burrow structure. We then use a genetic cross between mice with divergent burrow architectures to test for associations between genotype and behavior. By isolating the particular components of burrowing behavior that explain the bulk of heritable variation between species, we can begin to describe the number and types of mutations required to produce, over evolutionary time, a complex behavior from a relatively simple ancestral form. Taken together, these studies clarify the developmental and genetic mechanisms of burrow- ing behavior in Peromysc and characterize the social and ecological contexts in which burrowing behavior is expressed. iii Contents 0 Introduction 1 1 Peromyscus mice as a model for studying natural variation 6 1.1 Abstract . 7 1.2 Introduction . 7 1.3 Distribution and habitat . 9 1.4 Diet and predators . 12 1.5 Parasites and disease . 13 1.6 Longevity . 13 1.7 Life history . 14 1.8 Mating system and parental care . 15 1.9 Home building . 16 1.10 Pigmentation . 17 1.11 Adaptation to mountains, deserts and cities . 19 1.12 Peromysc and the history of evolutionary thought . 19 1.13 Peromysc in the Laboratory . 21 1.14 Conclusions . 22 1.15 Box 1. Future directions for Peromysc research . 23 1.16 References . 24 2 Evolution and genetics of precocious burrowing behavior in Peromyscus mice 32 2.1 Abstract . 33 2.2 Results . 34 2.3 Discussion . 43 2.4 References . 46 3 Behavioural mechanisms of cooperative burrowing in Peromyscus mice 50 3.1 Abstract . 51 3.2 Introduction . 51 3.3 Results . 53 iv 3.4 Discussion . 64 3.5 References . 67 4 The adaptive value of burrowing behavior in the wild 71 4.1 Abstract . 72 4.2 Introduction . 73 4.3 Results . 74 4.4 Discussion . 83 4.5 References . 85 5 The genetic architecture of burrowing behavior in Peromyscus mice: advances from automated phenotyping 88 5.1 Abstract . 89 5.2 Introduction . 90 5.3 Materials and Methods . 92 5.4 Results . 93 5.5 Discussion . 99 5.6 References . 101 6 Conclusion 103 Appendix A Supplementary Material for Chapter 2 104 A.1 Materials and Methods . 105 A.2 Supplementary Figures and Tables . 111 Appendix B Supplementary Material for Chapter 3 115 B.1 Materials and Methods . 116 B.2 Supplementary Figures . 123 Appendix C Supplementary Material for Chapter 4 124 C.1 Materials and Methods for November 2017 Fieldwork . 125 C.2 Materials and Methods for May 2016 Fieldwork . 132 C.3 Results for May 2016 Fieldwork . 134 Appendix D Supplementary Material for Chapter 5 140 D.1 Supplementary Figures and Tables . 141 v Listing of figures 1.1 Simplified phylogeny depicting the relationships among muroid rodent model organ- isms. 8 1.2 North American distributions of eight Peromysc species. 9 1.3 The ecology of Peromysc varies both within and among species. 12 1.4 Genetic crosses between the pale beach mouse P. polionot leucocephal and the darker mainland mouse P. p. polionot........................... 18 2.1 The ontogeny of burrow construction in two sister species of Peromysc. 36 2.2 Reciprocal interspecific cross-fostering. 38 2.3 Genetic dissection of precocious burrowing in P. polionot x P. maniculat hybrids. 40 2.4 Effect of the dominant P. polionot allele on linkage group 2 on burrowing behavior in backcross hybrids. 42 3.1 P. polionot pairs cooperatively construct burrows that are nearly twice as long as those dug by individuals. 55 3.2 P. polionot females dig longer burrows after cohabitation with a male, regardless of pregnancy status. 57 3.3 Sex differences in digging behaviour across social contexts. 59 3.4 Opposite-sex pairs have more affiliative and fewer agonistic interactions. 62 3.5 Opposite-sex pairs are more likely to engage in efficient simultaneous digging. 63 4.1 Home-range characterization and burrow use patterns as determined by capture-recapture and RFID-monitoring. 75 4.2 Groups of mice visit networks of spatially clustered burrows. 77 4.3 Nightly activity summaries, distance between burrows, and burrow use evenness. 78 4.4 Distribution of RFID timestamps and fraction of spatiotemporal overlap in the pop- ulation as a function of time-bin size. 78 4.5 Spatiotemporal overlap at burrow entrances. 79 4.6 Genetic relatedness predicts spatiotemporal overlap between pairs. 81 4.7 Close relatives sleep in the same burrow. 81 4.8 Distributions of burrow site attributes for 36 RFID-monitored burrows. 82 vi 4.9 Long burrows are better buffered against severe temperature fluctuations. 83 5.1 Novel burrowing assay reveals key differences in burrowing behavior between two Per- omysc species. 94 5.2 Trait correlations reveal additional species differences in burrowing behavior. 96 5.3 A QTL for time spent digging. 97 5.4 QTLs for component traits of burrowing behavior. 98 A.1 Morphological and motor development in P. polionot and P. maniculat. 111 A.2 Effect of genotype on juvenile and adult burrowing behavior in hybrids. 112 B.1 Different pair configurations differ in total time spent digging, burrow length, and di- vision of labour. 123 C.1 Beach mouse home-range sizes estimated from utilization distributions. 128 C.2 Home-range characterization and burrow use patterns as determined by capture-recapture and RFID-monitoring. 135 C.3 Groups of mice visit networks of spatially clustered burrows. 136 C.4 Nightly activity summaries, distance between burrows, and burrow use evenness. 137 C.5 Distribution of RFID timestamps and fraction of spatiotemporal overlap in the pop- ulation as a function of time-bin size. 137 C.6 Spatiotemporal overlap at burrow entrances. 138 C.7 Close relatives show greater spatiotemporal overlap. 139 D.1 Pearson correlation coefficients for pairs of component burrowing traits. 141 vii Acknowledgments I would like to thank Hopi and members of the Hoekstra Lab, both past and present, who have been such supportive friends and colleagues. Many thanks are owed to my Dissertation Committee for sharing their expertise and advice. I would also like to thank members of the OEB community, particularly my cohort who have been sources of inspiration and solidarity through- out the various stages of graduate school. I thank my family for always encouraging me to do my best. Finally, I thank Adam Nelson who, from the very beginning, has provided love and support in countless ways. viii 0 Introduction 1 In 1963, Niko Tinbergen1 outlined a set of four guiding questions that would unify and focus the various disciplines that, at the time, fell loosely under the emerging science of Ethology. Collectively, the four questions—ontogeny, evolution, survival value, and causation—address both historical and contemporary processes as well as proximate and ultimate causes2. In principle, this approach could be applied to any problem in Biology, but it has proven particularly useful for clarifying thinking about behavior. Tinbergen argued that “a comprehensive, coherent science of Ethology has to give equal attention to each of them and to their integration.” Under this framework, I present a series of studies that, taken together, offer a broad understanding of burrowing behavior in North American deer mice (genus Peromysc).
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