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Evolution of Boldness and Exploratory Behavior in Giant Mice from Gough Island

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Evolution of Boldness and Exploratory Behavior in Giant Mice from Gough Island bioRxiv preprint doi: https://doi.org/10.1101/2020.09.10.292185; this version posted September 10, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 2 3 4 5 6 Evolution of Boldness and Exploratory Behavior in Giant Mice from Gough Island 7 8 9 Jered A. Stratton, Mark J. Nolte, and Bret A. Payseur 10 11 12 Laboratory of Genetics, University of Wisconsin – Madison, Madison, WI 53706 13 14 Corresponding Author: Jered A. Stratton 15 Email for Correspondence: [email protected] 16 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.10.292185; this version posted September 10, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 17 Abstract 18 Island populations are hallmarks of extreme phenotypic evolution. Radical changes 19 in resource availability and predation risk accompanying island colonization drive changes 20 in behavior, which Darwin likened to tameness in domesticated animals. Although many 21 examples of animal boldness are found on islands, the heritability of observed behaviors, a 22 requirement for evolution, remains largely unknown. To fill this gap, we profiled anxiety 23 and exploration in island and mainland inbred strains of house mice raised in a common 24 laboratory environment. The island strain was descended from mice on Gough Island, the 25 largest wild house mice on record. Experiments utilizing open environments across two 26 ages showed that Gough Island mice are bolder and more exploratory, even when a shelter 27 is provided. Concurrently, Gough Island mice retain an avoidance response to predator 28 urine. F1 offspring from crosses between these two strains behave more similarly to the 29 mainland strain for most traits, suggesting recessive mutations contributed to behavioral 30 evolution on the island. Our results provide a rare example of novel, inherited behaviors in 31 an island population and demonstrate that behavioral evolution can be specific to different 32 forms of perceived danger. Our discoveries pave the way for a genetic understanding of 33 how island populations evolve unusual behaviors. 34 35 Keywords 36 Island syndrome, house mice, anxiety, island evolution, island tameness, behavior 37 38 39 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.10.292185; this version posted September 10, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 40 Introduction 41 Organisms that colonize islands experience unique environmental challenges that 42 require novel solutions [1]. New kinds and distributions of resources on islands can select 43 for new foraging strategies [2-4]. For many island colonizers, a loss of predators alleviates 44 the need for behavioral or morphological defenses [2, 5-6]. If resources are difficult to 45 acquire and predatory risk is absent, the optimal foraging-risk ratio is highly skewed, 46 favoring exploration and boldness [7-9]. Island populations, therefore, provide 47 opportunities to test hypotheses about the evolution of behavior in novel environments. 48 Populations that spread to islands often display behavioral changes. Many 49 populations lose anti-predator behaviors [6]. Some island inhabitants are more easily 50 approached by humans, a phenomenon Darwin called “island tameness” [10-11]. In some 51 island rodents, territoriality and conspecific aggression are reduced compared to mainland 52 populations [12-13]. Behavioral responses to island environments sometimes occur in the 53 context of other phenotypic shifts. New behaviors are often accompanied by transitions in 54 life history and morphology [12,14-15] in a pattern referred to as the “island syndrome” 55 [16]. 56 Although behavior is suspected to be an important component of adaptation to 57 island conditions, the question of whether island populations harbor heritable changes in 58 behavior has rarely been answered [13,17]. Demonstrating that behavior has evolved on 59 islands requires evidence of genetic change in behavioral traits. 60 A promising organismal system for testing hypotheses about behavioral evolution in 61 response to island environments is found on Gough Island, a remote volcanic island in the 62 middle of the South Atlantic Ocean. Despite the remote location of Gough Island, over 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.10.292185; this version posted September 10, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 63 2,700 miles from the nearest mainland, house mice (Mus musculus domesticus) colonized 64 the island, probably via sealing ships from western Europe a few hundred generations ago 65 [18-20]. In a remarkable phenotypic transformation, these mice evolved a body size twice 66 that of their mainland counterparts [21-22]. Laboratory-born offspring of Gough Island 67 mice (hereafter “GI mice”) maintain their unusual size, confirming that this morphological 68 distinction has a genetic basis [23-24]. On Gough Island, mice live without the predators 69 and without the human commensals they commonly exploit for food and shelter on the 70 mainland [21,25]. The diet of GI mice is highly variable and seasonal, with invertebrates 71 (mainly earthworms) and seeds being the most stable food source [22]. During the winter 72 season, GI mice predate on endangered seabird populations that use the island as a nesting 73 ground, leading to the deaths of an estimated 2 million chicks and/or eggs per year [26]. 74 The combination of increased body size, novel consumption of birds, loss of predatory 75 danger, and removal of human commensals predicts the evolution of increased exploration 76 and boldness in GI mice. Because GI mice are western European house mice (Mus musculus 77 domesticus), the same subspecies as the laboratory mouse [20], established methods in 78 biomedical research can be applied to profile behavioral evolution. 79 In this article, we use GI mice to examine recent behavioral evolution on an island. 80 By exposing juvenile and adult mice to novel environments with different levels of 81 perceived risk, we uncovered multiple lines of evidence that GI mice are bolder (i.e. less 82 anxious) and more exploratory than mice from a mainland reference strain. The detection 83 of these differences in inbred strains raised in a common environment demonstrates that 84 they are inherited. Our findings indicate that GI mice evolved enhanced boldness and 85 exploration over a short timescale and in concert with other substantial phenotypic 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.10.292185; this version posted September 10, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 86 changes. This work lays the foundation for identifying the genetic changes responsible for 87 behavioral evolution in organisms that colonize islands. 88 5 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.10.292185; this version posted September 10, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 89 Materials and Methods 90 Mouse Strains and Husbandry 91 Inbred strains of GI mice and mainland mice were used throughout this study. In 92 2009, GI mice were live-caught and shipped to the University of Wisconsin School of 93 Veterinary Medicine Charmany Instructional Facility, where a breeding colony was 94 established [23]. GI mice for this study belonged to a strain maintained for 21-23 95 generations of brother-sister mating. At this stage of inbreeding, we expect most of the 96 genome to be homozygous, allowing us to treat individual mice as replicates of the same 97 genetic background. Mainland mice belonged to the WSB/EiJ inbred strain founded from 98 breeding pairs caught in Maryland (purchased from the Jackson Laboratory, Bar Harbor, 99 ME) and were maintained in the same colony as GI mice for the same time period. F1s 100 were generated by crossing mice from the GI strain and the mainland strain in both 101 maternal directions. All mice were housed in micro-isolator cages with corn cob substrate 102 (1/8th inch; The Andersons Lab Bedding), with ad libitum access to food (Envigo 2020X 103 Teklad Global Diet) and water. Breeders were provided with a higher fat chow (Envigo 104 2019 Teklad Global Diet) and a red mouse igloo (Bio Serv). All cages were provided with 105 nesting material and irradiated sunflower seeds (Envigo). Cage changes occurred every 6- 106 8 days or, in the case of a new litter, 10 days after parturition. The colony was kept in a 107 temperature-controlled room (68-72°F) under a 12-hour light/dark cycle. 108 Mice used for behavioral testing were weaned 20-21 days after parturition and 109 housed with one littermate of the same sex to reduce behavioral effects of within-cage 110 hierarchies [27]. All mice were weighed to the nearest tenth of a gram during cage 111 changeouts and after the last behavioral assay (i.e. weekly from ages 4-10 weeks old +/- 1 6 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.10.292185; this version posted September 10, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 112 day). 113 114 Behavioral Assays 115 All behavioral assays were conducted in a room separate from the main colony.
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