Polygene Control and Trait Dominance in Death-Feigning Syndrome in the Red Flour Beetle Tribolium Castaneum
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bioRxiv preprint doi: https://doi.org/10.1101/2021.05.13.443963; this version posted May 14, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Article title: 2 Polygene control and trait dominance in death-feigning syndrome 3 in the red flour beetle Tribolium castaneum 4 5 Kentarou Matsumura1, Takahisa Miyatake2 6 7 Affiliations: 8 1. Graduate School of Agriculture, Kagawa University, Kagawa, Japan 9 2. Graduate School of Environmental and Life Science, Okayama University, 10 Okayama, Japan 11 12 Running head: 13 Reciprocal crossing for death-feigning 14 15 Corresponding author: 16 Kentarou Matsumura 17 Tell: +81-80-1796-8803 18 E-mail: [email protected] 19 Faculty of Agriculture, Kagawa University 20 2393 Ikenobe, Miki, Kagawa, Japan 761-0795 21 22 23 bioRxiv preprint doi: https://doi.org/10.1101/2021.05.13.443963; this version posted May 14, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 24 Abstract 25 Death-feigning behavior is an anti-predator behavior in a wide range of animal taxa, and 26 it often correlates with the movement (i.e. death-feigning syndrome). In the present 27 study, we performed reciprocal crossing among strains with genetically longer (L strain) 28 and shorter (S strain) duration of death feigning, and investigated related heritable 29 factors in the F1 and F2 populations. We also investigated moving activity which 30 negatively responded to artificial selection for death feigning in T. castaneum. Our 31 results showed that death feigning occurred more frequently and for shorter periods in 32 the F1 population. In the F2 population, death feigning and movement showed 33 continuous segregation. The distribution of each trait value in the F2 generation was 34 different from the distribution of trait values in the parental generation, and no 35 individuals transgressing the distribution of trait values in the parental generation 36 emerged in the F2 generation. Chi-square analysis of the observed death feigning and 37 movement of F1 and F2 progenies rejected the hypothesis of mono-major gene 38 inheritance. These results suggest that death-feigning syndrome is controlled in a 39 polygenic manner. Our study indicated that reciprocal crossing experiments are useful in 40 assessing the quantitative inheritance of behavioral traits. 41 42 Keywords: 43 Quantitative trait, death feigning, moving activity, artificial selection, Tribolium 44 castaneum 45 bioRxiv preprint doi: https://doi.org/10.1101/2021.05.13.443963; this version posted May 14, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 46 1. Introduction 47 Animal behaviors are often studied as quantitative traits (Boake 1994; Lynch and Walsh 48 1998). Reciprocal crossing experiment is a suitable method for studying quantitative 49 traits. When the frequency distribution at F2 generation after reciprocal crossing 50 between strains with different trait values does not overlap from the parental generation, 51 it is suggested that the trait is controlled in a polygenic manner. Each gene determines 52 properties that are governed by quantitative inheritance (Falconer and Mackay 1996). If 53 the distribution of the F2 population overlaps that of the parent distribution, the trait is 54 likely controlled by a major gene. Furthermore, observation of the distribution at the F1 55 generation after reciprocal crossing among different strains can estimate which gene is 56 dominant. Therefore, reciprocal crossing can also be used to assess trait dominance that 57 is the phenomenon of one allele of a gene on a chromosome masking or overriding the 58 effect of a different allele of the same gene on the other copy of the chromosome 59 (Falconer and Mackay 1996; Lynch and Walsh 1998). Although the reciprocal crossing 60 method is difficult to reveal the details of the molecular level as RNA-Seq, it is able to 61 investigate the gene inheritance by confirming the actual expression of the traits. 62 Some previous studies have conducted reciprocal crossing experiment. For 63 example, in cowpea Vigna unguiculata (Walp), reciprocal crossing experiments revealed 64 resistance to Callosobruchus maculatus (Fabricius) may be inherited as a major gene 65 effects (Redden et al. 1983). In lesser grain borer Rhyzopertha dominica (Fabricius), 66 reciprocal crossing with susceptible and resistant lines to phosphine suggested that 67 resistance is no single gene inheritance (Collins et al. 2002). In Drosophila 68 melanogaster (Meigen), larval foraging behavior (rover or sitter phenotypes) is 69 controlled by a foraging gene, and reciprocal crossing between rover and sitter lines bioRxiv preprint doi: https://doi.org/10.1101/2021.05.13.443963; this version posted May 14, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 70 showed that complete dominance of the rover phenotype in larval behavior (de Belle 71 and Sokolowski 1987). Furthermore, reciprocal crossing of strains with genetically 72 longer or shorter development periods has been conducted in the melon fly Zeugodacus 73 cucurbitae (Coquillett); the results showed that shorter developmental period was 74 dominant in the F1 population, and that segregation of developmental period in F2 did 75 not overlap that of the parent distribution (Miyatake 1997). These results suggest that 76 the developmental period of Z. cucurbitae is controlled in a polygenic manner 77 (Miyatake 1997). In another study of Z. cucurbitae, circadian rhythm, which is 78 genetically correlated with developmental period, was also investigated through 79 reciprocal crossing; segregation of the F2 population was found to overlap that of the 80 parent generation, suggesting that circadian rhythm is controlled by a major gene in this 81 species (Shimizu et al. 1997). These studies contributed to the discovery of a clock gene 82 in Z. cucurbitae (Fuchikawa et al. 2010). Therefore, although the reciprocal crossing 83 test is a classic and simple experimental method, it is an important experimental method 84 for investigating quantitative traits. 85 Death feigning, also known as thanatosis or tonic immobility, is observed in a wide 86 range of animal taxa and is considered to be an adaptive anti-predator behavior (e.g. 87 Edmunds 1974; Miyatake et al. 2009; Humphreys and Ruxton, 2018; Ruxton et al. 88 2018). A previous study conducted artificial selection for duration of death feigning in 89 the red flour beetle Tribolium castaneum (Herbst) and established strains with 90 genetically higher frequency and longer duration of death feigning (i.e., L-strains) and 91 strains with genetically lower frequency and shorter duration of death feigning (i.e., 92 S-strains) (Miyatake et al. 2004). Following encounters with a jumping spider Hasarius 93 adansoni (Audouin) as a model predator, L-strain beetles had higher survival rates than bioRxiv preprint doi: https://doi.org/10.1101/2021.05.13.443963; this version posted May 14, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 94 S-strain beetles (Miyatake et al. 2004). These findings suggest that death-feigning 95 behavior is an adaptive anti-predator strategy with a genetic basis. Furthermore, L-strain 96 beetles also show less movement than S-strain beetles, suggesting a negative genetic 97 correlation between the duration of death feigning and movement in T. castaneum; this 98 relationship has been termed the death-feigning syndrome (Miyatake et al. 2008; 99 Matsumura et al. 2017). Other studies have suggested that this genetic behavioral 100 correlation may be controlled by dopamine in T. castaneum (Miyatake et al. 2008; Nishi 101 et al. 2010). The death-feigning syndrome has also been observed in T. confusum 102 (Jaquelin Du Val) (Nakayama et al. 2012; Matsumura et al. 2017) and the adzuki bean 103 beetle Callosobruchus chinensis (Linnaeus) (Ohno and Miyatake 2007; Nakayama and 104 Miyatake 2010). 105 Although L and S strains of death feigning behavior have been established in T. 106 castaneum by artificial selection (Miyatake et al. 2004; Miyatake et al. 2008), no study 107 has conducted reciprocal crossing experiments to investigate both frequency and 108 duration of death feigning and movement in F1 and F2 populations. Therefore, in the 109 present study, we conducted reciprocal crossing of L and S strains to investigate 110 segregated phenotypes of death-feigning duration and frequency, as well as movement 111 in F1 and F2 T. castaneum populations. The current study provides more data on 112 inheritance of death-feigning behavior, for example, how many genes control this 113 behavior, and how this behavior inherits through generations in field? 114 115 2. Materials and Methods 116 2.1. Insects and artificial selection for death-feigning duration 117 In this study, we used previously established L- and S-strain T. castaneum beetles that bioRxiv preprint doi: https://doi.org/10.1101/2021.05.13.443963; this version posted May 14, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.