簡易檢索 / 詳目顯示

研究生: 陳伯飛
Chen, Bo-Fei
論文名稱: 尼泊爾埋葬蟲的社會演化與生殖適應的基因體研究
Social evolution and genomic investigation of breeding adaptation in burying beetles
指導教授: 沈聖峰
Shen, Sheng-Feng
蔡怡陞
Tsai, IshengJason
學位類別: 博士
Doctor
系所名稱: 生命科學系
Department of Life Science
論文出版年: 2019
畢業學年度: 107
語文別: 英文
論文頁數: 137
中文關鍵詞: social evolutioncooperative behaviorcomparative genomicsseasonal breedercontinuous breederburying beetle
英文關鍵詞: social evolution, cooperative behavior, comparative genomics, seasonal breeder, continuous breeder, burying beetle
DOI URL: http://doi.org/10.6345/NTNU201900769
論文種類: 學術論文
相關次數: 點閱:121下載:3
分享至:
查詢本校圖書館目錄 查詢臺灣博碩士論文知識加值系統 勘誤回報
  • Competition shapes the evolution of life and determines how organisms live now. Carcasses are nutritious but unpredictable and transient resources that drive intense competition among scavengers and microbiomes. Burying beetles (Coleoptera: Silphidae: Nicrophorus) are one of the unique scavenging insects which use small vertebrate carcasses as the sole resources to reproduce. To compete against the major interspecific competitor, blowflies, they formed cooperative groups on carcasses. This study used a series of field and laboratory experiments to clarify the mechanism of group formation in burying beetles and found that interspecific competition drove Nicrophorus nepalensis to use a sulfur-containing organic volatile compound, dimethyl disulfide (DMDS) as the cue to indicate interspecific competition and form social groups on carcasses. On the other hand, the interspecific competition also drove N. nepalensis to evolve two breeding types, i.e., continuous breeding (CB) and seasonal breeding (SB), among populations. To understand the transition in the molecular mechanism between two breeding types, I performed the genomic comparison among N. nepalensis and 14 Hexapoda species and the transcriptomic comparisons between two N. nepalensis populations. The results showed the insects of two breeding types had convergent evolution at gene levels, respectively, and N. nepalensis shared breeding-type specific genes with both breeding types. These two studies provide evidence to demonstrate how N. nepalensis adapt to interspecific competition in terms of cooperative behavior and also adjusting breeding seasons. When the pressure of interspecific competition increases, N. nepalensis shifts from intraspecific competition to cooperation to compete with interspecific competitors. Because N. nepalensis has both breeding-type specific gene features in its genome, N. nepalensis can adjust the breeding season to avoid interspecific competitors when the competitive pressure is too high. Differentiation in the length of breeding seasons implies N. nepalensis has local adaptation among populations. In future work, the study would be focused on the molecular evolution among populations using genomic data in order to further understand the local adaptation and its driving forces in N. nepalensis.

    Acknowledgement i Abstract iii Chapter 1 – Introduction 1 Evolution driven by competition 1 Behavioral mechanisms of group formation 2 Genomic and transcriptomic comparisons in breeding regulations 3 References 5 Chapter 2 – A chemically-triggered transition from conflict to cooperation in burying beetles 9 Abstract 9 Introduction 11 Results 13 Group size, social investment and conflict along the environmental gradient 13 Cooperation triggered by interspecific competition 14 A sulfur-containing organic compound as the cue of interspecific competition 15 Dominance hierarchy and body temperature among group members 17 Discussion 20 Materials and methods 22 References 29 Chapter 3 – The genomic and transcriptomic investigations of seasonal and continuous breeding adaptations in burying beetles 46 Abstract 46 Introduction 47 Results 49 Assembly, gene annotation, and genome characterization of the N. nepalensis genome 49 Convergent evolution at gene levels within CB and SB insects 50 N. nepalensis shared genetic features with both breeding types 52 Gene-expression changes between seasonal and continuous breeding N. nepalensis populations 53 Genes and their function correlated with sexual maturation and developmental stages 55 Breeding-type-specific orthologues or PDEGs and circadian clock genes in the regulation of continuous and seasonal breeding 57 Discussion 59 Materials and methods 61 References 67 Chapter 4 – Conclusion 135 References 137

    Chapter 1
    1 Parmenter, R. R. & MacMahon, J. A. Carrion decomposition and nutrient cycling in a semiarid shrub–steppe ecosystem. Ecological Monographs 79, 637-661 (2009).
    2 Carter, D., Yellowlees, D. & Tibbett, M. Cadaver decomposition in terrestrial ecosystems. Naturwissenschaften 94, 12-24 (2007).
    3 Sun, S.-J. et al. Climate-mediated cooperation promotes niche expansion in burying beetles. eLife 3 (2014).
    4 Scott, M. P. The ecology and behavior of burying beetles. Annual Review of Entomology 43, 595-618 (1998).
    5 Sikes, D. S., Madge, R. B. & Trumbo, S. T. Revision of Nicrophorus in part: new species and inferred phylogeny of the nepalensis-group based on evidence from morphology and mitochondrial DNA (Coleoptera : Silphidae : Nicrophorinae). Invertebrate Systematics 20, 305-365 (2006).
    6 Sikes, D. S., Vamosi, S. M., Trumbo, S. T., Ricketts, M. & Venables, C. Molecular systematics and biogeography of Nicrophorus in part—The investigator species group (Coleoptera: Silphidae) using mixture model MCMC. Molecular Phylogenetics and Evolution 48, 646-666 (2008).
    7 Sikes, D. S. & Venables, C. Molecular phylogeny of the burying beetles (Coleoptera: Silphidae: Nicrophorinae). Molecular Phylogenetics and Evolution 69, 552-565 (2013).
    8 Shukla, S. P. et al. Microbiome-assisted carrion preservation aids larval development in a burying beetle. Proceedings of the National Academy of Sciences 115, 11274-11279 (2018).
    9 Prokopy, R. J. & Roitberg, B. D. Joining and avoidance behavior in nonsocial insects. Annual Review of Entomology 46, 631-665 (2001).
    10 Eggert, A.-K. & Müller, J. Joint breeding in female burying beetles. Behavioral Ecology and Sociobiology 31, 237-242 (1992).
    11 Eggert, A.-K. & Sakaluk, S. K. Benefits of communal breeding in burying beetles: a field experiment. Ecological Entomology 25, 262-266 (2000).
    12 Robertson, I. C., Robertson, W. G. & Roitberg, B. D. A model of mutual tolerance and the origin of communal associations between unrelated females. Journal of Insect Behavior 11, 265-286 (1998).
    13 Scott, M. P. Competition with flies promotes communal breeding in the burying beetle, Nicrophorus tomentosus. Behavioral Ecology and Sociobiology 34, 367-373 (1994).
    14 Trumbo, S. T. Monogamy to communal breeding: exploitation of a broad resource base by burying beetles (Nicrophorus). Ecological Entomology 17, 289-298 (1992).
    15 Trumbo, S. T. & Fiore, A. J. Interspecific competition and the evolution of communal breeding in burying beetles. American Midland Naturalist 131, 169-174 (1994).
    16 Trumbo, S. T. & Wilson, D. S. Brood discrimination, nest mate discrimination, and determinants of social behavior in facultatively quasisocial beetles (Nicrophorus spp.). Behavioral Ecology 4, 332-339 (1993).
    17 Emlen, S. T. The evolution of helping. I. An ecological constraints model. The American Naturalist 119, 29-39 (1982).
    18 Emlen, S. T. Benefits, constrainsts and the evolution of the family. Trends in Ecology & Evolution 9, 282-285 (1994).
    19 Jetz, W. & Rubenstein, D. R. Environmental uncertainty and the global biogeography of cooperative breeding in birds. Current Biology 21, 72-78 (2011).
    20 Rubenstein, D. R. & Lovette, I. J. Temporal environmental variability drives the evolution of cooperative breeding in birds. Current Biology 17, 1414-1419 (2007).
    21 Bauer, R. T. Continuous reproduction and episodic recruitment in nine shrimp species inhabiting a tropical seagrass meadow. Journal of Experimental Marine Biology and Ecology 127, 175-187 (1989).
    22 Bronson, F. H. Mammalian reproduction: an ecological perspective. Biology of Reproduction 32, 1-26 (1985).
    23 Dawson, A., King, V. M., Bentley, G. E. & Ball, G. F. Photoperiodic control of seasonality in birds. Journal of Biological Rhythms 16, 365-380 (2001).
    24 Goodbody, I. Continuous breeding in three species of tropical ascidian. Proceedings of the Zoological Society of London 136, 403-409 (1961).
    25 Goodbody, I. Continuous breeding in populations of two tropical crustaceans, Mysidium Columbiae (Zimmer) and Emerita Portoricensis Schmidt. Ecology 46, 195-197 (1965).
    26 Mavrikakis, P. G., Economopoulos, A. P. & Carey, J. R. Continuous winter reproduction and growth of the Mediterranean fruit fly (Diptera: Tephritidae) in Heraklion, Crete, Southern Greece. Environmental Entomology 29, 1180-1187, 1188 (2000).
    27 Somoano, A., Ventura, J. & Miñarro, M. Continuous breeding of fossorial water voles in northwestern Spain: potential impact on apple orchards. Folia Zoologica 66, 29-36, 28 (2017).
    28 Verhulst, S. & Nilsson, J.-Å. The timing of birds' breeding seasons: a review of experiments that manipulated timing of breeding. Philosophical Transactions of the Royal Society B: Biological Sciences 363, 399-410 (2008).
    29 Visser, M. E., Caro, S. P., Oers, K. v., Schaper, S. V. & Helm, B. Phenology, seasonal timing and circannual rhythms: towards a unified framework. Philosophical Transactions of the Royal Society B: Biological Sciences 365, 3113-3127 (2010).

    Chapter 2
    1 Bourke AFG (2011) Principles of Social Evolution (Oxford University Press, Oxford).
    2 Bolnick DI, et al. (2010) Ecological release from interspecific competition leads to decoupled changes in population and individual niche width. Proc. R. Soc. Lond., Ser. B: Biol. Sci. 277(1689):1789-1797.
    3 Pianka ER (1974) Niche overlap and diffuse competition. Proc. Natl. Acad. Sci. USA 71(5):2141-2145.
    4 Hardin G (1960) The competitive exclusion principle. Science 131(3409):1292-1297.
    5 Pukowski E (1933) Ökologische Untersuchungen an Necrophorus F. Zeitschrift fur Morphologie und Ökologie der Tiere 27:518 – 586.
    6 Scott MP (1998) The ecology and behavior of burying beetles. Annu. Rev. Entomol. 43(1):595-618.
    7 Rozen D, Engelmoer D, & Smiseth P (2008) Antimicrobial strategies in burying beetles breeding on carrion. Proc. Natl. Acad. Sci. USA 105(46):17890-17895.
    8 Cotter SC & Kilner RM (2010) Sexual division of antibacterial resource defence in breeding burying beetles, Nicrophorus vespilloides. J. Anim. Ecol. 79(1):35-43.
    9 Sun S-J, et al. (2014) Climate-mediated cooperation promotes niche expansion in burying beetles. eLife 3:e02440.
    10 Liu M, et al. (in review) Ecological transitions in grouping benefits explain the paradox of environmental quality and sociality.
    11 Kalinova B, Podskalska H, Růžička J, & Hoskovec M (2009) Irresistible bouquet of death—how are burying beetles (Coleoptera: Silphidae: Nicrophorus) attracted by carcasses. Naturwissenschaften 96(8):889-899.
    12 Podskalská H, Růžička J, Hoskovec M, & Šálek M (2009) Use of infochemicals to attract carrion beetles into pitfall traps. Entomol. Exp. Appl. 132(1):59-64.
    13 Dicke M & Sabelis MW (1988) Infochemical terminology: based on cost-benefit analysis rather than origin of compounds? Funct. Ecol. 2:131-139.
    14 Korb J & Foster KR (2010) Ecological competition favours cooperation in termite societies. Ecol. Lett. 13(6):754-760.
    15 De Jaegher K & Hoyer B (2016) By-product mutualism and the ambiguous effects of harsher environments – A game-theoretic model. J. Theor. Biol. 393:82-97.
    16 Feeney WE, et al. (2013) Brood Parasitism and the Evolution of Cooperative Breeding in Birds. Science 342(6165):1506-1508.
    17 Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol. Evol. 11(2):92-98.
    18 Tomkins JL & Hazel W (2007) The status of the conditional evolutionarily stable strategy. Trends Ecol. Evol. 22(10):522-528.
    19 Celiker H & Gore J (2012) Competition between species can stabilize public-goods cooperation within a species. Mol. Syst. Biol. 8(1).
    20 Mitri S, Xavier JB, & Foster KR (2011) Social evolution in multispecies biofilms. Proc. Natl. Acad. Sci. USA 108(Supplement 2):10839-10846.
    21 Keller L & Nonacs P (1993) The role of queen pheromones in social insects: queen control or queen signal? Anim. Behav. 45(4):787-794.
    22 Vander Meer RK, Breed MD, Winston M, & Espelie K (1998) Pheromone Communication in Social Insects (Westview Press, Boulder, CO).
    23 Trible W, et al. (2017) Orco mutagenesis causes loss of antennal lobe glomeruli and impaired social behavior in ants. Cell 170(4):727-735. e710.
    24 Yan H, et al. (2017) An Engineered orco Mutation Produces Aberrant Social Behavior and Defective Neural Development in Ants. Cell 170(4):736-747.e739.
    25 Hofmann HA, et al. (2014) An evolutionary framework for studying mechanisms of social behavior. Trends Ecol. Evol. 29(10):581-589.
    26 Vas G & Vékey K (2004) Solid-phase microextraction: a powerful sample preparation tool prior to mass spectrometric analysis. J. Mass Spectrom. 39(3):233-254.
    27 Shizuka D & McDonald DB (2012) A social network perspective on measurements of dominance hierarchies. Anim. Behav. 83(4): 925-934
    28 Nakagawa S & Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4(2): 133-142.

    Chapter 3
    1 Bronson, F. H. Mammalian reproduction: an ecological perspective. Biology of Reproduction 32, 1-26 (1985).
    2 Verhulst, S. & Nilsson, J.-Å. The timing of birds' breeding seasons: a review of experiments that manipulated timing of breeding. Philosophical Transactions of the Royal Society B: Biological Sciences 363, 399-410 (2008).
    3 Visser, M. E., Caro, S. P., Oers, K. v., Schaper, S. V. & Helm, B. Phenology, seasonal timing and circannual rhythms: towards a unified framework. Philosophical Transactions of the Royal Society B: Biological Sciences 365, 3113-3127 (2010).
    4 Dawson, A., King, V. M., Bentley, G. E. & Ball, G. F. Photoperiodic control of seasonality in birds. Journal of Biological Rhythms 16, 365-380 (2001).
    5 Immelmann, K. in Avian biology Vol. 1 341-389 (1971).
    6 Miller, B. H. et al. Circadian Clock mutation disrupts estrous cyclicity and maintenance of pregnancy. Current Biology 14, 1367-1373 (2004).
    7 Rastogi, S. C. Essentials of animal physiology. (New Age International (P) Limited, Publishers, 2007).
    8 Simonneaux, V. & Bahougne, T. A multi-oscillatory circadian system times female reproduction. Frontiers in Endocrinology 6 (2015).
    9 Tsai, H.-Y. et al. Locally-adapted phenology determines population vulnerability to climate change. (in review).
    10 Scott, M. P. The ecology and behavior of burying beetles. Annual Review of Entomology 43, 595-618 (1998).
    11 Dudchenko, O. et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science 356, 92-95 (2017).
    12 Smith, S. G. Chromosome numbers of Coleoptera. Heredity 7, 31-48 (1953).
    13 Vorontsov, N. N., Yadav, J. S., Lyapunova, E. A., Korablev, V. P. & Yanina, I. Y. Comparative karyology of seven species of staphylinoid beetles (Polyphaga: Coleoptera). Genetica 63, 153-159 (1984).
    14 Holt, R. A. et al. The genome sequence of the malaria mosquito Anopheles gambiae. Science 298, 129-149 (2002).
    15 Keeling, C. I. et al. Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest. Genome Biology 14, 1-20 (2013).
    16 Holt, C. & Yandell, M. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinformatics 12, 491 (2011).
    17 Falda, M. et al. Argot2: a large scale function prediction tool relying on semantic similarity of weighted Gene Ontology terms. BMC Bioinformatics 13, S14 (2012).
    18 Brown, S. J., Henry, J. K., Black Iv, W. C. & Denell, R. E. Molecular genetic manipulation of the red flour beetle: genome organization and cloning of a ribosomal protein gene. Insect Biochemistry 20, 185-193 (1990).
    19 Manning, J. E., Schmid, C. W. & Davidson, N. Interspersion of repetitive and nonrepetitive DNA sequences in the Drosophila melanogaster genome. Cell 4, 141-155 (1975).
    20 Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15, 550 (2014).
    21 Langfelder, P. & Horvath, S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9, 559 (2008).
    22 Kehle, J. et al. dMi-2, a Hunchback-interacting protein that functions in Polycomb repression. Science 282, 1897-1900 (1998).
    23 Kowanda, M. et al. Loss of function of the Drosophila Ninein-related centrosomal protein Bsg25D causes mitotic defects and impairs embryonic development. Biology Open 5, 1040-1051 (2016).
    24 Lai, C. K. et al. Functional characterization of putative cilia genes by high-content analysis. Molecular Biology of the Cell 22, 1104-1119 (2011).
    25 Skonier, J. et al. βig-h3: a transforming growth factor-β-responsive gene encoding a secreted protein that inhibits cell attachment in vitro and suppresses the growth of CHO cells in nude mice. DNA and Cell Biology 13, 571-584 (1994).
    26 Heppner, C. et al. The tumor suppressor protein menin interacts with NF-κB proteins and inhibits NF-κB-mediated transactivation. Oncogene 20, 4917-4925 (2001).
    27 Lin, J. et al. Kielin/chordin-like protein, a novel enhancer of BMP signaling, attenuates renal fibrotic disease. Nature Medicine 11, 387-393 (2005).
    28 Soderbom, F., Anjard, C., Iranfar, N., Fuller, D. & Loomis, W. F. An adenylyl cyclase that functions during late development of Dictyostelium. Development 126, 5463-5471 (1999).
    29 Cui, X. A., Zhang, H. & Palazzo, A. F. p180 Promotes the Ribosome-Independent Localization of a Subset of mRNA to the Endoplasmic Reticulum. PLoS. Biol. 10, e1001336 (2012).
    30 Miazek, A. & Malissen, B. Two genes, three messengers: hybrid transcript between a gene expressed at specific stages of T-cell and sperm maturation and an unrelated adjacent gene. Immunogenetics 54, 681-692 (2003).
    31 Guglielmi, B. & Werner, M. The yeast homolog of human PinX1 is involved in rRNA and small nucleolar RNA maturation, not in telomere elongation inhibition. Journal of Biological Chemistry 277, 35712-35719 (2002).
    32 Haritos, V. S., Horne, I., Damcevski, K., Glover, K. & Gibb, N. Unexpected functional diversity in the fatty acid desaturases of the flour beetle Tribolium castaneum and identification of key residues determining activity. Insect Biochemistry and Molecular Biology 51, 62-70 (2014).
    33 Tonon, T. et al. Identification of a fatty acid Δ11-desaturase from the microalga Thalassiosira pseudonana. FEBS Letters 563, 28-34 (2004).
    34 Watanabe, N., Wachi, S. & Fujita, T. Identification and characterization of BCL-3-binding protein: implications for transcription and DNA repair or recombination. Journal of Biological Chemistry 278, 26102-26110 (2003).
    35 Tang, S. J., Meulemans, D., Vazquez, L., Colaco, N. & Schuman, E. A role for a rat homolog of staufen in the transport of RNA to neuronal dendrites. Neuron 32, 463-475 (2001).
    36 Blattes, R. et al. Displacement of D1, HP1 and topoisomerase II from satellite heterochromatin by a specific polyamide. The EMBO Journal 25, 2397-2408 (2006).
    37 Grenningloh, G., Jay Rehm, E. & Goodman, C. S. Genetic analysis of growth cone guidance in Drosophila: Fasciclin II functions as a neuronal recognition molecule. Cell 67, 45-57 (1991).
    38 Chen, Y. et al. A SNX10/V-ATPase pathway regulates ciliogenesis in vitro and in vivo. Cell Research 22, 333 (2011).
    39 Nishigori, H. et al. Identification and characterization of the gene encoding a second proteolipid subunit of human vacuolar H+-ATPase (ATP6F). Genomics 50, 222-228 (1998).
    40 Edwin Chan, H. Y., Harris, S. J. & O'Kane, C. J. Identification and characterization of kraken, a gene encoding a putative hydrolytic enzyme in Drosophila melanogaster. Gene 222, 195-201 (1998).
    41 Rauschenberger, K. et al. A non-enzymatic function of 17β-hydroxysteroid dehydrogenase type 10 is required for mitochondrial integrity and cell survival. EMBO Molecular Medicine 2, 51-62 (2010).
    42 Shafqat, N. et al. Expanded substrate screenings of human and Drosophila type 10 17β-hydroxysteroid dehydrogenases (HSDs) reveal multiple specificities in bile acid and steroid hormone metabolism: characterization of multifunctional 3α/7α/7β/17β/20β/21-HSD. Biochemical Journal 376, 49 (2003).
    43 Emms, D. & Kelly, S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biology 16, 157 (2015).
    44 Conesa, A. et al. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674-3676 (2005).
    45 Fretwell, S. D. Populations in a seasonal environment. (Princeton University Press, 1972).
    46 Tauber, M. J., Tauber, C. A. & Masaki, S. Seasonal adaptations of insects. (Oxford University Press on Demand, 1986).
    47 Nakayama, T. et al. Seasonal regulation of the lncRNA LDAIR modulates self-protective behaviours during the breeding season. Nature Ecology & Evolution 3, 845-852 (2019).
    48 Simon, S., Rühl, M., de Montaigu, A., Wötzel, S. & Coupland, G. Evolution of CONSTANS regulation and function after gene duplication produced a photoperiodic flowering switch in the Brassicaceae. Molecular Biology and Evolution 32, 2284-2301 (2015).
    49 Sikes, D. S., Madge, R. B. & Trumbo, S. T. Revision of Nicrophorus in part: new species and inferred phylogeny of the nepalensis-group based on evidence from morphology and mitochondrial DNA (Coleoptera : Silphidae : Nicrophorinae). Invertebrate Systematics 20, 305-365 (2006).
    50 Vurture, G. W. et al. GenomeScope: fast reference-free genome profiling from short reads. Bioinformatics 33, 2202-2204 (2017).
    51 Kajitani, R. et al. Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads. Genome Research 24, 1384-1395 (2014).
    52 Wences, A. & Schatz, M. Metassembler: merging and optimizing de novo genome assemblies. Genome Biology 16, 207 (2015).
    53 Durand, N. C. et al. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Systems 3, 95-98 (2016).
    54 Durand, N. C. et al. Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Systems 3, 99-101 (2016).
    55 Walker, B. J. et al. Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement. PLoS ONE 9, e112963 (2014).
    56 Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics (2015).
    57 Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094-3100 (2018).
    58 Picard Toolkit. (Broad Institute, 2019).
    59 RepeatModeler Open-1.0 (2015).
    60 RepeatMasker Open-4.0 (2015).
    61 Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics (2012).
    62 Pertea, M. et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature Biotechnology 33, 290-295 (2015).
    63 Song, L., Sabunciyan, S. & Florea, L. CLASS2: accurate and efficient splice variant annotation from RNA-seq reads. Nucleic Acids Research 44, e98-e98 (2016).
    64 Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29, 644-652 (2011).
    65 Wu, T. D. & Watanabe, C. K. GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21, 1859-1875 (2005).
    66 Venturini, L., Caim, S., Kaithakottil, G. G., Mapleson, D. L. & Swarbreck, D. Leveraging multiple transcriptome assembly methods for improved gene structure annotation. GigaScience 7 (2018).
    67 Stanke, M., Tzvetkova, A. & Morgenstern, B. AUGUSTUS at EGASP: using EST, protein and genomic alignments for improved gene prediction in the human genome. Genome Biology 7, S11 (2006).
    68 Korf, I. Gene finding in novel genomes. BMC Bioinformatics 5, 59 (2004).
    69 Hoff, K. J., Lange, S., Lomsadze, A., Borodovsky, M. & Stanke, M. BRAKER1: unsupervised RNA-seq-based genome annotation with GeneMark-ET and AUGUSTUS. Bioinformatics 32, 767-769 (2015).
    70 Bandow, C., Karau, N. & Römbke, J. Interactive effects of pyrimethanil, soil moisture and temperature on Folsomia candida and Sinella curviseta (Collembola). Applied Soil Ecology 81, 22-29 (2014).
    71 Xu, J. et al. Evaluation of growth and reproduction as indicators of soil metal toxicity to the Collembolan, Sinella curviseta. Insect Science 16, 57-63 (2009).
    72 Benoit, J. B., Lopez-Martinez, G., Teets, N. M., Phillips, S. A. & Denlinger, D. L. Responses of the bed bug, Cimex lectularius, to temperature extremes and dehydration: levels of tolerance, rapid cold hardening and expression of heat shock proteins. Medical and Veterinary Entomology 23, 418-425 (2009).
    73 Feldlaufer, M., Harlan, H. & Miller, D. 118-130 (2014).
    74 Montes, C., Cuadrillero, C. & Vilella, D. Maintenance of a laboratory colony of Cimex lectularius (Hemiptera: Cimicidae) using an artificial feeding technique. Journal of Medical Entomology 39, 675-679 (2002).
    75 Polanco, A. M., Brewster, C. C. & Miller, D. M. Population growth potential of the bed bug, Cimex lectularius L.: a life table analysis. Insects 2, 173-185 (2011).
    76 Nielsen, A. L., Chen, S. & Fleischer, S. J. Coupling developmental physiology, photoperiod, and temperature to model phenology and dynamics of an invasive Heteropteran, Halyomorpha halys. Frontiers in Physiology 7 (2016).
    77 Nielsen, A. L. et al. Phenology of brown marmorated stink bug described using female reproductive development. Ecology and Evolution 7, 6680-6690 (2017).
    78 Gadot, M., Burns, E. & Schal, C. Juvenile hormone biosynthesis and oocyte development in adult female Blattella germanica: effects of grouping and mating. Archives of Insect Biochemistry and Physiology 11, 189-200 (1989).
    79 Srinivasan, R., Jambulingam, P., Subramanian, S. & Kalyanasundaram, M. Laboratory evaluation of fipronil against Periplaneta americana & Blattella germanica. Indian Journal of Medical Research 122, 57 (2005).
    80 Uzsák, A. & Schal, C. Sensory cues involved in social facilitation of reproduction in Blattella germanica females. PLOS ONE 8, e55678 (2013).
    81 Zhu, D.-H., Liu, S.-D. & Zhao, L.-Q. Effects of photoperiod and temperature on nymphal development and adult reproduction in the forest-dwelling cockroach, Blattella germanica. Acta Ecologica Sinica 26, 2125-2132 (2006).
    82 de la Filia, A. G., Andrewes, S., Clark, J. M. & Ross, L. The unusual reproductive system of head and body lice (Pediculus humanus). Medical and Veterinary Entomology 32, 226-234 (2018).
    83 Johnston, J. S., Yoon, K. S., Strycharz, J. P., Pittendrigh, B. R. & Clark, J. M. Body lice and head lice (Anoplura: Pediculidae) have the smallest genomes of any hemimetabolous insect reported to date. Journal of Medical Entomology 44, 1009-1012, 1004 (2007).
    84 McMeniman, C. J. & Barker, S. C. Transmission ratio distortion in the human body louse, Pediculus humanus (Insecta: Phthiraptera). Heredity 96, 63-68 (2006).
    85 Saunders, D. S. & Sutton, D. Circadian rhythms in the insect photoperiodic clock. Nature 221, 559-561 (1969).
    86 Drury, D. W., Whitesell, M. E. & Wade, M. J. The effects of temperature, relative humidity, light, and resource quality on flight initiation in the red flour beetle, Tribolium castaneum. Entomologia Experimentalis et Applicata 158, 269-274 (2016).
    87 Kharel, K., Mason, L. J., Murdock, L. L. & Baributsa, D. Efficacy of hypoxia against Tribolium castaneum (Coleoptera: Tenebrionidae) throughout ontogeny. Journal of Economic Entomology 112, 1463-1468 (2019).
    88 Perez-Mendoza, J., Campbell, J. F. & Throne, J. E. Effect of abiotic factors on initiation of red flour beetle (Coleoptera: Tenebrionidae) flight. Journal of Economic Entomology 107, 469-472 (2014).
    89 Anderson, R. S. Resource partitioning in the carrion beetle (Coleoptera: Silphidae) fauna of southern Ontario: ecological and evolutionary considerations. Canadian Journal of Zoology 60, 1314-1325 (1982).
    90 Beninger, C. W. & Peck, S. B. Temporal and spatial patterns of resource use among Nicrophorus carrion beetles (Coleoptera: Silphidae) in a Sphagnum bog and adjacent forest near Ottawa, Canada. The Canadian Entomologist 124, 79-86 (1992).
    91 Müller, J. K. & Eggert, A.-K. Paternity assurance by “helpful” males: adaptations to sperm competition in burying beetles. Behavioral Ecology and Sociobiology 24, 245-249 (1989).
    92 Otronen, M. The effect of body size on the outcome of fights in burying beetles (Nicrophorus). Annales Zoologici Fennici 25, 191-201 (1988).
    93 Shimada, K. Photoperiodic induction of diapause in normal and allatectomized precocious pupae of Papilio machaon. Journal of Insect Physiology 29, 801-806 (1983).
    94 Shimizu, I. & Hasegawa, K. Photoperiodic induction of diapause in the silkworm, Bombyx mori: location of the photoreceptor using a chemiluminescent paint. Physiological Entomology 13, 81-88 (1988).
    95 Almirón, W. R. & Brewer, M. E. Winter biology of Culex pipiens quinquefasciatus say, (Diptera: Culicidae) from Córdoba, Argentina. Memórias do Instituto Oswaldo Cruz 91, 649-654 (1996).
    96 Kang, D. S., Tomas, R. & Sim, C. The effects of temperature and precipitation on Culex quinquefasciatus (Diptera: Culicidae) abundance: a case study in the Greater Waco City, Texas. Vol. 02 (2017).
    97 Ukubuiwe, A. C. et al. Effects of varying photoperiodic regimens on critical biological fitness traits of Culex quinquefasciatus (Diptera: Culicidae) mosquito vector. International Journal of Insect Science (2018).
    98 Doctor, J. Musca domestica, <https://animaldiversity.org/accounts/Musca_domestica/> (2013).
    99 Saunders, D. S., Henrich, V. C. & Gilbert, L. I. Induction of diapause in Drosophila melanogaster: photoperiodic regulation and the impact of arrhythmic clock mutations on time measurement. Proceedings of the National Academy of Sciences 86, 3748-3752 (1989).
    100 Katoh, K., Misawa, K., Kuma, K.-i. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059-3066 (2002).
    101 Stamatakis, A. RAxML Version 8: A tool for Phylogenetic Analysis and Post-Analysis of Large Phylogenies. Bioinformatic (2014).
    102 Finn, R. D. et al. Pfam: the protein families database. Nucleic Acids Research 42, D222-D230 (2014).
    103 Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923-930 (2013).
    104 Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Research 13, 2498-2504 (2003).
    105 topGO: enrichment analysis for gene ontology. R package version 2.37.0. (2019).

    Chapter 4
    1 Chen, B.-F. et al. A chemically-triggered transition from conflict to cooperation in burying beetles. bioRxiv, 389163 (2018).
    2 Sun, S.-J. et al. Climate-mediated cooperation promotes niche expansion in burying beetles. eLife 3 (2014).

    下載圖示
    QR CODE