in

Tribolium beetles as a model system in evolution and ecology

  • Adamski Z, Bufo SA, Chowański S, Falabella P, Lubawy J, Marciniak P et al. (2019) Beetles as model organisms in physiological, biomedical and environmental studies—a review. Front Physiol 10:319

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Ahmad F, Daglish GJ, Ridley AW, Burrill PR, Walter GH (2013) Short-range resource location by Tribolium castaneum Herbst (Coleoptera: Tenebrionidae) demonstrates a strong preference for fungi associated with cotton seed. J Stored Prod Res 52:21–27

    Article 

    Google Scholar 

  • Ahmad F, Ridley AW, Daglish GJ, Burrill PR, Walter GH (2013) Response of Tribolium castaneum and Rhyzopertha dominica to various resources, near and far from grain storage. J Appl Entomol 137:773–781

    Article 

    Google Scholar 

  • Alabi T, Michaud JP, Arnaud L, Haubruge E (2008) A comparative study of cannibalism and predation in seven species of flour beetle. Ecol Entomol 33:716–726

    Google Scholar 

  • Allee WC (1931) Animal aggregations: a study in general sociology. University of Chicago Press, Chicago

    Google Scholar 

  • Andres A (1931) Catalogue of the Egyptian Tenebrionidae. Bull de la Société R Entomologique d’Egypte 15:74–125

    Google Scholar 

  • Ankeny RA, Leonelli S (2011) What’s so special about model organisms? Stud Hist Philos Sci B Stud Hist Philos Mod Phys 42:313–323

    Google Scholar 

  • Arnaud L, Haubruge E, Gage MJG (2005) The malathion-specific resistance gene confers a sperm competition advantage in Tribolium castaneum. Funct Ecol 19:1032–1039

    Article 

    Google Scholar 

  • Arnaud L, Lognay G, Gaspar C, Haubruge E et al. (2000) Chemical communication in Tribolium castaneum (Coleoptera, Tenebrionidae): knowledge and perspectives. Bulletin OILB/SROP 23:195–209

  • Arnaud L, Lognay G, Verscheure M, Leenaers L, Gaspar C, Haubruge E (2002) Is dimethyldecanal a common aggregation pheromone of Tribolium flour beetles? J Chem Ecol 28:523–532

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Arnold PA, Cassey P, White CR (2016) Maturity matters for movement and metabolic rate: trait dynamics across the early adult life of red flour beetles. Anim Behav 111:181–188

    Article 

    Google Scholar 

  • Arnold PA, Cassey P, White CR (2017) Functional traits in red flour beetles: the dispersal phenotype is associated with leg length but not body size nor metabolic rate. Funct Ecol 31:653–661

    Article 

    Google Scholar 

  • Assie LK, Brostaux Y, Haubruge E (2008) Density-dependent reproductive success in Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). J Stored Prod Res 44:285–289

    Article 

    Google Scholar 

  • Attia FA, Tregenza T (2004) Divergence revealed by population crosses in the red flour beetle Tribolium castaneum. Evol Ecol Res 6:927–935

    Google Scholar 

  • Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK et al. (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Chang Biol 8:1–16

    Article 

    Google Scholar 

  • Barr MM (2003) Super models. Physiol Genom 13:15–24

    CAS 
    Article 

    Google Scholar 

  • Bell AE, Burris MJ (1973) Simultaneous selection for two correlated traits in Tribolium. Genet Res 21:29–46

    Article 

    Google Scholar 

  • Bolker J (2012) Model organisms: there’s more to life than rats and flies. Nature 491:31–33

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev Camb Philos Soc 80:205–225

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Boyer JF (1976) The effects of prior environments on Tribolium castaneum. J Anim Ecol 45:865–874

    Article 

    Google Scholar 

  • Brown SJ, Denell RE, Beeman RW (2003) Beetling around the genome. Genet Res 82:155–161

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Brown SJ, Shippy TD, Miller S, Bolognesi R, Beeman RW, Lorenzen MD et al. (2009) The red flour beetle, Tribolium castaneum (Coleoptera): a model for studies of development and pest biology Cold Spring Harb Protoc 2009:db.emo126

    Article 
    CAS 

    Google Scholar 

  • Calabrese EJ (2013) Low doses of radiation can enhance insect lifespans. Biogerontology 14:365–381

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Campbell JF, Hagstrum DW (2002) Patch exploitation by Tribolium castaneum: movement patterns, distribution, and oviposition. J Stored Prod Res 38:55–68

    Article 

    Google Scholar 

  • Campbell JF, Runnion C (2003) Patch exploitation by female red flour beetles, Tribolium castaneum. J Insect Sci 3:20

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Chapman RN (1918) The confused flour beetle (Tribolum confusum, Duval)

  • Chapman RN (1928) The quantitative analysis of environmental factors. Ecology 9:111–122

    Article 

    Google Scholar 

  • Chittenden FH (1896) Some insects injurious to stored grain. U.S. Department of Agriculture, Washington

  • Costantino RF, Desharnais RA (1991) Population dynamics and the tribolium model: genetics and demography. Springer Science & Business Media, New York

  • Costantino RF, Desharnais RA, Cushing JM, Dennis B, Henson SM, King AA (2005) Nonlinear stochastic population dynamics: the flour beetle Tribolium as an effective tool of discovery. Adv Ecol Res 37:101–141

    Article 

    Google Scholar 

  • Coyne JA, Barton NH, Turelli M (2000) Is Wright’s shifting balance process important in evolution? Evolution 54:306–317

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Costantino RF, Cushing JM, Dennis B, Desharnais RA (1995) Experimentally induced transitions in the dynamic behaviour of insect populations. Nature 375:227–230

  • Costantino RF, Desharnais RA, Cushing JM, Dennis B (1997) Chaotic Dynamics in an Insect Population. Science 275:389–391

  • Craig DM, Mertz DB (1994) Inbreeding effects on competition in Tribolium. Res Popul Ecol 36:251–254

    Article 

    Google Scholar 

  • Cushing JM, Costantino RF, Dennis B, Desharnais R, Henson SM (2002) Chaos in Ecology: Experimental Nonlinear Dynamics. Academic Press, San Diego CA

  • Daglish GJ, Ridley AW, Reid R, Walter GH (2017) Testing the consistency of spatio-temporal patterns of flight activity in the stored grain beetles Tribolium castaneum (Herbst) and Rhyzopertha dominica (F.). J Stored Prod Res 72:68–74

    Article 

    Google Scholar 

  • Davey WP (1917) The effect of X-rays on the length of life of Tribolium confusum. J Exp Zool 22:573–592

    Article 

    Google Scholar 

  • Dawson PS (1977) Life history strategy and evolutionary history of Tribolium flour beetles. Evolution 31:226–229

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Demont M, Grazer VM, Michalczyk Ł, Millard AL (2014) Experimental removal of sexual selection reveals adaptations to polyandry in both sexes. Evol Biol 41:62–70

  • Demuth JP, Wade MJ (2007) Population differentiation in the beetle Tribolium castaneum. II. Haldane’s rule and incipient speciation. Evolution 61:694–699

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Denell R (2008) Establishment of Tribolium as a genetic model system and its early contributions to evo-devo. Genetics 180:1779–1786

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Desharnais RA, Costantino RF, Cushing JM, Henson SM, Dennis B (2001) Chaos and population control of insect outbreaks. Ecol Lett 4:229–235

  • Desharnais RA, Reuman DC, Costantino RF, Cohen JE (2018) Temporal scale of environmental correlations affects ecological synchrony. Ecol Lett 21:1800–1811

  • Dönitz J, Schmitt-Engel C, Grossmann D, Gerischer L, Tech M, Schoppmeier M et al. (2015) iBeetle-Base: a database for RNAi phenotypes in the red flour beetle Tribolium castaneum. Nucleic Acids Res 43:D720–5

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • Droge-Young EM, Belote JM, Perez GS, Pitnick S (2016) Resolving mechanisms of short-term competitive fertilization success in the red flour beetle. J Insect Physiol 93-94:1–10

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Drury DW, Jideonwo VN, Ehmke RC, Wade MJ (2011) An unusual barrier to gene flow: perpetually immature larvae from inter-population crosses in the flour beetle, Tribolium castaneum. J Evol Biol 24:2678–2686

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Drury DW, Siniard AL, Wade MJ (2009) Genetic differentiation among wild populations of Tribolium castaneum estimated using microsatellite markers. J Hered 100:732–741

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Drury DW, Whitesell ME, Wade MJ (2016) The effects of temperature, relative humidity, light, and resource quality on flight initiation in the red flour beetle, Tribolium castaneum. Entomol Exp Appl 158:269–274

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Ducoff HS (1986) Radiation and longevity enhancement in Tribolium. In: Collatz K-G, Sohal RS (eds) Insect aging: strategies and mechanisms. Springer Berlin Heidelberg, Berlin, Heidelberg, p 73–89

    Google Scholar 

  • Dunbrack RL, Coffin C, Howe R (1995) The cost of males and the paradox of sex – experimental investigation of the short-term competitive advantages of evoltion in sexual populations. Proc R Soc B-Biol Sci 262:45–49

    Article 

    Google Scholar 

  • Eggert H, Diddens-de Buhr MF, Kurtz J (2015) A temperature shock can lead to trans-generational immune priming in the red flour beetle Tribolium castaneum. Ecol Evol 5:1318–1326

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • El-Aziz SEA (2011) Control strategies of stored product pests. J Entomol 8:101–122

    Article 

    Google Scholar 

  • El-Desouky TA, Elbadawy SS, Hussain HBH, Hassan NA (2018) Impact of insect densities Tribolium castaneum on the benzoquinone secretions and aflatoxins levels in wheat flour during storage periods. Open Biotechnol J 12:104–111

    CAS 
    Article 

    Google Scholar 

  • Ellen ED, Peeters K, Verhoeven M, Gols R, Harvey JA, Wade MJ et al. (2016) Direct and indirect genetic effects in life-history traits of flour beetles (Tribolium castaneum): Indirect genetic effects in Tribolium. Evolution 70:207–217

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Endriss SB, Vahsen ML, Bitume EV, Grey Monroe J, Turner KG, Norton AP et al. (2019) The importance of growing up: juvenile environment influences dispersal of individuals and their neighbours. Ecol Lett 22:45–55

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Fedina TY, Lewis SM (2008) An integrative view of sexual selection in Tribolium flour beetles. Biol Rev Camb Philos Soc 83:151–171

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Flinn PW, Campbell JF (2012) Effects of flour conditioning on cannibalism of T. castaneum eggs and pupae. Environ Entomol 41:1501–1504

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Franklin AD, Siewerdt F (2011) Post-bottleneck inbreeding accumulation reduces fitness and adaptive potential in populations of Tribolium castaneum under environmental stress. Genomics and Quantitative. Genetics 2:19–30

    Google Scholar 

  • Godwin JL, Lumley AJ, Michalczyk L, Martin OY, Gage MJG (2020) Mating patterns influence vulnerability to the extinction vortex. Global Change Biology 26:4226–4239

  • Godwin JL, Spurgin LG, Michalczyk Ł, Martin OY, Lumley AJ, Chapman T et al. (2018) Lineages evolved under stronger sexual selection show superior ability to invade conspecific competitor populations. Evol Lett 2:511–523

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Godwin JL, Vasudeva R, Michalczyk Ł, Martin OY, Lumley AJ, Chapman T et al. (2017) Experimental evolution reveals that sperm competition intensity selects for longer, more costly sperm. Evol Lett 1:102–113

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Gokhale CS, Traulsen A, Joop G (2017) Social dilemma in the external immune system of the red flour beetle? It is a matter of time. Ecol Evol 7:6758–6765

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Good NE (1936) The flour beetles of the genus Tribolium. ageconsearch.umn.edu

  • Grazer VM, Demont M, Michalczyk Ł, MJG Gage, Martin OY (2014) Environmental quality alters female costs and benefits of evolving under enforced monogamy. BMC Evol Biol 14:21

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Gurdasani K, Rafter MA, Daglish GJ, Walter GH (2018) Characterising the variables associated with Tribolium castaneum adults that initiate flight in laboratory tests – generating predictions for the field. J Stored Prod Res 79:123–131

    Article 

    Google Scholar 

  • Gurdasani K, Rafter MA, Daglish GJ, Walter GH (2019) The dispersal flight of Tribolium castaneum—a field test of laboratory generated predictions. J Stored Prod Res 83:25–33

    Article 

    Google Scholar 

  • Hagstrum DW, Smittle BJ (1980) Age- and sex-specific tunneling rates of adult Tribolium castaneum. Ann Entomol Soc Am 73:11–13

    Article 

    Google Scholar 

  • Halle S, Nowizki A, Scharf I (2015) The consequences of parental age for development, body mass and resistance to stress in the red flour beetle. Biol J Linn Soc Lond 115:305–314

    Article 

    Google Scholar 

  • Halliday WD, Blouin-Demers G (2017) A test of the thermal coadaptation hypothesis with ultimate measures of fitness in flour beetles. J Therm Biol 69:206–212

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Halliday WD, Blouin-Demers G (2018) Can temperature modify the strength of density-dependent habitat selection in ectotherms? A test with red flour beetles. J Zool 304:159–168

    Article 

    Google Scholar 

  • Halliday WD, Bourque C, Blouin-Demers G (2019) Food quality influences density-dependent fitness, but not always density-dependent habitat selection, in red flour beetles (Coleoptera: Tenebrionidae). Can Entomol 151:728–737

    Article 

    Google Scholar 

  • Halliday WD, Slevan-Tremblay I, Blouin-Demers G (2019) Do female red flour beetles assess both current and future competition during oviposition? J Insect Behav 32:181–187

    Article 

    Google Scholar 

  • Hartmann S, Frigg R (2005) Scientific models. In: Sarkar Sahotra (ed.) The philosophy of science: an encyclopedia, Vol. 2, Routledge, London

  • Haubruge E, Arnaud L (2001) Fitness consequences of malathion-specific resistance in red flour beetle (Coleoptera: Tenebrionidae) and selection for resistance in the absence of malathion. J Econ Entomol 94:552–557

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Hedges SB (2002) The origin and evolution of model organisms. Nat Rev Genet 3:838–849

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Henson SM, Costantino RF, Cushing JM, Desharnais RA, Dennis B, King AA (2001) Lattice effects observed in chaotic dynamics of experimental populations. Science 294:602–605

  • Herndon N, Shelton J, Gerischer L, Ioannidis P, Ninova M, Dönitz J et al. (2020) Enhanced genome assembly and a new official gene set for Tribolium castaneum. BMC Genom 21:47

    CAS 
    Article 

    Google Scholar 

  • Holman L, Jacomb F (2017) The effects of stress and sex on selection, genetic covariance, and the evolutionary response. J Evol Biol 30:1898–1909

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Hoste R (1968) The Use of Tribolium beetles for class practical work in genetics. J Biol Educ 2:365–372

    Article 

    Google Scholar 

  • Hufbauer RA, Szűcs M, Kasyon E, Youngberg C, Koontz MJ, Richards C et al. (2015) Three types of rescue can avert extinction in a changing environment. Proc Natl Acad Sci USA 112:10557–10562

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Irwin KK, Carter PA (2014) Artificial selection on larval growth curves in Tribolium: correlated responses and constraints. J Evol Biol 27:2069–2079

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Izadi H, Mohammadzadeh M, Mehrabian M (2019) Cold tolerance of the Tribolium castaneum (Coleoptera: Tenebrionidae), under different thermal regimes: impact of cold acclimation. J Econ Entomol 112:1983–1988

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Jacomb F, Marsh J, Holman L (2016) Sexual selection expedites the evolution of pesticide resistance. Evolution 70:2746–2751

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Janus MC (1989) Phenotypic diversity of Tribolium confusum pupae in heterogeneous environments. Entomol Exp Appl 50:281–286

    Article 

    Google Scholar 

  • Jasieński M, Korzeniak U, Łomnicki A (1988) Ecology of kin and nonkin larval interactions in Tribolium beetles. Behav Ecol Sociobiol 22:277–284

    Article 

    Google Scholar 

  • Katz AJ, Enfield FD (1977) Response to selection for increased pupa weight in Tribolium castaneum as related to population structure*. Genet Res 30:237–246

    Article 

    Google Scholar 

  • Kennedy BK (2008) The genetics of ageing: insight from genome-wide approaches in invertebrate model organisms. J Intern Med 263:142–152

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Kerstes NAG, Martin OY (2014) Insect host-parasite coevolution in the light of experimental evolution. Insect Sci 21:401–414

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Khan I, Prakash A, Agashe D (2016) Divergent immune priming responses across flour beetle life stages and populations. Ecol Evol 6:7847–7855

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Khan I, Prakash A, Issar S, Umarani M, Sasidharan R, Masagalli JN et al. (2018) Female density-dependent chemical warfare underlies fitness effects of group sex ratio in flour beetles. Am Nat 191:306–317

    Article 

    Google Scholar 

  • Kim HS, Murphy T, Xia J, Caragea D, Park Y, Beeman RW et al. (2010) BeetleBase in 2010: revisions to provide comprehensive genomic information for Tribolium castaneum. Nucleic Acids Res 38:D437–42

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • King AA, Costantino RF, Cushing JM, Henson SM, Desharnais RA, Dennis B (2004) Anatomy of a chaotic attractor: Subtle model-predicted patterns revealed in population data. P Natl Acad Sci USA 101:408–413

  • King CE, Dawson PS (1972) Population biology and the Tribolium model. Evol Biol 1972:5

    Google Scholar 

  • Koontz MJ, Oldfather MF, Melbourne BA, Hufbauer RA (2018) Parsing propagule pressure: Number, not size, of introductions drives colonization success in a novel environment. Ecol Evol 8:8043–8054

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Lavie B, Ritte U (1980) Correlated effects of the response to conditioned medium in the flour beetle, Tribolium castaneum. Res Popul Ecol 21:228–232

    Article 

    Google Scholar 

  • Leslie PH (1962) A stochastic model for two competing species of Tribolium and its application to some experimental data. Biometrika 49:1–25

    Article 

    Google Scholar 

  • Lewis SM, Tigreros N, Fedina T, Ming QL (2012) Genetic and nutritional effects on male traits and reproductive performance in Tribolium flour beetles. J Evol Biol 25:438–451

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Lewontin RC, Hubby JL (1966) A molecular approach to the study of genic heterozygosity in natural populations. II. Amount of variation and degree of heterozygosity in natural populations of Drosophila pseudoobscura. Genetics 54:595–609

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • López-Fanjul C, Jódar B (1977) The genetic properties of egg laying of virgin females of Tribolium castaneum. Heredity 39:251–258

    Article 

    Google Scholar 

  • Lumley AJ, Michalczyk Ł, Kitson JJN, Spurgin LG, Morrison CA, Godwin JL et al. (2015) Sexual selection protects against extinction. Nature 522:470–473

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Martin CM, Kruse KC, Switzer PV (2015) Social experience affects same-sex pairing behavior in male red flour beetles (Tribolium castaneum Herbst). J Insect Behav 28:268–279

    Article 

    Google Scholar 

  • Matsumura K, Archer CR, Hosken DJ, Miyatake T (2019) Artificial selection on walking distance suggests a mobility-sperm competitiveness trade-off. Behav Ecol

  • Matsumura K, Miyatake T (2015) Differences in attack avoidance and mating success between strains artificially selected for dispersal distance in Tribolium castaneum. PLoS ONE 10:e0127042

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Matsumura K, Miyatake T (2019) Lines selected for different durations of tonic immobility have different leg lengths in the red flour beetle Tribolium castaneum. Behaviour 157:17–31

    Article 

    Google Scholar 

  • Mayes PA, Englert DC (1984) Interstrain differences for larval dispersal and egg cannibalism in the flour beetle, Tribolium castaneum. Can J Genet Cytol 26:420–424

    Article 

    Google Scholar 

  • McCauley DE, Wade MJ (1981) The populational effects of inbreeding in Tribolium. Heredity 46:59–67

    Article 

    Google Scholar 

  • McCulloch GA, Mohankumar S, Subramanian S, Rajan TS, Rahul C, Surendran R et al. (2019) Contrasting patterns of phylogeographic structuring in two key beetle pests of stored grain in India and Australia. J Pest Sci 92:1249–1259

    Article 

    Google Scholar 

  • McNemee R, Marshall J (2018) Temperature stressed males are less attractive to female red flour beetles. In: Proceeding of 3rd Entomology Undergraduate Research Poster Symposium. Kansas State University, Department of Entomology, Manhattan, KS

  • Melbourne BA, Hastings A (2009) Highly variable spread rates in replicated biological invasions: fundamental limits to predictability. Science 325:1536–1539

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Mertz DB (1972) The Tribolium model and the mathematics of population growth. Annu Rev Ecol Syst 3:51–78

    Article 

    Google Scholar 

  • Mertz DB (1975) Senescent decline in flour beetle strains selected for early adult fitness. Physiol Zool 48:1–23

    Article 

    Google Scholar 

  • Mertz DB, Cawthon DA, Park T (1976) An experimental analysis of competitive indeterminacy in Tribolium. Proc Natl Acad Sci USA 73:1368–1372

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Mertz DB, Robertson JR (1970) Some developmental consequences of handling, egg-eating, and population density for flour beetle larvae. Ecology 51:989–998

    Article 

    Google Scholar 

  • Michalczyk Ł, Millard AL, Martin OY, Lumley AJ, Emerson BC, Chapman T et al. (2011) Inbreeding promotes female promiscuity. Science 333:1739–1742

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Ming Q-L, Lewis SM (2010) Pheromone production by male Tribolium castaneum (Coleoptera: Tenebrionidae) is influenced by diet quality. J Econ Entomol 103:1915–1919

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Miyatake T, Katayama K, Takeda Y, Nakashima A, Sugita A, Mizumoto M (2004) Is death-feigning adaptive? Heritable variation in fitness difference of death-feigning behaviour. Proc R Soc B-Biol Sci 271:2293–2296

  • Müller B, Grossniklaus U (2010) Model organisms–a historical perspective. J Proteom 73:2054–2063

    Article 
    CAS 

    Google Scholar 

  • Naylor AF (1965) Dispersal responses of female flour beetles, Tribolium confusum, to presence of larvae. Ecology 46:341–343

    Article 

    Google Scholar 

  • Orozco F, Bell AE (1974) A genetic study of egg laying of Tribolium in optimal and stress environments. Can J Genet Cytol 16:49–60

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Pai A, Bernasconi G (2008) Polyandry and female control: the red flour beetle Tribolium castaneum as a case study. J Exp Zool B Mol Dev Evol 310:148–159

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Pai A, Yan G (2002) Female mate choice in relation to heterozygosity in Tribolium castaneum: female mate choice and heterozygosity. J Evol Biol 15:1076–1082

    Article 

    Google Scholar 

  • Park T (1932) Studies in population physiology: the relation of numbers to initial population growth in the flour beetle Tribolium confusum Duval. Ecology 13:172–181

    Article 

    Google Scholar 

  • Park T (1934) Observations on the general biology of the flour beetle, Tribolium confusum. Q Rev Biol 9:36–54

    Article 

    Google Scholar 

  • Park T (1962) Beetles, competition, and populations. Science 138:1369–1375

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Park T, Leslie PH, Mertz DB (1964) Genetic strains and competition in populations of Tribolium. Physiol Zool 37:97–162

    Article 

    Google Scholar 

  • Park T, Lloyd M (1955) Natural selection and the outcome of competition. Am Nat 89:235–240

    Article 

    Google Scholar 

  • Park T, Mertz DB, Grodzinski W, Prus T (1965) Cannibalistic predation in populations of flour beetles. Physiol Zool 38:289–321

    Article 

    Google Scholar 

  • Park T, Miller EV, Lutherman CZ (1939) Studies in population physiology. IX. The effect of imago population density on the duration of the larval and pupal stages of Tribolium confusum Duval. Ecology 20:365–373

    Article 

    Google Scholar 

  • Perkin LC, Oppert B (2019) Gene expression in Tribolium castaneum life stages: Identifying a species-specific target for pest control applications. PeerJ 7:e6946

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Pray LA (1997) The effect of inbreeding on population-level genetic correlations in the red flour beetle Tribolium castaneum. Evolution 51:614–619

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Pray LA, Goodnight CJ (1995) Genetic variation in inbreeding depression in the red flour beetle Tribolium castaneum. Evolution 49:176–188

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Pray LA, Goodnight CJ, Stevens L, Schwartz JM, Yan G (1996) The effect of population size on effective population size: an empirical study in the red flour beetle Tribolium castaneum. Genet Res 68:151–155

    Article 

    Google Scholar 

  • Pray LA, Schwartz JM, Goodnight CJ, Stevens L (1994) Environmental dependency of inbreeding depression: implications for conservation biology. Conserv Biol 8:562–568

    Article 

    Google Scholar 

  • Prendeville HR, Stevens L (2002) Microbe inhibition by Tribolium flour beetles varies with beetle species, strain, sex, and microbe group. J Chem Ecol 28:1183–1190

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Prokop ZM, Hlebowicz K, Gaczorek TS, Antol WM, Martin OY, Gage MJG et al. (2019) No evidence for short-term purging benefits of sexual selection in inbred red flour beetle populations. J Zool 307:178–185

    Article 

    Google Scholar 

  • Prus T (1963) Search for methods to investigate mobility in Tribolium. Ecology 44:801–803

    Article 

    Google Scholar 

  • Rafter MA, Muralitharan V, Chandrasekaran S, Mohankumar S, Daglish GJ, Loganathan M et al. (2019) Behaviour in the presence of resource excess—flight of Tribolium castaneum around heavily-infested grain storage facilities. J Pest Sci 92:1227–1238

    Article 

    Google Scholar 

  • Rajan TS, Muralitharan V, Daglish GJ, Mohankumar S, Rafter MA, Chandrasekaran S et al. (2018) Flight of three major insect pests of stored grain in the monsoonal tropics of India, by latitude, season and habitat. J Stored Prod Res 76:43–50

    Article 

    Google Scholar 

  • Reuman DC, Costantino RF, Desharnais RA, Cohen JE (2008) Colour of environmental noise affects the nonlinear dynamics of cycling, stage-structured populations. Ecol Lett 11:820–830

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Rich SS, Bell AE, Wilson SP (1979) Genetic drift in small populations of Tribolium. Evolution 33:579–584

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Ritte U, Agur Z (1977) Variability for dispersal behavior in a wild population of Tribolium castaneum. Tribolium Inf Bull 20:122–131

  • Robinson T, Johnson NA, Wade MJ (1994) Postcopulatory, prezygotic isolation: intraspecific and interspecific sperm precedence in Tribolium spp., flour beetles. Heredity 73(Pt 2):155–159

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Sales K, Trent T, Gardner J, Lumley AJ, Vasudeva R (2018) Experimental evolution with an insect model reveals that male homosexual behaviour occurs due to inaccurate mate choice. Anim Behav

  • Sales K, Vasudeva R, Dickinson ME, Godwin JL, Lumley AJ, Michalczyk Ł et al. (2018) Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect. Nat Commun 9:4771

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Sbilordo SH, Gräzer VM (2011) Impacts of starvation on male reproductive success in Tribolium castaneum. Evol Ecol Res 13:347–359

  • Schamber EM, Muir WM (2001) Wright’s shifting balance theory of evolution in artificial breeding programmes: empirical testing using the model organism Tribolium castaneum. J Anim Breed Genet-Z Fur Tierz Und Zuchtungsbiologie 118:181–188

    Article 

    Google Scholar 

  • Scharf I, Galkin N, Halle S (2015) Disentangling the consequences of growth temperature and adult acclimation temperature on starvation and thermal tolerance in the red flour beetle. Evol Biol 42:54–62

    Article 

    Google Scholar 

  • Schlager G (1960) Sperm Precedence in the Fertilization of Eggs in Tribolium castaneum. Ann Entomol Soc Am 53:557–560

    Article 

    Google Scholar 

  • Schlötterer C, Kofler R, Versace E, Tobler R, Franssen SU (2015) Combining experimental evolution with next-generation sequencing: a powerful tool to study adaptation from standing genetic variation. Heredity 114:431–440

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Shen J-F, Cheng C, Ming Q-L (2016) Study on reproductive isolation between Tribolium castaneum and T. confusum. J Environ Entomol 3:508–513

  • Shostak AW, Van Buuren KG, Cook R (2015) Response of flour beetles to multiple stressors of parasitic (Hymenolepis diminuta), environmental (Diatomaceous Earth), and host (Reproduction) origin. J Parasitol 101:405–417

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Sinha RN (1966) Development and mortality of Tribolium castaneum and T. confusum (Coleoptera: Tenebrionidae) on seed-borne fungi. Ann Entomol Soc Am 59:192–201

    Article 

    Google Scholar 

  • Sokal RR, Sonleitner FJ (1968) The ecology of selection in hybrid populations of Tribolium castaneum. Ecol Monogr 38:345–379

    Article 

    Google Scholar 

  • Sokoloff A (1977) The biology of Tribolium with special emphasis on genetic aspects. Volume 3. Clarendon Press, Oxford

  • Sokoloff A, Franklin IR, Overton LF, Ho FK (1966) Comparative studies with Tribolium (Coleoptera, Tenebrionidae)—I: Productivity of T. castaneum (Herbst) and T. confusum Duv. on several commercially-available diets. J Stored Prod Res 1:295–311

    Article 

    Google Scholar 

  • Soliman MH (1972) Correlated response to natural selection in laboratory populations of Tribolium castaneum. Can J Genet Cytol 15:971–978

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Soliman MH (1987) Ageing and parental age effects in Tribolium (review). Arch Gerontol Geriatr 6:43–60

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Soliman MH, Lints FA (1975) Longevity, growth rate and related traits among strains of Tribolium castaneum. Gerontologia 21:102–116

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Sommer RJ (2009) The future of evo-devo: model systems and evolutionary theory. Nat Rev Genet 10:416–422

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Sonleitner FJ, Gutherie J (1991) Factors affecting oviposition rate in the flour beetle Tribolium castaneum and the origin of the population regulation mechanism. Res Popul Ecol 33:1–11

    Article 

    Google Scholar 

  • South A, Sirot LK, Lewis SM (2011) Identification of predicted seminal fluid proteins in Tribolium castaneum. Insect Mol Biol 20:447–456

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Stephens PA, Sutherland WJ, Freckleton RP (1999) What is the allee effect? Oikos 87:185–190

  • Stevens L (1989) The genetics and evolution of cannibalism in flour beetles (genus Tribolium). Evolution 43:169–179

    PubMed 
    PubMed Central 

    Google Scholar 

  • Stevenson BJ, Cai L, Faucher C, Michie M, Berna A, Ren Y et al. (2017) Walking responses of Tribolium castaneum (Coleoptera: Tenebrionidae) to Its aggregation pheromone and odors of wheat infestations. J Econ Entomol 110:1351–1358

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Stewart GS, Morris MR, Genis AB, Szűcs M, Melbourne BA, Tavener SJ et al. (2017) The power of evolutionary rescue is constrained by genetic load. Evol Appl 10:731–741

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Stork NE, McBroom J, Gely C, Hamilton AJ (2015) New approaches narrow global species estimates for beetles, insects, and terrestrial arthropods. Proc Natl Acad Sci USA 112:7519–7523

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Surtees G (1963) Laboratory studies on dispersion behaviour of adult beetles in grain. III.—Tribolium castaneum (Hbst.) (Coleoptera, Tenebrionidae) and Cryptolestes ferrugineus (Steph.) (Coleoptera, Cucujidae). Bull Entomol Res 54:297–306

    Article 

    Google Scholar 

  • Suzuki T (1980) 4,8-Dimethyldecanal: the aggregation pheromone of the flour beetles, Tribolium castaneum and T. confusum (Coleoptera: Tenebrionidae). Agric Biol Chem 44:2519–2520

    CAS 

    Google Scholar 

  • Szűcs M, Melbourne BA, Tuff T, Hufbauer RA (2014) The roles of demography and genetics in the early stages of colonization. Proc R Soc B-Biol Sci 281:20141073

  • Szűcs M, Melbourne BA, Tuff T, Weiss-Lehman C, Hufbauer RA (2017) Genetic and demographic founder effects have long-term fitness consequences for colonising populations. Ecol Lett 20:436–444

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Szűcs M, Vahsen ML, Melbourne BA, Hoover C, Weiss-Lehman C, Hufbauer RA (2017) Rapid adaptive evolution in novel environments acts as an architect of population range expansion. Proc Natl Acad Sci USA 114:13501–13506

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • Tigreros N, Lewis SM (2011) Direct and correlated responses to artificial selection on sexual size dimorphism in the flour beetle, Tribolium castaneum. J Evol Biol 24:835–842

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Tribolium Genome Sequencing Consortium, Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R et al. (2008) The genome of the model beetle and pest Tribolium castaneum. Nature 452:949–955

    Article 
    CAS 

    Google Scholar 

  • Vahsen ML, Shea K, Hovis CL, Teller BJ, Hufbauer RA (2018) Prior adaptation, diversity, and introduction frequency mediate the positive relationship between propagule pressure and the initial success of founding populations. Biol Invasions 20:2451–2459

    Article 

    Google Scholar 

  • Van Allen BG, Bhavsar P (2014) Natal habitat effects drive density-dependent scaling of dispersal decisions. Oikos 123:699–704

    Article 

    Google Scholar 

  • Van Allen BG, Rudolf VHW (2013) Ghosts of habitats past: environmental carry-over effects drive population dynamics in novel habitat. Am Nat 181:596–608

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Van Allen BG, Rudolf VHW (2015) Habitat-mediated carry-over effects lead to context-dependent outcomes of species interactions. J Anim Ecol 84:1646–1656

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Vasudeva R, Sutter A, Sales K, Dickinson ME, Lumley AJ, Gage MJ (2019) Adaptive thermal plasticity enhances sperm and egg performance in a model insect. Elife 8:e49452

  • Verheggen F, Ryne C, Olsson POC, Arnaud L, Lognay G, Högberg HE et al. (2007) Electrophysiological and behavioral activity of secondary metabolites in the confused flour beetle, Tribolium confusum. J Chem Ecol 33:525–539

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Via S (1999) Cannibalism facilitates the use of a novel environment in the flour beetle, Tribolium castaneum. Heredity 82(Pt 3):267–275

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Wade MJ (1980a) Effective population size: the effects of sex, genotype, and density on the mean and variance of offspring numbers in the flour beetle, Tribolium castaneum. Genet Res 36:1–10

    Article 

    Google Scholar 

  • Wade MJ (1980b) An experimental study of kin selection. Evolution 34:844–855

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Wade MJ, Beeman RW (1994) The population dynamics of maternal-effect selfish genes. Genetics 138:1309–1314

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Wade MJ, Chang NW, Mcnaughton M (1995) Incipient speciation in the flour beetle, Tribolium confusum – premating isolation between natural populations. Heredity 75:453–459

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Wade MJ, Goodnight CJ (1998) Perspective: the theories of Fisher and Wright in the context of metapopulations: when nature does many small experiments. Evolution 52:1537–1553

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Wade MJ, Johnson NA (1994) Reproductive isolation between two species of flour beetles, Tribolium castaneum and T. freemani: variation within and among geographical populations of T. castaneum. Heredity 72(Pt 2):155–162

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Wade MJ, Johnson NA, Jones R, Siguel V, McNaughton M (1997) Genetic variation segregating in natural populations of Tribolium castaneum affecting traits observed in hybrids with T. freemani. Genetics 147:1235–1247

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Wade MJ, Shuster SM, Stevens L (1996) Inbreeding: its effect on response to selection for pupal weight and the heritable variance in fitness in the flour beetle, Tribolium castaneum. Evolution 50:723–733

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Weiss-Lehman C, Tittes S, Kane NC, Hufbauer RA, Melbourne BA (2019) Stochastic processes drive rapid genomic divergence during experimental range expansions. Proc R Soc B-Biol Sci 286:20190231

  • Wexler Y, Scharf I (2017) Distinct effects of two separately applied stressors on behavior in the red flour beetle. Behav Process 145:86–92

    Article 

    Google Scholar 

  • Wexler Y, Subach A, Pruitt JN, Scharf I (2016) Behavioral repeatability of flour beetles before and after metamorphosis and throughout aging. Behav Ecol Sociobiol 70:745–753

    Article 

    Google Scholar 

  • Wexler Y, Wertheimer K-O, Subach A, Pruitt JN, Scharf I (2017) Mating alters the link between movement activity and pattern in the red flour beetle: the effects of mating on behaviour. Physiol Entomol 42:299–306

    Article 

    Google Scholar 

  • Williams GC (1975) Sex and evolution. Princeton University Press, Princeton NJ

  • Winther RG, Giordano R, Edge MD, Nielsen R (2015) The mind, the lab, and the field: three kinds of populations in scientific practice. Stud Hist Philos Biol Biomed Sci 52:12–21

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Wong N, Lee C-Y (2011) Relationship between population growth of the red flour beetle Tribolium castaneum and protein and carbohydrate content in flour and starch. J Econ Entomol 104:2087–2094

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Wright S (1932) The roles of mutation, inbreeding, crossbreeding, and selection in evolution. na

  • Wright S, Dobzhansky T (1946) Genetics of natural populations; experimental reproduction of some of the changes caused by natural selection in certain populations of Drosophila pseudoobscura. Genetics 31:125–156

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Yamada Y (1974) Tribolium as a biological model in quantitative genetics. 1st World Congress on Genetics Applied to Livestock Production, Proc 1:439–450

  • Yamauchi H, Harada M, Miyanoshita A (2018) Polymorphism observed in mitochondrial genes of red flour beetle, Tribolium castaneum (Coleoptera: Tenebrionidae) of different origin in laboratory cultures. Biosci Biotechnol Biochem 82:229–231

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Yan G, Stevens L, Goodnight CJ, Schall JJ (1998) Effects of a tapeworm parasite on the competition of Tribolium beetles. Ecology 79:1093–1103

    Article 

    Google Scholar 

  • Yezerski A, Gilmor TP, Stevens L (2004) Genetic analysis of benzoquinone production in Tribolium confusum. J Chem Ecol 30:1035–1044

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Young AM (1970) Predation and abundance in populations of flour beetles. Ecology 51:602–619

    Article 

    Google Scholar 

  • Ziegler JR (1972) Maintenance and regulation of unconfined populations of Tribolium, the flour beetle. University of Chicago, Chicago

  • Ziegler JR (1976) Evolution of the migration response: emigration by Tribolium and the influence of age. Evolution 30:579–592

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • Ziegler JR (1977) Dispersal and reproduction in Tribolium: the influence of food level. J Insect Physiol 23:955–960

    Article 

    Google Scholar 

  • Ziegler JR (1978) Dispersal and reproduction in Tribolium: the influence of initial density. Environ Entomol 7:149–156

    Article 

    Google Scholar 

  • Zirkle DF, Dawson PS, Lavie B (1988) An experimental analysis of the genetic relationships among life-history traits and emigration behavior in Tribolium castaneum. Oikos 53:391–397

    Article 

    Google Scholar 

  • Zromska-Rudzka H (1966) Abundance and emigrations of Tribolium in a laboratory model. Ekol Polska, Seria A 14: 491–518


  • Source: Ecology - nature.com

    Old-growth forest carbon sinks overestimated

    MIT engineers make filters from tree branches to purify drinking water