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Niche explosion

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Abstract

The following syndrome of features occurs in several groups of phytophagous insects: (1) wingless females, (2) dispersal by larvae, (3) woody hosts, (4) extreme polyphagy, (5) high abundance, resulting in status as economic pests, (6) invasiveness, and (7) obligate parthenogenesis in some populations. If extreme polyphagy is defined as feeding on 20 or more families of hostplants, this syndrome is found convergently in several species of bagworm moths, tussock moths, root weevils, and 5 families of scale insects. We hypothesize that extreme polyphagy in these taxa results from “niche explosion”, a positive feedback loop connecting large population size to broad host range. The niche explosion has a demographic component (sometimes called the “amplification effect” in studies of pathogens) as well as a population-genetic component, due mainly to the increased effectiveness of natural selection in larger populations. The frequent origins of parthenogenesis in extreme polyphages are, in our interpretation, a consequence of this increased effectiveness of natural selection and consequent reduced importance of sexuality. The niche explosion hypothesis makes detailed predictions about the comparative genomics and population genetics of extreme polyphages and related specialists. It has a number of potentially important implications, including an explanation for the lack of observed trade-offs between generalists and specialists, a re-interpretation of the ecological correlates of parthenogenesis, and a general expectation that Malthusian population explosions may be amplified by Darwinian effects.

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References

  • Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EGJ, Deleury E et al (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol 26:909–915

    Article  PubMed  CAS  Google Scholar 

  • Agosta SJ, Klemens JA (2009) Resource specialization in a phytophagous insect: no evidence for genetically based performance trade-offs across hosts in the field or laboratory. J Evol Biol 22:907–912

    Article  PubMed  CAS  Google Scholar 

  • Alstad DN, Edmunds GF (1989) Haploid and diploid survival differences demonstrate selection in scale insect demes. Evol Ecol 3:253–263

    Article  Google Scholar 

  • Baker HG (1965) Characteristics and modes of origin of weeds. Genetics of colonizing species. Academic Press, New York, pp 147–172

    Google Scholar 

  • Barbosa P, Krischik V, Lance D (1989) Life-history traits of forest-inhabiting flightless Lepidoptera. Am Midl Nat 122:262–274

    Article  Google Scholar 

  • Bell G (1982) The masterpiece of nature. University of California Press, Berkeley

    Google Scholar 

  • Ben Dov Y, German V (2003) A systematic catalogue of the Diaspididae (armoured scale insects) of the world, subfamilies Aspidiotinae, Comstockiellinae and Odonaspidinae. Intercept, Andover

    Google Scholar 

  • Ben-Dov Y (2009) ScaleNet catalogues for Coccidae, Diaspididae (subfamily Aspidiotinae), Kerriidae, and Pseudococcidae. November 2009. http://www.sel.barc.usda.gov/scalenet/scalenet.htm

  • Ben-Dov Y, Miller DR, Gibson GAP (2010) ScaleNet classification. Accessed 23 Jan 2010. http://www.sel.barc.usda.gov/scalenet/classif.htm

  • Berenbaum MR, Feeny PF (2008) Chemical mediation of host-plant specialization: the papilionid paradigm. Specialization, speciation and radiation: the evolutionary biology of herbivorous insects. University of California Press, Berkeley, pp 3–19

    Google Scholar 

  • Bierzychudek P (1985) Patterns in plant parthenogenesis. Experientia 41:1255–1264

    Article  Google Scholar 

  • Bjornstad ON, Robinet C, Liebhold AM (2010) Geographic variation in North American gypsy moth cycles: subharmonics, generalist predators, and spatial coupling. Ecology 91:106–118

    Article  PubMed  Google Scholar 

  • Blackman RL, Eastop VF (1994) Aphids on the world’s trees: an identification and information guide. CAB International, Wallingford

    Google Scholar 

  • Blackman RL, Eastop VF (2000) Aphids on the world’s crops: an identification and information guide, 2nd edn. Wiley, Chichester

    Google Scholar 

  • Blackman RL, Eastop VF (2006a) Aphids on the world’s herbaceous plants and shrubs. Volume 1: host lists and keys. Wiley, Chichester

    Google Scholar 

  • Blackman RL, Eastop VF (2006b) Aphids on the world’s herbaceous plants and shrubs. Volume 2: the aphids. Wiley, Chichester

    Google Scholar 

  • Burt A (2000) Perspective: sex, recombination, and the efficacy of selection—was Weismann right? Evolution 54:337–351

    PubMed  CAS  Google Scholar 

  • Chadwick CE (1965) A review of Fuller’s rose weevil (Pantomorus cervinus (Boh.))(Col., Curculionidae). J Entomol Soc Aust (New South Wales) 2:10–20

    Google Scholar 

  • Charlesworth B (1990) Optimization models, quantitative genetics, and mutation. Evolution 44:520–538

    Article  Google Scholar 

  • Childers CC, French JV, Rodrigues JCV (2003) Brevipalpus californicus, B-obovatus, B-phoenicis, and B-lewisi (Acari: Tenuipalpidae): a review of their biology, feeding injury and economic importance. Exp Appl Acarol 30:5–28

    Article  PubMed  Google Scholar 

  • Clark AG (1987) Senescence and the genetic-correlation hang-up. Am Nat 129:932–940

    Article  Google Scholar 

  • Colles A, Liow LH, Prinzing A (2009) Are specialists at risk under environmental change? Neoecological, paleoecological and phylogenetic approaches. Ecol Lett 12:849–863

    Article  PubMed  Google Scholar 

  • Crespi B (2004) Vicious circles: positive feedback in major evolutionary and ecological transitions. Trends Ecol Evol 19:628–633

    Article  Google Scholar 

  • Dobson A (2004) Population dynamics of pathogens with multiple host species. Am Nat 164:S64–S78

    Article  PubMed  Google Scholar 

  • Egas M, Dieckmann U, Sabelis MW (2004) Evolution restricts the coexistence of specialists and generalists: the role of trade-off structure. Am Nat 163:518–531

    Article  PubMed  Google Scholar 

  • Feyereisen R (1999) Insect P450 enzymes. Annu Rev Entomol 44:507–533

    Article  PubMed  CAS  Google Scholar 

  • Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, Oxford

    Google Scholar 

  • Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233

    Article  Google Scholar 

  • Gabriel W, Lynch M, Bürger R (1993) Muller’s ratchet and mutational meltdowns. Evolution 47:1744–1757

    Article  Google Scholar 

  • Glesener RR, Tilman D (1978) Sexuality and the components of environmental uncertainty: clues from geographic parthenogenesis in terrestrial animals. Am Nat 112:659–673

    Article  Google Scholar 

  • Hamilton WD (1967) Extraordinary sex ratios. Science 156:477–488

    Article  PubMed  CAS  Google Scholar 

  • Hamilton WD (1980) Sex versus non-sex versus parasite. Oikos 35:282–290

    Article  Google Scholar 

  • Hamilton WD, May RM (1977) Dispersal in stable habitats. Nature 269:578–581

    Article  Google Scholar 

  • Hamilton WD, Axelrod R, Tanese R (1990) Sexual reproduction as an adaptation to resist parasites (a review). Proc Natl Acad Sci USA 87:3566–3573

    Article  PubMed  CAS  Google Scholar 

  • Hanks LM, Denno RF (1994) Local adaptation in the armored scale insect Pseudaulacaspis pentagona (Homoptera: Diaspididae). Ecology 75:2301–2310

    Article  Google Scholar 

  • Hanks LM, Denno RF (1998) Dispersal and adaptive deme formation in sedentary coccoid insects. Genetic structure and local adaptation in natural insect populations. Chapman and Hall, New York, pp 239–262

    Google Scholar 

  • Hellgren O, Pérez-Tris J, Bensch S (2009) A jack-of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology 90:2840–2849

    Article  PubMed  Google Scholar 

  • Hoffmann AA, Reynolds KT, Nash MA, Weeks AR (2008) A high incidence of parthenogenesis in agricultural pests. Proc R Soc Lond B 275:2473–2481

    Article  Google Scholar 

  • Holman J (2009) Host plant catalog of aphids: Palearctic region. Springer, Dordrecht

    Book  Google Scholar 

  • Holt RD (2009) Bringing the Hutchinsonian niche into the 21st century: ecological and evolutionary perspectives. Proc Natl Acad Sci USA 106:19659–19665

    Article  PubMed  CAS  Google Scholar 

  • Holterman M, Karssen G, van den Elsen S, van Megen H, Bakker J, Helder J (2009) Small subunit rDNA-based phylogeny of the Tylenchida sheds light on relationships among some high-impact plant-parasitic nematodes and the evolution of plant feeding. Phytopathology 99:227–235

    Article  PubMed  CAS  Google Scholar 

  • Hopkin SP (1997) Biology of the springtails (Insecta: Collembola). Oxford University Press, Oxford

    Google Scholar 

  • Jaenike J (1990) Host specialization in phytophagous insects. Annu Rev Ecol Syst 21:243–273

    Article  Google Scholar 

  • Jaenike J, Selander RK (1979) Evolution and ecology of parthenogenesis in earthworms. Am Zool 19:729–737

    Google Scholar 

  • Janz N, Nylin S (2008) The oscillation hypothesis of host-plant range and speciation. Specialization, speciation and radiation: the evolutionary biology of herbivorous insects. University of California Press, Berkeley, pp 203–215

    Google Scholar 

  • Janz N, Nylin S, Wahlberg N (2006) Diversity begets diversity: host expansions and the diversification of plant-feeding insects. BMC Evol Biol 6:4

    Article  PubMed  Google Scholar 

  • Kawecki TJ, Barton NH, Fry JD (1997) Mutational collapse of fitness in marginal habitats and the evolution of ecological specialisation. J Evol Biol 10:407–429

    Article  Google Scholar 

  • Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecol Lett 9:485–498

    Article  PubMed  CAS  Google Scholar 

  • Kirk WDJ (1997) Feeding. Thrips as crop pests. CAB International, Wallingford, pp 119–174

    Google Scholar 

  • Kirkpatrick M (1997) Evolution of a species’ range. Am Nat 150:1–23

    Article  PubMed  CAS  Google Scholar 

  • Kondrashov AS (1988) Deleterious mutations and the evolution of sexual reproduction. Nature 336:435–440

    Article  PubMed  CAS  Google Scholar 

  • Kondrashov AS (1993) Classification of hypotheses on the advantage of amphimixis. J Hered 84:372–387

    PubMed  CAS  Google Scholar 

  • Lanteri AA, Normark BB (1995) Parthenogenesis in the tribe Naupactini (Coleoptera: Curculionidae). Ann Entomol Soc Am 88:722–731

    Google Scholar 

  • Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189

    Article  Google Scholar 

  • Lynch M (1984) Destabilizing hybridization, general-purpose genotypes and geographical parthenogenesis. Q Rev Biol 59:257–290

    Article  Google Scholar 

  • Lynch M (2007) The origins of genome architecture. Sinauer, Sunderland

    Google Scholar 

  • Malthus TR (1798) An essay on the principle of population. J. Johnson, London

    Google Scholar 

  • Mattos VM, Feres RJF (2009) Morphological pattern and life cycle of Eutetranychus banksi (Acari: Tetranychidae) from different localities and hosts. Zoologia 26:427–442

    Google Scholar 

  • Maynard Smith J (1978) The evolution of sex. Cambridge University Press, Cambridge

    Google Scholar 

  • Miller DR, Gimpel ME (2009) ScaleNet catalogues for Diaspididae (subfamily Diaspidinae). November 2009. http://www.sel.barc.usda.gov/scalenet/scalenet.htm

  • Miller DR, Miller GL, Hodges GS, Davidson JA (2005) Introduced scale insects (Hemiptera: Coccoidea) of the United States and their impact on US agriculture. Proc Entomol Soc Wash 107:123–158

    Google Scholar 

  • Mitter C, Farrell B, Wiegmann B (1988) The phylogenetic study of adaptive zones: has phytophagy promoted insect diversification? Am Nat 132:107–128

    Article  Google Scholar 

  • Morris MG (1997) Broad-nosed weevils. Coleoptera: Curculionidae (Entiminae). Royal Entomological Society, London

    Google Scholar 

  • Mound LA (1997) Biological diversity. Thrips as crop pests. CAB International, Wallingford, pp 197–215

    Google Scholar 

  • Mound LA, Teulon DAJ (1995) Thysanoptera as phytophagous opportunists. Thrips biology and management. Plenum, New York

    Google Scholar 

  • Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 1:2–9

    Google Scholar 

  • Normark BB (1994) Phylogeny and evolution of parthenogenesis in the Aramigus tessellatus complex (Coleoptera: Curculionidae). Ph.D. Cornell University, Ithaca

    Google Scholar 

  • Normark BB (1996) Phylogeny and evolution of parthenogenetic weevils of the Aramigus tessellatus species complex (Coleoptera: Curculionidae: Naupactini): evidence from mitochondrial DNA sequences. Evolution 50:734–745

    Article  CAS  Google Scholar 

  • Normark BB (2003) The evolution of alternative genetic systems in insects. Annu Rev Entomol 48:397–423

    Article  PubMed  CAS  Google Scholar 

  • Nothnagle PJ, Schultz JC (1987) What is a forest pest? Insect outbreaks. Academic Press, San Diego, pp 59–80

    Google Scholar 

  • Opperman CH, Bird DM, Williamson VM, Rokhsar DS, Burke M, Cohn J et al (2008) Sequence and genetic map of Meloidogyne hapla: a compact nematode genome for plant parasitism. Proc Natl Acad Sci USA 105:14802–14807

    Article  PubMed  CAS  Google Scholar 

  • Osakabe M, Isobe H, Kasai A, Masuda R, Kubota S, Umeda M (2008) Aerodynamic advantages of upside down take-off for aerial dispersal in Tetranychus spider mites. Exp Appl Acarol 44:165–183

    Article  PubMed  Google Scholar 

  • Otto SP (2009) The evolutionary enigma of sex. Am Nat 174(Suppl 1):S1–S14

    Article  PubMed  Google Scholar 

  • Palaima A (2007) The fitness cost of generalization: present limitations and future possible solutions. Biol J Linn Soc 90:583–590

    Article  Google Scholar 

  • Ravigné V, Dieckmann U, Olivieri I (2009) Live where you thrive: joint evolution of habitat choice and local adaptation facilitates specialization and promotes diversity. Am Nat 174:E141–E169

    Article  PubMed  Google Scholar 

  • Rhainds M, Leather SR, Sadof C (2008) Polyphagy, flightlessness, and reproductive output of females: a case study with bagworms (Lepidoptera : Psychidae). Ecol Entomol 33:663–672

    Article  Google Scholar 

  • Rhainds M, Davis DR, Price PW (2009) Bionomics of bagworms (Lepidoptera: Psychidae). Annu Rev Entomol 54:209–226

    Article  PubMed  CAS  Google Scholar 

  • Rice WR, Friberg U (2009) A graphical approach to lineage selection between clonals and sexuals. Lost sex. Springer, Berlin, pp 75–97

    Google Scholar 

  • Robinson GS, Ackery PR, Kitching IJ, Beccaloni GW, Hernández LM (2010) HOSTS—a Database of the World’s Lepidopteran Hostplants. http://www.nhm.ac.uk/research-curation/research/projects/hostplants/. Natural History Museum, London

  • Ros VID, Breeuwer JAJ, Menken SBJ (2008) Origins of asexuality in Bryobia mites (Acari: Tetranychidae). BMC Evol Biol 8: article 153

  • Rupasinghe SG, Wen Z, Chiu T-L, Schuler MA (2007) Helicoverpa zea CYP6B8 and CYP321A1: different molecular solutions to the problem of metabolizing plant toxins and insecticides. Protein Eng Des Sel 20:615–624

    Article  PubMed  CAS  Google Scholar 

  • Scheffer S, Lewis M (2006) Mitochondrial phylogeography of the vegetable pest Liriomyza trifolii (Diptera: Agromyzidae): diverged clades and invasive populations. Ann Entomol Soc Am 99:991–998

    Article  Google Scholar 

  • Scheirs J, Jordaens K, de Bruyn L (2005) Have genetic trade-offs in host use been overlooked in arthropods? Evol Ecol 19:551–561

    Article  Google Scholar 

  • Schneider JC (1980) The role of parthenogenesis and female aptery in microgeographic, ecological adaptation in the fall cankerworm, Alsophila pometaria Harris (Lepidoptera: Geometridae). Ecology 61:1082–1090

    Article  Google Scholar 

  • Simpson SE, Nigg HN, Coile NC, Adair RA (1996) Diaprepes abbreviatus (Coleoptera: Curculionidae): host plant associations. Environ Entomol 25:333–349

    Google Scholar 

  • Singer MS (2008) Evolutionary ecology of polyphagy. Specialization, speciation and radiation: the evolutionary biology of herbivorous insects. University of California Press, Berkeley, pp 29–42

    Google Scholar 

  • Snäll N, Tammaru T, Wahlberg N, Viidalepp J, Ruohomaki K, Savontaus ML et al (2007) Phylogenetic relationships of the tribe Operophterini (Lepidoptera, Geometridae): a case study of the evolution of female flightlessness. Biol J Linn Soc 92:241–252

    Article  Google Scholar 

  • Snell-Rood EC, Van Dyken JD, Cruickshank T, Wade MJ, Moczek AP (2010) Toward a population genetic framework of developmental evolution: the costs, limits, and consequences of phenotypic plasticity. BioEssays 32:71–81

    Article  PubMed  CAS  Google Scholar 

  • Spencer K (1990) Host specialization in the world Agromyzidae (Diptera). Kluwer, Dordrecht

    Google Scholar 

  • Stenberg P, Lundmark M, Knutelski S, Saura A (2003) Evolution of clonality and polyploidy in a weevil system. Mol Biol Evol 20:1626–1632

    Article  PubMed  CAS  Google Scholar 

  • Stireman JOI (2005) The evolution of generalization? Parasitoid flies and the perils of inferring host range evolution from phylogenies. J Evol Biol 18:325–336

    Article  PubMed  Google Scholar 

  • Suomalainen E (1969) Evolution in parthenogenetic Curculionidae. Evol Biol 3:261–296

    Google Scholar 

  • Suomalainen E, Saura A, Lokki J (1987) Cytology and evolution in parthenogenesis. CRC Press, Boca Raton

    Google Scholar 

  • Tenow O, Nilssen AC, Bylund H, Hogstad O (2007) Waves and synchrony in Epirrita autumnata/Operophtera brumata outbreaks. I. Lagged synchrony: regionally, locally and among species. J Anim Ecol 76:258–268

    Article  PubMed  CAS  Google Scholar 

  • Tosh CR, Krause J, Ruxton GD (2009) Theoretical predictions strongly support decision accuracy as a major driver of ecological specialization. Proc Natl Acad Sci USA 106:5698–5702

    Article  PubMed  CAS  Google Scholar 

  • Trudgill DL, Blok VC (2001) Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Annu Rev Phytopathol 39:53–77

    Article  PubMed  CAS  Google Scholar 

  • Van Zandt PA, Mopper S (1998) A meta-analysis of adaptive deme formation in phytophagous insect populations. Am Nat 152:595–604

    Article  PubMed  CAS  Google Scholar 

  • Vrijenhoek RC, Parker ED Jr (2009) Geographical parthenogenesis: general purpose genotypes and frozen niche variation. Lost sex. Springer, Berlin, pp 99–131

    Google Scholar 

  • Whitlock MC (1996) The red queen beats the jack-of-all-trades: the limitations on the evolution of phenotypic plasticity and niche breadth. Am Nat 148:S65–S77

    Article  Google Scholar 

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

    Google Scholar 

  • Williams GC (1992) Natural selection: domains, levels, and challenges. Oxford University Press, Oxford

    Google Scholar 

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Acknowledgments

We dedicate this paper to Richard G. Harrison, who served as the ideal graduate advisor to BBN. Thanks to Richard Cowles for inviting BBN to talk about weevil evolution at the Biology and Management of Root Weevils symposium at the 2005 Entomological Society of America meeting, a talk that ultimately led to the writing of this paper. The paper was also crucially informed by studies of host use in armored scale insects, conducted by Jeremy Andersen, Rodger Gwiazdowski, and Jin Wu, and funded by the National Science Foundation (DEB-0447880). Thanks to Michael Lynch, Roger Blackman, Victor Eastop, May Berenbaum, Jan Engelstädter, Douglas Futuyma, Michael Whitlock, Ary Hoffman, and Sally Otto for discussion and encouragement. Thanks to Adrian Hine for help with HOSTS database queries. Thanks to Dan Howard and two anonymous reviewers for comments on an earlier draft of manuscript.

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Normark, B.B., Johnson, N.A. Niche explosion. Genetica 139, 551–564 (2011). https://doi.org/10.1007/s10709-010-9513-5

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