Skip to main content

Microevolution of Insect–Bacterial Mutualists: A Population Genomics Perspective

  • Chapter
  • First Online:
Book cover Evolutionary Biology: Genome Evolution, Speciation, Coevolution and Origin of Life
  • 2563 Accesses

Abstract

The advent of high-throughput sequencing has ushered in a new era with enormous promise for study of short-timescale evolution. Insect–bacterial mutualists typically have tiny genomes allowing deep coverage for large populations. The importance of mutualists in ecological phenomena, such as invasions, leave much room for study. Nutritional mutualists of Order Hemiptera are of interest for being long coevolved with their hosts, thus degenerated in gene content, yet able to support their hosts on varying diets and during invasions. Determining the symbiont’s role and how adaptation might be achieved with a limited genetic repertoire is a challenge. One fruitful approach is highlighted in a recent population genomic study using a natural experiment: the 2009—present spread of the U.S. soybean pest Megacopta cribraria (Hemiptera: Plataspidae). This invasive species’ symbiont Ishikawaella capsulata (Gamma-proteobacteria) was previously shown to determine the pest-status of its host. Deep sequencing revealed allele frequency change since arrival that matched predictions, showing signatures of purifying and positive selection, with differences in “symbiont role” genes associated with different host plants. In the near future, this approach applied to other systems may illuminate the important role and dynamic potential of microbial symbionts in ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abbot P, Moran NA (2002) Extremely low levels of genetic polymorphism in endosymbionts (Buchnera) of aphids (Pemphigus). Mol Ecol 11:2649–2660

    Google Scholar 

  • Andersson DI (2008) Shrinking bacterial genomes. Microbe 3:124–130

    Google Scholar 

  • Aslan CE, Zavaleta ES, Tershy B, Croll D (2013) Mutualism disruption threatens global plant biodiversity: a systematic review. PLoS ONE 8(6):e66993

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barrett RDH, Schluter D (2008) Adaptation from standing genetic variation. Trends Ecol Evol 23:38–44

    Article  PubMed  Google Scholar 

  • Baumann P (2005) Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59:155–189

    Article  CAS  PubMed  Google Scholar 

  • Bennett AE (2013) Can plant–microbe–insect interactions enhance or inhibit the spread of invasive species? Funct Ecol 27(3):661–671

    Article  Google Scholar 

  • Bennett GM, Moran NA (2013) Small, smaller, smallest: the origins and evolution of ancient symbioses in a phloem-feeding insect. Genome Biol Evol 5(9):1675–1688

    Google Scholar 

  • Brown A, Huynh LY, Bolender CM, Nelson KG, McCutcheon JP (2013) Population genomics of a symbiont in the early stages of a pest invasion. Mol Ecol (published online in advance of print, Jul 11). doi:10.1111/mec.12366

  • Buchner P (1965) Endosymbiosis of animals with plant microorganisms. Interscience Publishers, New York

    Google Scholar 

  • Chubiz LM, Lee MC, Delaney NF, Marx CJ (2012) FREQ-Seq: a rapid, cost-effective, sequencing-based method to determine allele frequencies directly from mixed populations. PLoS ONE 7(10):e47959

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742–1744

    Article  CAS  PubMed  Google Scholar 

  • Dale C, Moran NA (2006) Molecular interactions between bacterial symbionts and their hosts. Cell 126:453–465

    Article  CAS  PubMed  Google Scholar 

  • De Grassi A, Segala C, Iannelli F, Volorio S, Bertario L, Radice P, Bernard L, Ciccarelli FD (2010) Ultradeep sequencing of a human ultraconserved region reveals somatic and constitutional genomic instability. PLoS Biol 8:e1000275

    Article  PubMed Central  PubMed  Google Scholar 

  • Desprez-Loustau M-L, Robin C, Buée M, Courtecuisse R, Garbaye J, Suffert F, Sache I, Rizzo DM (2007) The fungal dimension of biological invasions. Trends Ecol Evol 22:472–480

    Article  PubMed  Google Scholar 

  • Dunning Hotopp JC (2011) Horizontal gene transfer between bacteria and animals. Trends Genet 27(4):157–163

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Eger JE Jr, Ames LM, Suiter DR, Jenkins TM, Rider DA, Halbert SE (2010) Occurrence of the old world bug Megacopta cribraria (Fabricius) (Heteroptera: Plataspidae) in Georgia: a serious home invader and potential legume pest. Insecta Mundi 0121:1–11

    Google Scholar 

  • Excoffier L, Ray N (2008) Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol Evol 23:347–351

    Article  PubMed  Google Scholar 

  • Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36:533–543

    Article  Google Scholar 

  • Ferrari J, Vavre F (2011) Bacterial symbionts in insects or the story of communities affecting communities. Philos Trans R Soc B 366(1569):1389–1400

    Article  Google Scholar 

  • Forseth IN, Innis AF (2004) Kudzu (Pueraria montana): history, physiology, and ecology combine to make a major ecosystem threat. Crit Rev Plant Sci 23(5):401–413

    Article  Google Scholar 

  • François O, Currat M, Ray N, Han E, Excoffier L, Novembre J (2010) Principal component analysis under population genetic models of range expansion and admixture. Mol Biol Evol 27:1257–1268

    Article  PubMed  Google Scholar 

  • Fukatsu T, Hosokawa T (2002) Capsule-transmitted gut symbiotic bacterium of the Japanese common plataspid stinkbug, Megacopta punctatissima. Appl Environ Microbiol 68:389–396

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Funk DJ, Wernegreen JJ, Moran NA (2001) Intraspecific variation in symbiont genomes: bottlenecks and the aphid-Buchnera association. Genetics 157(2):477–489

    CAS  PubMed Central  PubMed  Google Scholar 

  • Goodrich-Blair H, Hussa E (2013) It takes a village: ecological and fitness impacts of multipartite mutualism. Annu Rev Microbiol 67:161–178

    Article  PubMed  Google Scholar 

  • Hansen AK, Moran NA (2013) The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol Ecol (published online in advance of print, Aug 16). doi:10.1111/mec.12421

  • Hosokawa T, Kikuchi Y, Meng XY, Fukatsu T (2005) The making of symbiont capsule in the plataspid stinkbug Megacopta punctatissima. FEMS Microbiol Ecol 54:471–477

    Article  CAS  PubMed  Google Scholar 

  • Hosokawa T, Kikuchi Y, Shimada M, Fukatsu T (2007) Obligate symbiont involved in pest status of host insect. Proc R Soc Lond Ser B 274:1979–1984

    Article  CAS  Google Scholar 

  • Hosokawa T, Kikuchi Y, Shimada M, Fukatsu T (2008) Symbiont acquisition alters behaviour of stinkbug nymphs. Biol Lett 4:45–48

    Article  PubMed Central  PubMed  Google Scholar 

  • Husnik F, Nikoh N, Koga R, Ross L, Duncan RP, Fujie M, Tanaka M, Satoh N, Bachtrog D, Wilson AC, von Dohlen CD, Fukatsu T, McCutcheon JP (2013) Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153(7):1567–1578

    Article  CAS  PubMed  Google Scholar 

  • Janson EM, Stireman JO III, Singer MS, Abbot P (2008) Phytophagous insect–microbe mutualisms and adaptive evolutionary diversification. Evolution 62:997–1012

    Article  PubMed  Google Scholar 

  • Jenkins TMJ, Eaton TD (2011) Population genetic baseline of the first plataspid stink bug symbiosis (Hemiptera: Heteroptera: Plataspidae) reported in North America. Insects 2:264–272

    Article  Google Scholar 

  • Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14(2):49–53

    Article  PubMed  Google Scholar 

  • Kikuchi A, Kobayashi H (2010) Effect of injury by adult Megacopta punctatissima (Montandon) (Hemiptera: Plataspidae) on the growth of soybean during the vegetative stage of growth. Jpn J Appl Entomol Zool 54:37–43

    Article  Google Scholar 

  • Lichman E (2010) Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecol Lett 13:1560–1572

    Article  Google Scholar 

  • MacDonald SJ, Thomas GH, Douglas AE (2011) Genetic and metabolic determinants of nutritional phenotype in an insect–bacterial symbiosis. Mol Ecol 20:2073–2084

    Article  CAS  PubMed  Google Scholar 

  • McCutcheon JP, Moran NA (2010) Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biol Evol 2:708–718

    PubMed Central  PubMed  Google Scholar 

  • McCutcheon JP, Moran NA (2011) Extreme genome reduction in symbiotic bacteria. Nature Rev Microbiol 10:13–26

    Google Scholar 

  • Mira A, Moran NA (2002) Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb Ecol 44(2):137–143

    Article  CAS  PubMed  Google Scholar 

  • Mira A, Ochman H, Moran NA (2001) Deletional bias and the evolution of bacterial genomes. Trends Genet 17:589–596

    Article  CAS  PubMed  Google Scholar 

  • Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190

    Article  CAS  PubMed  Google Scholar 

  • Nikoh N, Hosokawa T, Oshima K, Hattori M, Fukatsu T (2011) Reductive evolution of bacterial genome in insect gut environment. Genome Biol Evol 3:702–714

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nikoh N, McCutcheon JP, Kudo T, Miyagishima SY, Moran NA, Nakabachi A (2010) Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its host. PLoS Genet 6(2):e1000827

    Article  PubMed Central  PubMed  Google Scholar 

  • Orphan VJ (2009) Methods for unveiling cryptic microbial partnerships in nature. Curr Opin Microbiol 12:231–237

    Google Scholar 

  • Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmanek M (2000) Plant invasions—the role of mutualisms. Biol Rev 75(1):65–93

    Article  CAS  PubMed  Google Scholar 

  • Russell JA, Weldon S, Smith AH, Kim KL, Hu Y, Łukasik P, Doll S, Anastopoulos I, Novin M, Oliver KM (2013) Uncovering symbiont-driven genetic diversity across North American pea aphids. Mol Ecol 22(7):2045–2059

    Article  PubMed  Google Scholar 

  • Sandström J, Pettersson J (1994) Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance. J Insect Physiol 40:947–955

    Article  Google Scholar 

  • Suiter DR, Eger JE Jr, Gardner WA, Kemerait RC, All JN, Roberts PM, Greene JK, Ames LM, Buntin GD, Jenkins TM, Douce GK (2010) Discovery and distribution of Megacopta cribraria (Hemiptera: Heteroptera: Plataspidae) in northeast Georgia. J Integr Pest Manage 1:1–4

    Article  Google Scholar 

  • Palmer TM, Doak DF, Stanton ML, Bronstein JL, Kiers ET, Young TP, Goheen JR, Pringle RM (2010) Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism. Proc Nat Acad Sci 107(40):17234–17239

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

    Article  Google Scholar 

  • Traveset A, Richardson DM (2011) Mutualisms: key drivers of invasions… key casualties of invasions. In: Rchardson DM (ed) Fifty years of invasion ecology: the legacy of Charles Elton. Wiley-Blackwell, Oxford, pp 143–160

    Google Scholar 

  • Travis JM, Münkemüller T, Burton OJ, Best A, Dytham C, Johst K (2007) Deleterious mutations can surf to high densities on the wave front of an expanding population. Mol Biol Evol 24:2334–2343

    Article  CAS  PubMed  Google Scholar 

  • University of Georgia—Center for Invasive Species and Ecosystem Health (2013) Distribution map Megacopta cribraria. http://www.kudzubug.org/distribution_map.cfm. Accessed 20 Nov 2013

  • United States Department of Agriculture (2012) USDA Economic Research Service soybeans-oil-crops. http://www.ers.usda.gov/topics/crops/soybeans-oil-crops.aspx. Accessed 15 Oct 2012

  • Zhang Y, Hanula JL, Horn S (2012) The biology and preliminary host range of Megacopta cribraria (Heteroptera: Plataspidae) and its impact on kudzu growth. Environ Entomol 41:40–50

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

I am grateful to J. P. McCutcheon and N. M. Gerardo for support in the population genomic study discussed in this chapter. I also thank L. Y. Huynh, C. M. Bolender, K. G. Nelson, T. M. Jenkins, D. R. Suiter, J. K. Greene, M. L. Allen, and J. T. Van Leuven for help. The latter was funded by a USDA AFRI grant (2011-67013-30090) to J. P. McCutcheon.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Amanda M. V. Brown .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Brown, A.M.V. (2014). Microevolution of Insect–Bacterial Mutualists: A Population Genomics Perspective. In: Pontarotti, P. (eds) Evolutionary Biology: Genome Evolution, Speciation, Coevolution and Origin of Life. Springer, Cham. https://doi.org/10.1007/978-3-319-07623-2_12

Download citation

Publish with us

Policies and ethics