Ants farm subterranean aphids mostly in single clone groups--an example of prudent husbandry for carbohydrates and proteins?

Aniek B F Ivens, Daniel J C Kronauer, Ido Pen, Franz J Weissing, Jacobus J Boomsma
Author Information
  1. Aniek B F Ivens: Theoretical Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, Groningen, The Netherlands. A.B.F.Ivens@rug.nl

Abstract

BACKGROUND: Mutualistic interactions are wide-spread but the mechanisms underlying their evolutionary stability and ecological dynamics remain poorly understood. Cultivation mutualisms in which hosts consume symbionts occur in phylogenetically diverse groups, but often have symbiont monocultures for each host. This is consistent with the prediction that symbionts should avoid coexistence with other strains so that host services continue to benefit relatives, but it is less clear whether hosts should always favor monocultures and what mechanisms they might have to manipulate symbiont diversity. Few mutualisms have been studied in sufficient genetic detail to address these issues, so we decided to characterize symbiont diversity in the complex mutualism between multiple root aphid species and Lasius flavus ants. After showing elsewhere that three of these aphid species have low dispersal and mostly if not exclusively asexual reproduction, we here investigate aphid diversity within and between ant nest mounds.
RESULTS: The three focal species (Geoica utricularia, Forda marginata and Tetraneura ulmi) had considerable clonal diversity at the population level. Yet more than half of the ant mounds contained just a single aphid species, a significantly higher percentage than expected from a random distribution. Over 60% of these single-species mounds had a single aphid clone, and clones tended to persist across subsequent years. Whenever multiple species/clones co-occurred in the same mound, they were spatially separated with more than 95% of the aphid chambers containing individuals of a single clone.
CONCLUSIONS: L. flavus "husbandry" is characterized by low aphid "livestock" diversity per colony, especially at the nest-chamber level, but it lacks the exclusive monocultures known from other cultivation mutualisms. The ants appear to eat most of the early instar aphids, so that adult aphids are unlikely to face limited phloem resources and scramble competition with other aphids. We suggest that such culling of carbohydrate-providing symbionts for protein ingestion may maintain maximal host yield per aphid while also benefitting the domesticated aphids as long as their clone-mates reproduce successfully. The cost-benefit logic of this type of polyculture husbandry has striking analogies with human farming practices based on slaughtering young animals for meat to maximize milk-production by a carefully regulated adult livestock population.

References

  1. Biotechniques. 1991 Apr;10(4):506-13 [PMID: 1867860]
  2. Trends Ecol Evol. 1999 Feb;14(2):49-53 [PMID: 10234251]
  3. Proc Natl Acad Sci U S A. 2010 Sep 7;107(36):15712-6 [PMID: 20733067]
  4. Mycologia. 2003 May-Jun;95(3):388-98 [PMID: 21156627]
  5. Proc Biol Sci. 1996 Mar 22;263(1368):339-44 [PMID: 8920255]
  6. Proc Natl Acad Sci U S A. 2011 Jan 18;108(3):E7; author reply E8 [PMID: 21220350]
  7. Science. 2005 Feb 4;307(5710):741-4 [PMID: 15692054]
  8. Mol Ecol. 2011 Nov;20(22):4772-85 [PMID: 21777319]
  9. Biol Lett. 2006 Dec 22;2(4):593-6 [PMID: 17148297]
  10. Mol Ecol. 2012 Sep;21(17):4257-69 [PMID: 22804757]
  11. Am Nat. 2011 Jan;177(1):75-85 [PMID: 21091210]
  12. Curr Biol. 2007 Aug 21;17(16):R661-72 [PMID: 17714660]
  13. Proc Biol Sci. 2002 Oct 7;269(1504):2023-7 [PMID: 12396501]
  14. Nature. 2006 Jun 22;441(7096):975-8 [PMID: 16791194]
  15. PLoS One. 2010 Sep 10;5(9): [PMID: 20844760]
  16. J Evol Biol. 2010 Dec;23(12):2507-28 [PMID: 20942825]
  17. Evolution. 2001 Oct;55(10):1980-91 [PMID: 11761059]
  18. Ecol Lett. 2009 Jan;12(1):13-21 [PMID: 19019195]
  19. Proc Natl Acad Sci U S A. 2010 Oct 5;107(40):17234-9 [PMID: 20855614]
  20. Science. 2011 Oct 21;334(6054):362-5 [PMID: 22021855]
  21. Biol Lett. 2010 Apr 23;6(2):282-6 [PMID: 19923136]
  22. Ecology. 2006 Jan;87(1):103-12 [PMID: 16634301]
  23. Mycorrhiza. 2005 Nov;15(8):571-579 [PMID: 15947957]
  24. Annu Rev Genet. 2008;42:165-90 [PMID: 18983256]
  25. Science. 2009 Nov 20;326(5956):1103-6 [PMID: 19965427]
  26. Proc Biol Sci. 2006 Mar 7;273(1586):595-602 [PMID: 16537131]

MeSH Term

Animals
Ants
Aphids
Biodiversity
Carbohydrates
Microsatellite Repeats
Proteins
Reproduction, Asexual
Sequence Analysis, DNA
Symbiosis

Chemicals

Carbohydrates
Proteins

Word Cloud

Created with Highcharts 10.0.0aphiddiversityaphidsspeciessinglemutualismssymbiontssymbiontmonocultureshostmoundsclonemechanismshostsmultipleflavusantsthreelowmostlyantpopulationlevelperadulthusbandryBACKGROUND:Mutualisticinteractionswide-spreadunderlyingevolutionarystabilityecologicaldynamicsremainpoorlyunderstoodCultivationconsumeoccurphylogeneticallydiversegroupsoftenconsistentpredictionavoidcoexistencestrainsservicescontinuebenefitrelativeslessclearwhetheralwaysfavormightmanipulatestudiedsufficientgeneticdetailaddressissuesdecidedcharacterizecomplexmutualismrootLasiusshowingelsewheredispersalexclusivelyasexualreproductioninvestigatewithinnestRESULTS:focalGeoicautriculariaFordamarginataTetraneuraulmiconsiderableclonalYethalfcontainedjustsignificantlyhigherpercentageexpectedrandomdistribution60%single-speciesclonestendedpersistacrosssubsequentyearsWheneverspecies/clonesco-occurredmoundspatiallyseparated95%chamberscontainingindividualsCONCLUSIONS:L"husbandry"characterized"livestock"colonyespeciallynest-chamberlacksexclusiveknowncultivationappeareatearlyinstarunlikelyfacelimitedphloemresourcesscramblecompetitionsuggestcullingcarbohydrate-providingproteiningestionmaymaintainmaximalyieldalsobenefittingdomesticatedlongclone-matesreproducesuccessfullycost-benefitlogictypepolyculturestrikinganalogieshumanfarmingpracticesbasedslaughteringyounganimalsmeatmaximizemilk-productioncarefullyregulatedlivestockAntsfarmsubterraneangroups--anexampleprudentcarbohydratesproteins?

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