The eco-evolutionary impacts of domestication and agricultural practices on wild species

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 372, Issue 1712, 2017, Pages

  Turcotte, Martin M ^a   Araki, Hitoshi ^b   Karp, Daniel S ^c   Poveda, Katja ^d   Whitehead, Susan R ^d  

^a ETH ZURICH   (Switzerland)

^b HOKKAIDO UNIVERSITY   (Japan)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d Cornell University ^*  (United States)

Author keywords

Agricultural sustainability; Contemporary evolution; Eco evolutionary impacts; Evolutionary agroecology; Resistance evolution; Spillover effects

Indexed keywords

ADAPTATION; AGRICULTURAL PRACTICE; AGROECOLOGY; ALTERNATIVE AGRICULTURE; ANTHROPOGENIC EFFECT; DOMESTICATION; ECOSYSTEM RESILIENCE; EVOLUTIONARY BIOLOGY; GENE FLOW; INDUCED RESPONSE; SPECIALIZATION; WILD POPULATION;

ADAPTATION; AGRICULTURE; CROP; DOMESTICATION; EVOLUTION; GENE FLOW; GENETICS; GROWTH, DEVELOPMENT AND AGING; PROCEDURES;

ADAPTATION, BIOLOGICAL; AGRICULTURE; BIOLOGICAL EVOLUTION; CROPS, AGRICULTURAL; DOMESTICATION; GENE FLOW;

EID: 85006065034     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2016.0033     Document Type: Review

References (79)

1. Palumbi SR. 2001 Humans as the world’s greatest evolutionary force. Science 293, 1786-1790. (doi:10.1126/science.293.5536.1786)
2. Milla R, Osborne CP, Turcotte MM, Violle C. 2015 Plant domestication through an ecological lens. Trends Ecol. Evol. 30, 463-469. (doi:10.1016/j.tree.2015.06.006)
3. Khush GS. 2001 Green revolution: the way forward. Nat. Rev. Genet. 2, 815-822. (doi:10.1038/35093585)
4. Foley JA et al. 2005 Global consequences of land use. Science 309, 570-574. (doi:10.1126/science.1111772)
5. Newbold T et al. 2015 Global effects of land use on local terrestrial biodiversity. Nature 520, 45-50. (doi:10.1038/nature14324)
6. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE. 2010 Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25, 345-353. (doi:10.1016/j.tree.2010.01.007)
7. Settle WH, Ariawan H, Astuti ET, Cahyana W, Hakim AL, Hindayana D, Lestari AS. 1996 Managing tropical rice pests through conservation of generalist natural enemies and alternative prey. Ecology 77, 1975-1988. (doi:10.2307/2265694)
8. Chaplin-Kramer R, O’Rourke ME, Blitzer EJ, Kremen C. 2011 A meta-analysis of crop pest and natural enemy response to landscape complexity. Ecol. Lett. 14, 922-932. (doi:10.1111/j.1461-0248.2011.01642.x)
9. Karp DS, Rominger AJ, Zook J, Ranganathan J, Ehrlich PR, Daily GC. 2012 Intensive agriculture erodes b-diversity at large scales. Ecol. Lett. 15, 963-970. (doi:10.1111/j.1461-0248.2012.01815.x)
10. Frishkoff LO, Karp DS, M’Gonigle LK, Mendenhall CD, Zook J, Kremen C, Hadly EA, Daily GC. 2014 Loss of avian phylogenetic diversity in neotropical agricultural systems. Science 345, 1343-1346. (doi:10.1126/science.1254610)
11. Kremen C, Miles A. 2012 Ecosystem services in biologically diversified versus conventional farming systems: benefits, externalities, and trade-offs. Ecol. Soc. 17, 40. (doi:10.5751/ES-05035-170440)
12. Drès M, Mallet J. 2002 Host races in plant-feeding insects and their importance in sympatric speciation. Phil. Trans. R. Soc. Lond. B 357, 471-492. (doi:10.1098/rstb.2002.1059)
13. Stukenbrock EH, McDonald BA. 2008 The origins of plant pathogens in agro-ecosystems. Annu. Rev. Phytopathol. 46, 75-100. (doi:10.1146/annurev.phyto.010708.154114)
14. Meyer RS, Purugganan MD. 2013 Evolution of crop species: genetics of domestication and diversification. Nat. Rev. Genet. 14, 840-852. (doi:10.1038/nrg3605)
15. Tabashnik BE. 1983 Host range evolution: the shift from native legume hosts to alfalfa by the butterfly, Colias philodice eriphyle. Evolution 37, 150-162. (doi:10.2307/2408183)
16. Filchak KE, Roethele JB, Feder JL. 2000 Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella. Nature 407, 739-742. (doi:10.1038/35037578)
17. Powell THQ, Hood GR, Murphy MO, Heilveil JS, Berlocher SH, Nosil P, Feder JL. 2013 Genetic divergence along the speciation continuum: the transition from host race to species in Rhagoletis (Diptera: Tephritidae). Evolution 67, 2561-2576. (doi:10.1111/evo.12209)
18. Kingsley RA, Bäumler AJ. 2000 Host adaptation and the emergence of infectious disease: the Salmonella paradigm. Mol. Microbiol. 36, 1006-1014. (doi:10.1046/j.1365-2958.2000.01907.x)
19. Messina FJ. 2004 Predictable modification of body size and competitive ability following a host shift by a seed beetle. Evolution 58, 2788-2797. (doi:10.1111/j.0014-3820.2004.tb01630.x)
20. Turcotte MM, Lochab AK, Turley NE, Johnson MTJ. 2015 Plant domestication slows pest evolution. Ecol. Lett. 18, 907-915. (doi:10.1111/ele.12467)
21. Stear MJ, Bishop SC, Mallard BA, Raadsma H. 2001 The sustainability, feasibility and desirability of breeding livestock for disease resistance. Res. Vet. Sci. 71, 1-7. (doi:10.1053/rvsc.2001.0496)
22. Burdon JJ, Thrall PH. 2008 Pathogen evolution across the agro-ecological interface: implications for disease management. Evol. Appl. 1, 57-65. (doi:10.1111/j.1752-4571.2007.00005.x)
23. McDonald BA, Linde C. 2002 Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40, 349-379. (doi:10.1146/annurev.phyto.40.120501.101443)
24. Brown JKM. 2015 Durable resistance of crops to disease: A Darwinian perspective. Annu. Rev. Phytopathol. 53, 513-539. (doi:10.1146/annurev-phyto-102313-045914)
25. Rogalski MA, Gowler CD, Shaw CL, Hufbauer RA, Duffy MA. 2017 Human drivers of ecological and evolutionary dynamics in emerging and disappearing infectious disease systems. Phil. Trans. R. Soc. B 372, 20160043. (doi:10.1098/rstb.2016.0043)
26. Neve P, Vila-Aiub M, Roux F. 2009 Evolutionary-thinking in agricultural weed management. New Phytol. 184, 783-793. (doi:10.1111/j.1469-8137.2009.03034.x)
27. Jin L, Zhang H, Lu Y, Yang Y, Wu K, Tabashnik BE, Wu Y. 2015 Large-scale test of the natural refuge strategy for delaying insect resistance to transgenic Bt crops. Nat. Biotechnol. 33, 169-174. (doi:10.1038/nbt.3100)
28. Gould F. 1991 The evolutionary potential of crop pests. Am. Sci. 79, 496-507. (doi:10.2307/29774519)
29. Liu X, Chen M, Collins HL, Onstad DW, Roush RT, Zhang Q, Earle ED, Shelton AM. 2014 Natural enemies delay insect resistance to BT crops. PLoS ONE 9, e90366. (doi:10.1371/journal.pone.0090366)
30. Barrett SH. 1983 Crop mimicry in weeds. Econ. Bot. 37, 255-282. (doi:10.1007/BF02858881)
31. Krysan JL, Foster DE, Branson TF, Ostlie KR, Cranshaw WS. 1986 Two years before the hatch: rootworms adapt to crop rotation. Bull. Entomol. Soc. Am. 32, 250-253. (doi:10.1093/besa/32.4.250)
32. Gray ME, Sappington TW, Miller NJ, Moeser J, Bohn MO. 2009 Adaptation and invasiveness of western corn rootworm: intensifying research on a worsening pest. Annu. Rev. Entomol. 54, 303-321. (doi:10.1146/annurev.ento.54.110807.090434)
33. Knolhoff LM, Onstad DW, Spencer JL, Levine E. 2006 Behavioral differences between rotation-resistant and wild-type Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae). Environ. Entomol. 35, 1049-1057. (doi:10.1603/0046-225X-35.4.1049)
34. Georghiou GP, Saito T. 1983 Pest resistance to pesticides. New York, NY: Plenum Press.
35. Sutherland IA, Leathwick DM. 2011 Anthelmintic resistance in nematode parasites of cattle: a global issue? Trends Parasitol. 27, 176-181. (doi:10.1016/j.pt.2010.11.008)
36. Abbas RZ, Zaman MA, Colwell DD, Gilleard J, Iqbal Z. 2014 Acaricide resistance in cattle ticks and approaches to its management: the state of play. Vet. Parasitol. 203, 6-20. (doi:10.1016/j.vetpar.2014.03.006)
37. Heap I. 2016 The International Survey of Herbicide Resistant Weeds. 14 May 2016. See http://www.weedscience.org.
38. Délye C, Jasieniuk M, Le Corre V. 2013 Deciphering the evolution of herbicide resistance in weeds. Trends Genet. 29, 649-658. (doi:10.1016/j.tig.2013.06.001)
39. Laxminarayan R et al. 2013 Antibiotic resistance-the need for global solutions. Lancet Infect. Dis. 13, 1057-1098. (doi:10.1016/S1473-3099(13)70318-9)
40. Hiltunen T, Virta M, Laine A-L. 2017 Antibiotic resistance in the wild: an eco-evolutionary perspective. Phil. Trans. R. Soc. B 372, 20160039. (doi:10.1098/rstb.2016.0039)
41. Tabashnik BE, Brévault T, Carrière Y. 2013 Insect resistance to Bt crops: lessons from the first billion acres. Nat. Biotechnol. 31, 510-521. (doi:10.1038/nbt.2597)
42. Powles SB. 2008 Evolution in action: glyphosate-resistant weeds threaten world crops. Outlooks Pest Manage. 19, 256-259. (doi:10.1564/19dec07)
43. McNair CM. 2015 Ectoparasites of medical and veterinary importance: drug resistance and the need for alternative control methods. J. Pharm. Pharmacol. 67, 351-363. (doi:10.1111/jphp.12368)
44. Ellstrand NC, Prentice HC, Hancock JF. 1999 Gene flow and introgression from domesticated plants into their wild relatives. Annu. Rev. Ecol. Syst. 30, 539-563. (doi:10.1146/annurev.ecolsys.30.1.539)
45. Marshall FB, Dobney K, Denham T, Capriles JM. 2014 Evaluating the roles of directed breeding and gene flow in animal domestication. Proc. Natl Acad. Sci. USA 111, 6153-6158. (doi:10.1073/pnas.1312984110)
46. Crow JF, Kimura M. 1970 An introduction to population genetics theory. New York, NY: Harper & Row.
47. Lynch M, O’Hely M. 2001 Captive breeding and the genetic fitness of natural populations. Conserv. Genet. 2, 363-378. (doi:10.1023/A:1012550620717)
48. Satake A, Araki H. 2012 Stocking of captive-bred fish can cause long-term population decline and gene pool replacement: predictions from a population dynamics model incorporating density-dependent mortality. Theor. Ecol. 5, 283-296. (doi:10.1007/s12080-011-0128-y)
49. Araki H, Cooper B, Blouin MS. 2007 Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318, 100-103.(doi:10.1126/science.1145621)
50. Araki H, Cooper B, Blouin MS. 2009 Carry-over effect of captive breeding reduces reproductive fitness of wild-born descendants in the wild. Biol. Lett. 5, 621-624. (doi:10.1098/rsbl.2009.0315)
51. Ellstrand NC, Heredia SM, Leak-Garcia JA, Heraty JM, Burger JC, Yao L, Nohzadeh-Malakshah S, Ridley CE. 2010 Crops gone wild: evolution of weeds and invasives from domesticated ancestors. Evol. Appl. 3, 494-504. (doi:10.1111/j.1752-4571.2010.00140.x)
52. Andow DA, Zwahlen C. 2006 Assessing environmental risks of transgenic plants. Ecol. Lett. 9, 196-214. (doi:10.1111/j.1461-0248.2005.00846.x)
53. Ervin DE et al. 2010 Impact of genetically engineered 8 crops on farm sustainability in the United States. Washington, DC: National Academy of Sciences.
54. Rosenthal BM. 2009 How has agriculture influenced the geography and genetics of animal parasites? Trends Parasitol. 25, 67-70. (doi:10.1016/j.pt.2008.10.004)
55. Leroy T, Caffier V, Celton J-M, Anger N, Durel C-E, Lemaire C, Le Cam B. 2016 When virulence originates from nonagricultural hosts: evolutionary and epidemiological consequences of introgressions following secondary contacts in Venturia inaequalis. New Phytol. 210, 1443-1452. (doi:10.1111/nph.13873)
56. Ristaino JB, Groves CT, Parra GR. 2001 PCR amplification of the Irish potato famine pathogen from historic specimens. Nature 411, 695-697. (doi:10.1038/35079606)
57. Hendry AP, Gotanda KM, Svensson EI. 2017 Human influences on evolution, and the ecological and societal consequences. Phil. Trans. R. Soc. B 372, 20160028. (doi:10.1098/rstb.2016.0028)
58. Pimentel D et al. 1992 Environmental and economic costs of pesticide use. BioScience 42, 750-760. (doi:10.2307/1311994)
59. Oerke EC. 2006 Crop losses to pests. J. Agric. Sci. 144, 31-43. (doi:10.1017/S0021859605005708)
60. Bouchard MF et al. 2011 Prenatal exposure to organophosphate pesticides and IQ in 7-year-old children. Environ. Health Perspect. 119, 1189-1195. (doi:10.1289/ehp.1003185)
61. Köhler H-R, Triebskorn R. 2013 Wildlife ecotoxicology of pesticides: can we track effects to the population level and beyond? Science 341, 759-765. (doi:10.1126/science.1237591)
62. Alyokhin A, Mota-Sanchez D, Baker M, Snyder WE, Menasha S, Whalon M, Dively G, Moarsi WF. 2015 The Red Queen in a potato field: integrated pest management versus chemical dependency in Colorado potato beetle control. Pest Manage. Sci. 71, 343-356. (doi:10.1002/ps.3826)
63. Komadina N, McVernon J, Hall R, Leder K. 2014 A historical perspective of influenza A(H1N2) virus. Emerg. Infect. Dis. 20, 6-12. (doi:10.3201/eid2001.121848)
64. Warzecha D, Diekötter T, Wolters V, Jauker F. 2016 Intraspecific body size increases with habitat fragmentation in wild bee pollinators. Landsc. Ecol. 31, 1449-1455. (doi:10.1007/s10980-016-0349-y)
65. Renauld M, Hutchinson A, Loeb G, Poveda K, Connelly H. 2016 Landscape simplification constrains adult size in a native ground-nesting bee. PLoS ONE 11, e0150946. (doi:10.1371/journal.pone.0150946)
66. Nouhuys S, Via S. 1999 Natural selection and genetic differentiation of behaviour between parasitoids from wild and cultivated habitats. Heredity 83, 127-137. (doi:10.1046/j.1365-2540.1999.00549.x)
67. Fussmann GF, Loreau M, Abrams PA. 2007 Eco-evolutionary dynamics of communities and ecosystems. Funct. Ecol. 21, 465-477. (doi:10.1111/j.1365-2435.2007.01275.x)
68. Gámez-Virués S et al. 2015 Landscape simplification filters species traits and drives biotic homogenization. Nat. Commun. 6, 8568. (doi:10.1038/ncomms9568)
69. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, Ley RE. 2013 Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc. Natl Acad. Sci. USA 110, 6548-6553. (doi:10.1073/pnas.1302837110)
70. Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J, Pan Y, McHardy AC, Schulze-Lefert P. 2015 Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17, 392-403. (doi:10.1016/j.chom.2015.01.011)
71. Clark TL, Hibbard BE. 2004 Comparison of nonmaize hosts to support eastern corn rootworm (Coleoptera: Chrysomelidae) larval biology. Environ. Entomol. 33, 681-689. (doi:10.1603/0046-225X-33.3.681)
72. Chen YH, Gols R, Benrey B. 2015 Crop domestication and its impact on naturally selected trophic interactions. Annu. Rev. Entomol. 60, 35-58. (doi:10.1146/annurev-ento-010814-020601)
73. Whitehead SR, Turcotte MM, Poveda K. 2017 Domestication impacts on plant-herbivore interactions: a meta-analysis. Phil. Trans. R. Soc. B 372, 20160034. (doi:10.1098/rstb.2016.0034)
74. Turcotte MM, Turley NE, Johnson MTJ. 2014 The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events. New Phytol. 204, 671-681. (doi:10.1111/nph.12935)
75. Rausher MD. 2001 Co-evolution and plant resistance to natural enemies. Nature 411, 857-864. (doi:10.1038/35081193)
76. Svensson EI, Råberg L. 2010 Resistance and tolerance in animal enemy-victim coevolution. Trends Ecol. Evol. 25, 267-274. (doi:10.1016/j.tree.92009.12.005)
77. Wall E, Simm G, Moran D. 2010 Developing breeding schemes to assist mitigation of greenhouse gas emissions. Animal 4, 366-376. (doi:10.1017/S175173110999070X)
78. de Haas Y, Windig JJ, Calus MPL, Dijkstra J, de Haan M, Bannink A, Veerkamp RF. 2011 Genetic parameters for predicted methane production and potential for reducing enteric emissions through genomic selection. J. Dairy Sci. 94, 6122-6134. (doi:10.3168/jds.2011-4439)
79. Parry MAJ, Hawkesford MJ. 2010 Genetic approaches to reduce greenhouse gas emissions: increasing carbon capture and decreasing environmental impact. In Climate change and crop production (ed. MP Reynolds), pp. 139-150. Wallingford, UK: CAB International.