Does early learning drive ecological divergence during speciation processes in parasitoid wasps?

Proceedings of the Royal Society B: Biological Sciences

Volumn 282, Issue 1799, 2015, Pages

  König, Kerstin ^a   Krimmer, Elena ^a   Brose, Sören ^a   Gantert, Cornelia ^a   Buschlüter, Ines ^a   König, Christian ^b   Klopfstein, Seraina ^c   Wendt, Ingo ^b   Baur, Hannes ^d   Krogmann, Lars ^b   Steidle, Johannes L M ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b STAATLICHES MUSEUM FÜR NATURKUNDE   (Germany)

^c SWEDISH MUSEUM OF NATURAL HISTORY   (Sweden)

^d NATURHISTORISCHES MUSEUM DER BURGERGEMEINDE BERN   (Switzerland)

Author keywords

Early adult experience; Early learning; Ecological speciation; Host preference; Host switch; Lariophagus distinguendus

Indexed keywords

EID: 84920982546     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.1850     Document Type: Article

References (69)

1. Resh VH, Carde´ RT. 2003 Encyclopedia of insects, pp. XXV. New York, NY: Academic Press.
2. Mayhew PJ. 2007 Why are there so many insect species? Perspectives from fossils and phylogenies. Biol. Rev. Camb. Philos. Soc. 82, 425–454. (doi:10. 1111/j.1469-185X.2007.00018.x)
3. Schluter D. 2009 Evidence for ecological speciation and its alternative. Science 323, 737–739. (doi:10. 1126/science.1160006)
4. Nosil P. 2012 Ecological speciation. Oxford, UK: Oxford University Press.
5. Funk DJ, Filchak KE, Feder JL. 2002 Herbivorous insects: model systems for the comparative study of speciation ecology. Genetics 116, 251–267. (doi:10. 1007/978-94-010-0265-3_10)
6. Funk DJ, Nosil P, Etges WJ. 2006 Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proc. R. Soc. B 103, 3209–3213. (doi:10.1073/pnas. 0508653103)
7. Davis JM, Stamps JA. 2004 The effect of natal experience on habitat preferences. Trends Ecol. Evol. 19, 411–416. (doi:10.1016/j.tree.2004.04.006)
8. Feder JL, Opp SB, Wlazlo B, Reynolds K, Go W, Spisak S. 1994 Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly. Proc. Natl Acad. Sci. USA 91, 7990–7994. (doi:10.1073/pnas.91.17.7990)
9. Thorpe W, Jones F. 1937 Olfactory conditioning in a parasitic insect and its relation to the problem of host selection. Proc. R. Soc. Lond. B 124, 56–81. (doi:10.1098/rspb.1937.0072)
10. Immelmann K. 1975 Significance of imprinting and early learning. Annu. Rev. Ecol. Evol. Syst. 6, 15–37. (doi:10.1146/annurev.es.06.110175.000311)
11. Dukas R. 2008 Evolutionary biology of insect learning. Annu. Rev. Entomol. 53, 145–160. (doi:10.1146/annurev.ento.53.103106.093343)
12. Askew RR. 1968 Considerations on speciation in Chalcidoidea (Hymenoptera). Evolution 22, 642–645. (doi:10.2307/2406886)
13. Godfray HCJ. 1994 Parasitoids: behavioral and evolutionary ecology. Princeton, NJ: Princeton University Press.
14. Quicke DLJ. 1997 Parasitic wasps, ch. 10, pp. 302–328. London, UK: Chapman & Hall.
15. Pak GA, Buis HCEM, Heck ICC, Hermans MLG. 1986 Behavioural variations among strains of Trichogramma spp.: host-age selection. Entomol. Exp. Appl. 40, 247–258. (doi:10.1111/j.1570-7458.1986.tb00508.x)
16. Vos M, Vet LEM. 2004 Geographic variation in host acceptance by an insect parasitoid: genotype versus experience. Evol. Ecol. Res. 6, 1021–1035.
17. Forbes AA, Hood GR, Feder JL. 2010 Geographic and ecological overlap of parasitoid wasps associated with the Rhagoletis pomonella (Diptera: Tephritidae) species complex. Ann. Entomol. Soc. Am. 103/6, 908–915. (doi:10.1603/AN10046)
18. Heimpel GE, Antolin MF, Franqui RA, Strand MR. 1997 Reproductive isolation and genetic variation between two ‘strains’ of Bracon hebetor (Hymenoptera: Braconidae). Biol. Control 9, 149–156. (doi:10.1006/bcon.1997.0529)
19. Caubet Y, Jaisson P. 1991 A post-eclosion early learning involved in host recognition by Dinarmus basalis Rondani (Hymenoptera: Pteromalidae). Anim. Behav. 42, 977–980. (doi:10.1016/S0003- 3472(05)80150-2)
20. Hare JD. 1996 Priming Aphytis: behavioral modification of host selection by exposure to a synthetic contact kairomone. Entomol. Exp. Appl. 78, 263–269. (doi:10.1111/j.1570-7458.1996. tb00790.x)
21. Villagra CA, Pennacchio F, Niemeyer HM. 2007 The effect of larval and early adult experience on behavioural plasticity of the aphid parasitoid Aphidius ervi (Hymenoptera, Braconidae, Aphidiinae). Naturwissenschaften 94, 903–910. (doi:10.1007/s00114-007-0269-4)
22. Barron AB. 2001 The life and death of Hopkins’ host selection principle. J. Ins. Behav. 14, 725–737. (doi:10.1023/A:1013033332535)
23. Noyes JS. 2014 Universal chalcidoidea database. See http://www.nhm.ac.uk/chalcidoids.
24. Goodrich ES. 1921 Note on the Hymenoptera parasite in beetles infesting grains. Report of the Grain Pest (War) Committee of the Royal Society of London 9, 5–7. Cambridge Scholars Publishing.
25. Kaschef AH. 1961 Gibbium psylloides Czemp. (Col., Ptinidae), new host of Lariophagus distinguendus Foerst. (Hym., Pteromalidae). Z Parasitenk. 21, 65–70. (doi:10.1007/BF00260177)
26. Bellows Jr TS. 1985 Effects of host age and host availability on developmental period, adult size, sex ratio, longevity and fecundity in Lariophagus distinguendus Fo¨rster (Hymenoptera: Pteromalidae). Res. Popul. Ecol. 27, 55–64. (doi:10.1007/ BF02515479)
27. Niedermayer S, Steidle JLM. 2013 The Hohenheimer Box – a new way to rear and release Lariophagus distinguendus to control stored product pest insects. Biol. Control 64, 263–269. (doi:101016/j.biocontrol.2012.12.005)
28. Steidle JLM, Scho¨ller M. 2002 Fecundity and ability of the parasitoid Lariophagus distinguendus (Hymenoptera: Pteromalidae) to parasitize larvae of the granary weevil Sitophilus granarius (Coleoptera: Curculionidae) in bulk grain. J. Stored Prod. Res. 38, 43–53. (doi:10.1016/S0022-474X(00)00044-8)
29. Steidle JLM. 2000 Host recognition cues of the granary weevil parasitoid Lariophagus distinguendus (Hymenoptera: Pteromalidae). Entomol. Exp. Appl. 95, 185–192. (doi:10.1023/A:1003934224535)
30. Steidle JLM, Steppuhn A, Reinhard J. 2001 Volatile cues from different host complexes used for host location by the generalist parasitoid Lariophagus distinguendus (Hymenoptera: Pteromalidae). Basic Appl. Ecol. 2, 45–51. (doi:10.1078/1439- 1791-00035)
31. Steidle JLM, Steppuhn A, Ruther J. 2003 Specific foraging kairomones used by a generalist parasitoid. J. Chem. Ecol. 29, 131–143. (doi:10.1023/ A:1021932731350)
32. Steidle JLM. 1998 Learning pays off: influence of experience on host finding and parasitism in Lariophagus distinguendus (Hymenoptera: Pteromalidae). Ecol. Ent. 23, 451–456. (doi:10. 1046/j.1365-2311.1998.00144.x)
33. Collatz J, Muller C, Steidle J L M,. 2006 Proteinsynthesis dependent long-term memory induced by one single associative training trial in the parasitic wasp Lariophagus distinguendus. Learn. Mem. 13, 263–266. (doi:10.1101/lm.192506)
34. Ruther J, Homann M, Steidle JLM. 2000 Femalederived sex pheromone mediates courtship behaviour in the parasitoid Lariophagus distinguendus. Entomol. Exp. Appl. 96, 265–274. (doi:10.1046/j.1570-7458.2000.00705.x)
35. Steiner S, Steidle JLM, Ruther J. 2005 Female sex pheromone in immature insect males: a case of preemergence chemical mimicry? Behav. Ecol. Sociobiol. 58, 111–120. (doi:10.1007/s00265-005-0930-x)
36. Schurmann D, Sommer C, Schinko APB, Greschista M, Smid H, Steidle JLM. 2012 Demonstration of long-term memory in the parasitic wasp Nasonia vitripennis (Hymenoptera: Pteromalidae). Entomol. Exp. Appl. 143, 199–206. (doi:10.1111/j.1570-7458.2012.01253.x)
37. Hartig G, Peters RS, Borner J, Etzbauer C, Misof B, Niehuis O. 2012 Oligonucleotide primers for targeted amplification of single-copy nuclear genes in apocritan Hymenoptera. PLoS ONE 7/6, 39826. (doi:10.1371/journal.pone.0039826)
38. Katoh K, Standley DM. 2013 MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780. (doi:10.1093/molbev/ mst010)
39. Katoh K, Kuma K, Toh H, Miyata T. 2005 MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511–518. (doi:10.1093/nar/gki198)
40. Wernersson R. 2006 Virtual ribosome: a comprehensive DNA translation tool with support for integration of sequence feature annotation. Nucleic Acids Res. 34, W385–W388. (doi:10.1093/ nar/gkl252)
41. Oliveira DCSG, Raychoudhury R, Lavrov DV, Werren JH. 2008 Rapidly evolving mitochondrial genome and directional selection in mitochondrial genes in the parasitic wasp Nasonia (Hymenoptera: Pteromalidae). Mol. Biol. Evol. 25, 2167–2180. (doi:10.1093/molbev/msn159)
42. Klopfstein S, Vilhelmsen L, Heraty JM, Sharkey M, Ronquist F. 2013 The hymenopteran tree of life: evidence from protein-coding genes and objectively aligned ribosomal data. PLoS ONE 8, 69344. (doi:10.1371/journal.pone.0069344)
43. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013 MEGA6: molecular evolutionary genetics analysis v.6.0. Mol. Biol. Evol. 30, 2725–2729. (doi:10.1093/molbev/mst197)
44. Schwarz GE. 1978 Estimating the dimension of a model. Ann. Stat. 6, 461–464. (doi:10.1214/aos/ 1176344136)
45. Lanfear R, Calcott B, Ho SYW, Guindon S. 2012 PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29, 1695–1701. (doi:10. 1093/molbev/mss020)
46. Zwickl DJ. 2006 Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD dissertation, The University of Texas at Austin, TX.
47. Swofford DL. 2002 PAUP*:phylogenetic analysis using parsimony (*and other methods). (version 4.0b10). Sunderland, MA: Sinauer Associates.
48. Hebert PDN, Cywinska A, Ball SL, deWaard JR. 2003 Biological identifications through DNA barcodes. Proc. R. Soc. Lond. B 270, 313–321. (doi:10.1098/ rspb.2002.2218)
49. N’gendo RN, Osiemo ZB, Brandl R. 2012 DNA barcodes for species identification in the hyperdiverse ant genus Pheidole (Formicidae: Myrmicinae). J. Insect Sci. 13,27. (doi:10.1673/031.013.2701)
50. Ruther J, Steiner S. 2008 Costs of female odour in males of the parasitic wasp Lariophagus distinguendus (Hymenoptera: Pteromalidae). Naturwissenschaften 95, 547–552. (doi:10.1007/ s00114-008-0357-0)
51. Gibson JD, Niehuis O, Peirson BRE, Cash EI, Gadau J. 2013 Genetic and developmental basis of F2 hybrid breakdown in Nasonia parasitoid wasps. Evolution 67, 2124–2132. (doi:10.1111/evo.12080)
52. Werren JH. 1997 Biology of Wolbachia. Annu. Rev. Entomol. 42, 587–609. (doi:10.1146/annurev.ento.42.1.587)
53. Niehuis O et al. 2013 Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones. Nature 494, 345–348. (doi:10. 1038/nature11838)
54. Kuehbandner S, Hacker K, Niedermayer S, Steidle JLM, Ruther R. 2012 Composition of cuticular lipids in the pteromalid wasp Lariophagus distinguendus is host dependent. Bull. Entomol. Res. 102, 610–617. (doi:10.1017/S000748531200017X)
55. Graham MWRDV. 1969 The Pteromalidae of northwestern Europe (Hymenoptera: Chalcidoidea). Bull. Br. Mus. (Nat. Hist.) Entomol. Suppl. 16, 1–908.
56. Hopkins AD. 1917 A discussion of CG. Hewitt’s paper on ‘Insect behaviour’. J. Econ. Entomol. 10, 92–93.
57. van Emden HF, Sponagl B, Wagner E, Baker T, Ganguly S, Douloumpaka S. 1996 Hopkins’ ‘host selection principle’, another nail in its coffin. Physiol. Entomol. 21, 325–328. (doi:10.1111/j. 1365-3032.1996.tb00873.x)
58. Jaenike J. 1983 Induction of host preference in Drosophila melanogaster. Oecologia 58, 320–325. (doi:10.1007/BF00385230)
59. Corbet S. 1985 Insect chemosensory responses: a chemical legacy hypothesis. Ecol. Entomol. 10, 143–153. (doi:10.1111/j.1365-2311.1985. tb00543.x)
60. Tully T, Cambiazo V, Kruse L. 1994 Memory through metamorphosis in normal and mutant Drososphila. J. Neurosci. 14, 68–74.
61. Ray S. 1999 Survival of olfactory memory through metamorphosis in the fly Musca domestica. Neurosci. Lett. 259, 37–40. (doi:10.1016/S0304- 3940(98)00892-1)
62. Gandolfi M, Mattiacci L, Dorn S. 2003 Preimaginal learning determines adult response to chemical stimuli in a parasitic wasp. Proc. R. Soc. Lond. B 270, 2623–2629. (doi:10.1098/rspb.2003.2541)
63. Eilenberg J, Hajek A, Lomer C. 2001 Suggestions for unifying the terminology in biological control. Biocontrol 46, 387–400. (doi:10.1023/A:1014 193329979)
64. Louda SM, Pemberton RW, Johnson MT, Follett PA. 2003 Nontarget effects: the Achilles´ heel of biological control? Retrospective analyses to reduce risk associated with biocontrol introductions. Annu. Rev. Entomol. 48, 365–396. (doi:10.1146/annurev. ento.48.060402.102800)
65. Beltman JB, Haccou P. 2005 Speciation through learning of habitat features. Theor. Popul. Biol. 67, 189–202. (doi:10.1016/j.tpb.2005.01.001)
66. Payne RB, Payne LL, Woods JL. 1998 Song learning in brood-parasitic indigobirds Vidua chalybeata: song mimicry of the host species. Anim. Behav. 55/ 6, 1537–1553. (doi:10.1006/anbe.1997.0701)
67. Payne RB, Payne LL, Woods JL, Sorenson MD. 2000 Imprinting and the origin of parasite–host species associations in female brood parasitic indigobirds, Vidua chalybeata. Anim. Behav. 59, 69–81. (doi:10. 1006/anbe.1999.1283)
68. Sorenson MD, Sefc KM, Payne RB. 2003 Speciation by host switch in brood parasitic indigobirds. Nature 424, 928–931. (doi:10.1038/nature01863)
69. Schoonhoven LM, van Loon JJA, Dicke M. 2005 Insect plant biology, pp. 209–232, ch. 8. Oxford, UK: Oxford University Press.