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Host shift capability of a specialist seed predator of an invasive plant: roles of competition, population genetics and plant chemistry

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Abstract

Acanthoscelides macrophthalmus is a seed predator that has become widely distributed along with its native host, Leucaena leucocephala (Mimosoideae), which is a neotropical leguminous tree and one of the most invasive plants worldwide. Previous studies revealed that A. macrophthalmus is able to host-shift to several mimosoid species. Here, we aim to test the host-shift potential to other mimosoid and non-mimosoid plants and possible roles of interspecific competition, genetic background, and plant chemistry in host-shift. First, we found that A. macrophthalmus predator completed development on two new hosts: pigeon pea Cajanus cajan and Cajanus scarabaeoides (Faboideae), by rearing from seeds collected in South/Southeast Asia and Hawaii. In contrast, in most regions, both Cajanus species were infested only by other beetle species. Second, we performed no-choice tests using 11 leguminous plants, covering all three subfamilies as potential hosts, including the two new hosts. A Taiwanese A. macrophthalmus population reared in the laboratory on Leucaena did not deposit eggs on any of the seeds of each tested species. To compare host-shift responses between populations, we also used a Hawaiian A. macrophthalmus population that had completed its development on freshly collected Leucaena seeds from the field. This population deposited eggs onto and hatching larvae burrowed into C. cajan seeds, although none developed beyond the larval stage. Third, the surface chemical composition of seed-pods of L. leucocephala and the two Cajanus species was dissimilar, although that of seeds was highly similar. Finally, all of the host-shifting A. macrophthalmus populations shared the same haplotypic group.

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References

  • Adams R, Cristol SJ, Anderson AA, Albert AA (1945) The structure of leucenol, 1. J Am Chem Soc 67:89–92

    Article  CAS  Google Scholar 

  • Agosta SJ (2006) On ecological fitting, plant-insect associations, herbivore host shifts, and host plant selection. Oikos 114:556–565

    Article  Google Scholar 

  • Agosta SJ, Janz N, Brooks DR (2010) How specialists can be generalists: resolving the “parasite paradox” and implications for emerging infectious disease. Zoologia 27:151–162

    Article  Google Scholar 

  • Amarillo-Suarez AR, Fox CW (2006) Population differences in host use by a seed-beetle: local adaptation, phenotypic plasticity and maternal effects. Oecologia 150:247–258

    Article  PubMed  Google Scholar 

  • Bell EA, Lackey JA, Polhill RM (1978) Systematic significance of canavanine in the Papilionoideae. Biochem Syst Ecol 6:201–212

    Article  CAS  Google Scholar 

  • Benda N, Possley J, Powell D, Buchanan-McGrath C, Cuda J (2012) New host plant record for the poison ivy sawfly, Arge humeralis (Hymenoptera: Argidae), and its performance on two host plant species. Fla Entomol 95:529–531

    Article  Google Scholar 

  • Bernays EA, Chapman RF (1994) Host-plant selection by phytophagous insects. Chapman and Hall, New York

    Google Scholar 

  • Bertheau C, Brockerhoff EG, Roux-Morabito G, Lieutier F, Jactel H (2010) Novel insect-tree associations resulting from accidental and intentional biological ‘invasions’: a meta-analysis of effects on insect fitness. Ecol Lett 13:506–515

    Article  PubMed  Google Scholar 

  • Cavalcante GM, Moreira AFC, Vasconcelos SD (2006) Insecticidal potential of aqueous extracts from arboreous species against whitefly. Pesqui Agropecu Bras 41:9–14

    Article  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  PubMed  Google Scholar 

  • Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insects—competition reexamined and resurrected. Annu Rev Entomol 40:297–331

    Article  CAS  Google Scholar 

  • Effowe TQ, Amevoin K, Nuto Y, Mondedji D, Glitho IA (2010) Reproductive capacities and development of a seed bruchid beetle, Acanthoscelides macrophthalmus, a potential host for the mass rearing of the parasitoid, Dinarmus basalis. J Insect Sci 10:1–14

    Google Scholar 

  • Egli D, Olckers T (2012) Oviposition patterns and egg mortality in Acanthoscelides macrophthalmus (Chrysomelidae: Bruchinae), a biological control agent of Leucaena leucocephala (Fabaceae) in South Africa. Afr Entomol 20:111–118

    Article  Google Scholar 

  • Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608

    Article  Google Scholar 

  • Eigenbrode SD, Espelie KE (1995) Effects of plant epicuticular lipids on insect herbivores. Annu Rev Entomol 40:171–194

    Article  Google Scholar 

  • Feder JL, Reynolds K, Go W, Wang EC (1995) Intraspecific and interspecific competition and host race formation in the apple maggot fly, Rhagoletis pomonella (Diptera, Tephritidae). Oecologia 101:416–425

    Article  Google Scholar 

  • Finlay-Doney M, Walter GH (2005) Discrimination among host plants (Leucaena species and accessions) by the psyllid pest Heteropsylla cubana and implications for understanding resistance. Agric For Entomol 7:153–160

    Article  Google Scholar 

  • Forister ML, Dyer LA, Singer MS, Stireman JO, Lill JT (2012) Revisiting the evolution of ecological specialization, with emphasis on insect-plant interactions. Ecology 93:981–991

    Article  CAS  PubMed  Google Scholar 

  • Gouinguene S, Buser HR, Stadler E (2005) Host-plant leaf surface compounds influencing oviposition in Delia antique. Chemoecology 15:243–249

    Article  CAS  Google Scholar 

  • Guerra AA, Martinez S, Delrio HS (1994) Natural and synthetic oviposition stimulants for Catolaccus grandis (Burks) females. J Chem Ecol 20:1583–1594

    Article  CAS  PubMed  Google Scholar 

  • Hartlieb E, Rembold H (1996) Behavioral response of female Helicoverpa (Heliothis) armigera Hb (Lepidoptera: Noctuidae) moths to synthetic pigeonpea (Cajanus cajan L) kairomone. J Chem Ecol 22:821–837

    Article  CAS  PubMed  Google Scholar 

  • Hetz M, Johnson CD (1988) Hymenopterous parasites of some bruchid beetles of North and Central America. J Stored Prod Res 24:131–143

    Article  Google Scholar 

  • Hora KH, Roessingh P (1999) Oviposition in Yponomeuta cagnagellus: the importance of contact cues for host plant acceptance. Physiol Entomol 24:109–120

    Article  Google Scholar 

  • Hudaib T, Hayes W, Brown S, Eady PE (2010) Effect of seed moisture content and D-limonene on oviposition decisions of the seed beetle Callosobruchus maculatus. Entomol Exp Appl 137:120–125

    Article  CAS  Google Scholar 

  • Hughes CE, Johnson CD (1996) New host records and notes on Bruchidae (Coleoptera) from Leucaena Benth. (Leguminosae, Mimosoideae) from Mexico, Central and South America. J Appl Entomol 120:137–141

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Janz N (2011) Ehrlich and Raven revisited: mechanisms underlying codiversification of plants and enemies. Annu Rev Ecol Evol Syst 42:71–89

    Article  Google Scholar 

  • Janz N, Nylin S (1998) Butterflies and plants: a phylogenetic study. Evolution 52:486–502

    Article  Google Scholar 

  • Janzen DH (1973) Host plants as islands. II. Competition in evolutionary and contemporary time. Am Nat 107:786–790

    Article  Google Scholar 

  • Janzen DH (1985) On ecological fitting. Oikos 45:308–310

    Article  Google Scholar 

  • Jermy T (1984) Evolution of insect/host plant relationships. Am Nat 124:609–630

    Article  Google Scholar 

  • Johnson CD (1979) New host records for Acanthoscelides (Coleoptera: Bruchidae). Pan-Pacific Entomol 55:61–71

    Google Scholar 

  • Johnson CD, Siemens DH (1991) Expanded oviposition range by a seed beetle (Coleoptera, Bruchidae) in proximity to a normal host. Environ Entomol 20:1577–1582

    Google Scholar 

  • Kato T, Bonet A, Yoshitake H, Romero-Napoles J, Jinbo U, Ito M, Shimada M (2010) Evolution of host utilization patterns in the seed beetle genus Mimosestes Bridwell (Coleoptera: Chrysomelidae: Bruchinae). Mol Phylogenet Evol 55:816–832

    Article  CAS  PubMed  Google Scholar 

  • Kergoat GJ, Alvarez N, Hossaert-McKey M, Faure N, Silvain J-F (2005) Parallels in the evolution of the two largest New and Old World seed-beetle genera (Coleoptera, Bruchidae). Mol Ecol 14:4003–4021

    Google Scholar 

  • Kergoat GJ, Silvain J-F, Buranapanichpan S, Tuda M (2007) When insects help to resolve plant phylogeny: evidence for a paraphyletic genus Acacia from the systematics and host-plant range of their seed-predators. Zool Scr 36:143–152

    Article  Google Scholar 

  • Kingsolver JM (2004) Handbook of the Bruchidae of the United States and Canada (Insecta, Coleoptera), vol I. USDA-ARS, Tech Bull 1912

    Google Scholar 

  • Li G, Ishikawa Y (2006) Leaf epicuticular wax chemicals of the Japanese knotweed Fallopia japonica as oviposition stimulants for Ostrinia latipennis. J Chem Ecol 32:595–604

    Article  CAS  PubMed  Google Scholar 

  • Little EL Jr, Skolmen RG (1989) Common forest trees of Hawaii. USDA Agriculture Handbook 67

  • Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the World’s worst invasive alien species: A selection from the global invasive species database. The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN)

  • Mascré M (1937) Compt rend 204:890

    Google Scholar 

  • Merrill ED (1921–1926) An enumeration of Philippine flowering plants, vol 4. Bureau of Science, Manila

  • Messina FJ, Jones JC, Mendenhall M, Muller A (2009) Genetic modification of host acceptance by a seed beetle, Callosobruchus maculatus (Coleoptera: Bruchidae). Ann Entomol Soc Am 102:181–188

    Article  Google Scholar 

  • Mitter C, Farrell B, Futuyma DJ (1991) Phylogenetic studies of insect-plant interactions: insights into the genesis of diversity. TREE 6:290–293

    CAS  PubMed  Google Scholar 

  • Moran NA (1988) The evolution of host-plant alternation in aphids: evidence for specialization as a dead end. Am Nat 132:681–706

    Article  Google Scholar 

  • Nawrot J, Gawlak M, Szafranek J, Szafranek B, Synak E, Warchalewski JR, Piasecka-Kwiatkowska D, Blaszczak W, Jelinski T, Fornal J (2010) The effect of wheat grain composition, cuticular lipids and kernel surface microstructure on feeding, egg-laying, and the development of the granary weevil, Sitophilus granarius (L.). J Stored Prod Res 46:133–141

    Article  CAS  Google Scholar 

  • Nazzi F, Vidoni F, Frilli F (2008) Semiochemicals affecting the host-related behaviour of the dry bean beetle Acanthoscelides obtectus (Say). J Stored Prod Res 44:108–114

    Article  CAS  Google Scholar 

  • Neser S (1994) Conflicts of interest? The Leucaena controversy. Plant Prot News S Afr 6:8

    Google Scholar 

  • Nosil P, Mooers AO (2005) Testing hypotheses about ecological specialization using phylogenetic trees. Evolution 59:2256–2263

    CAS  PubMed  Google Scholar 

  • Ogunbinu AO, Flamini G, Cioni PL, Adebayo MA, Ogunwande IA (2009) Constituents of Cajanus cajan (L.) Millsp., Moringa oleifera Lam., Heliotropium indicum L. and Bidens pilosa L. from Nigeria. Nat Prod Comm 4:573–578

    CAS  Google Scholar 

  • Olckers T (2004) Targeting emerging weeds for biological control in South Africa: the benefits of halting the spread of alien plants at an early stage of their invasion. S Afr J Sci 100:64–68

    Google Scholar 

  • Olckers T (2011) Biological control of Leucaena leucocephala (Lam.) de Wit (Fabaceae) in South Africa: a tale of opportunism, seed feeders and unanswered questions. Afr Entomol 19:356–365

    Article  Google Scholar 

  • Parr MJ, Tran BMD, Simmonds MSJ, Kite GC, Credland PF (1998) Influence of some fatty acids on oviposition by the bruchid beetle, Callosobruchus maculatus. J Chem Ecol 24:1577–1593

    Article  CAS  Google Scholar 

  • Raghu S, Wiltshire C, Dhileepan K (2005) Intensity of predispersal seed predation in the invasive legume Leucaena leucocephala is limited by the duration of pod retention. Austral Ecol 30:310–318

    Article  Google Scholar 

  • Sambaraju KR, Phillips TW (2008) Effects of physical and chemical factors on oviposition by Plodia interpunctella (Lepidoptera: Pyralidae). Ann Entomol Soc Am 101:955–963

    Article  Google Scholar 

  • Samuelson GA (1991) Bruchid in koa haole pods—Acanthoscelides macrophthalmus. Hawaii Entomol Soc Newsl 1:2

    Google Scholar 

  • Saxena KB, Singh L, Reddy MV, Singh U, Lateef SS, Sharma SB, Remanandan P (1990) Intra species variation in Atylosia scarabaeoides (L.) Benth., a wild relative of pigeonpea (Cajanus cajan (L.) Millsp.). Euphytica 49:185–191

    Google Scholar 

  • Sembene M (2006) The origin of groundnut infestation by the seed beetle Caryedon serratus (Olivier) (Coleoptera: Bruchidae): Results from cytochrome B and ITS1 gene sequences. J Stored Prod Res 42:97–111

    Article  CAS  Google Scholar 

  • Shanower TG, Romeis J, Minja EM (1999) Insect pests of pigeonpea and their management. Annu Rev Entomol 44:77–96

    Article  CAS  PubMed  Google Scholar 

  • Shoba Z, Olckers T (2010) Reassessment of the biology and host range of Acanthoscelides macrophthalmus (Chrysomelidae: Bruchinae), a seed feeding beetle released for the biological control of Leucaena leucocephala in South Africa. Afr Entomol 18(Suppl 1):1–9

    Article  Google Scholar 

  • Smartt J (1990) Grain legumes: evolution and genetic resources. Cambridge University Press, Cambridge 381 pp

    Book  Google Scholar 

  • Smith CW (1985) Impact of alien plants on Hawai’i’s native biota. In: Stone CP, Scott JM (eds) Hawai’i’s terrestrial ecosystems: preservation and management. Cooperative National Park Resources Studies Unit. University of Hawaii Press, Honolulu, pp 180–250

    Google Scholar 

  • Southgate BJ, McFarlane JA (1979) Host records of Specularius species (Coleoptera, Bruchidae) with notes on the infestation of pigeon peas (Cajanus cajan (L.)) by these beetles. East Afr Agric For J 42:219–223

    Google Scholar 

  • Strong DR (1977) Time and number of herbivore species: pests of sugarcane. Ecology 58:167–175

    Article  Google Scholar 

  • Sulehrie MAQ, Golob P, Tran BMD, Farrell G (2003) The effect of attributes of Vigna spp. on the bionomics of Callosobruchus maculatus. Entomol Exp Appl 106:159–168

    Article  Google Scholar 

  • Syrett P (1999) Broom beetle gets taste for tagasaste. Biocontrol News Inf 20:51

    Google Scholar 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633

    CAS  PubMed  Google Scholar 

  • Tilmon KJ, Wood TK, Pesek JD (1998) Genetic variation in performance traits and the potential for host shifts in Enchenopa treehoppers (Homoptera: Membracidae). Ann Entomol Soc Am 91:397–403

    Google Scholar 

  • Tuda M (2007) Applied evolutionary ecology of insects of the subfamily Bruchinae (Coleoptera: Chrysomelidae). Appl Entomol Zool 42:337–346

    Article  Google Scholar 

  • Tuda M, Fukatsu T, Shimada M (1995) Species differentiation of bruchid beetles (Coleoptera: Bruchidae) analyzed by mitochondrial DNA polymorphism. Appl Entomol Zool 30:377–380

    Google Scholar 

  • Tuda M, Wasano N, Kondo N, Horng S-B, Chou L-Y, Tateishi Y (2004) Habitat-related mtDNA polymorphism in a stored-bean pest Callosobruchus chinensis (Coleoptera: Bruchidae). Bull Entomol Res 94:75–80

    Article  CAS  PubMed  Google Scholar 

  • Tuda M, Chou L-Y, Niyomdham C, Buranapanichpan S, Tateishi Y (2005) Ecological factors associated with pest status in Callosobruchus (Coleoptera: Bruchidae): high host specificity of non-pests to Cajaninae (Fabaceae). J Stored Prod Res 41:31–45

    Article  Google Scholar 

  • Tuda M, Ronn J, Buranapanichpan S, Wasano N, Arnqvist G (2006) Evolutionary diversification of the bean beetle genus Callosobruchus (Coleoptera : Bruchidae): traits associated with stored-product pest status. Mol Ecol 15:3541–3551

    Article  CAS  PubMed  Google Scholar 

  • Tuda M, Wu L-H, Tateishi Y, Niyomdham C, Buranapanichpan S, Morimoto K, Wu W-J, Wang C-P, Chen Z-Q, Zhu H-Y, Zhang Y-C, Murugan K, Chou L-Y, Johnson CD (2009) A novel host shift and invaded range of a seed predator, Acanthoscelides macrophthalmus (Coleoptera: Chrysomelidae: Bruchinae), of an invasive weed, Leucaena leucocephala. Entomol Sci 12:1–8

    Article  Google Scholar 

  • Vassiliou VA, Papadoulis G (2008) First record of Acanthoscelides macrophthalmus (Schaeffer) (Coleoptera: Bruchidae) in Cyprus. Entomol Hellenica 17:52–55

    Google Scholar 

  • Walton CS (2003) Leucaena (Leucaena leucocephala) in Queensland. Department of Natural Resources and Mines, Queensland

    Google Scholar 

  • Wasserman SS (1986) Genetic variation in adaptation to foodplants among populations of the southern cowpea weevil, Callosobruchus maculatus: evolution of oviposition preference. Entomol Exp Appl 42:201–212

    Article  Google Scholar 

  • Williams RD, Hoagland RE (2007) Phytotoxicity of mimosine and albizziine on seed germination and seedling growth of crops and weeds. Allelopath J 19:423–430

    Google Scholar 

  • Wu S-H, Chaw S-M, Rejmanek M (2003) Naturalized Fabaceae (Leguminosae) species in Taiwan: the first approximation. Bot Bull Acad Sinica 44:59–66

    Google Scholar 

  • Wu L-H, Wu W-J, Wang C-P, Chen S-W (2007) A new record of bruchid beetle from Taiwan (Acanthoscelides macrophthalmus) (Coleoptera: Bruchidae). Plant Prot Bull Taiwan 49:75–80

    Google Scholar 

  • Wu L-H, Wang C-P, Wu W-J (2012) Description and differentiation of the four larval instars of Acanthoscelides macrophthalmus (Coleoptera: Chrysomelidae: Bruchinae). Ann Entomol Soc Am 105:259–267

    Article  Google Scholar 

  • Wu L-H, Wang C-P, Wu W-J (2013) Effects of temperature and adult nutrition on the development of Acanthoscelides macrophthalmus, a natural enemy of an invasive tree, Leucaena leucocephala. Biol Control 65:322–329

    Article  Google Scholar 

  • Yang J (2000) Primary analysis on utilization and extension of Leucaena leucocephala. South Fodd Column 3:2

    Google Scholar 

  • Yoshida K, Oka S (2004) Invasion of Leucaena leucocephala and its effects on the native plant community in the Ogasawara (Bonin) Islands. Weed Technol 18:1371–1375

    Article  Google Scholar 

  • Yotoko KSC, Prado PI, Russo CAM, Solferini VN (2005) Testing the trend towards specialization in herbivore-host plant associations using a molecular phylogeny of Tomoplagia (Diptera: Tephritidae). Mol Phylogenet Evol 35:701–711

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank G. A. Samuelson and J. Romero for the identification of A. macrophthalmus. We also thank L.-Y. Chou, Y. Tateishi, and C. Niyomdham for partly assisting with the collection and identification of legumes. This study was supported in part by Grant-in-Aids for Scientific Research from JSPS and by the Research Grant for Young Investigators of Faculty of Agriculture, Kyushu University to MT. This study complies with the current laws of countries in which collection and experiments were performed.

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  1. L.-H. Wu

    Present address: Centre for Environmental Stress and Adaptation Research, Zoology Department, University of Melbourne, Bio21, 30 Flemington Rd., Parkville, VIC, 3010, Australia

Authors and Affiliations

  1. Institute of Biological Control, Bioresource Sciences, Faculty of Agriculture, Kyushu University, Fukuoka, 812-8581, Japan

    M. Tuda

  2. Department of Entomology, National Taiwan University, Taipei, 106, Taiwan

    L.-H. Wu & W.-J. Wu

  3. Faculty of Agriculture, Kyushu University, Fukuoka, 812-8581, Japan

    N. Yamada & K. Kagoshima

  4. Silviculture Division, Taiwan Forestry Research Institute, Council of Agriculture, Taipei, 100, Taiwan

    C.-P. Wang

  5. Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai, 50200, Thailand

    S. Buranapanichpan

  6. Institute of Plant Protection, Yunnan Academy of Agricultural Sciences, Kunming, Yunnan, China

    Z.-Q. Chen

  7. Hawaii Department of Agriculture, 1428 South King St., Honolulu, HI, 96814-2512, USA

    K. K. Teramoto, B. R. Kumashiro & R. Heu

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  1. M. Tuda
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Correspondence to M. Tuda.

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M. Tuda, L.-H. Wu and N. Yamada have equally contributed to this study.

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Tuda, M., Wu, LH., Yamada, N. et al. Host shift capability of a specialist seed predator of an invasive plant: roles of competition, population genetics and plant chemistry. Biol Invasions 16, 303–313 (2014). https://doi.org/10.1007/s10530-013-0519-7

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