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Host specialization by reproductive interference between closely related herbivorous insects

  • Special feature: Original article
  • Reproductive Interference
  • Published:
Population Ecology

Abstract

Host specialization among closely related herbivores is common and is therefore a major theme in ecology. Despite its ecological importance, no general explanatory framework for host specialization is currently available. We introduce a new model of the evolution of host specialization in herbivorous insects. We use a two-dimensional lattice comprising 32 × 32 cells. Moreover, the model incorporates reproductive interference, defined as any negative outcomes resulting from interspecific mating, between two species of herbivores feeding on two different host plants as well as ordinary resource competition and differences in host suitability. Our simulation showed that reproductive interference, together with other factors such as host-related performance and resource competition, can actually drive the evolution of host specialization and thereby host partitioning between herbivorous insects during secondary contact. Host specialization arises particularly when levels of both reproductive interference and resource competition are intermediate. In contrast, host specialization seldom occurs if reproductive interference is absent. Thus, reproductive interference is as key to specialization as is spatial partitioning, which was not regarded as a realistic outcome when only resource competition was considered.

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References

  • Bernays E, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892

    Article  Google Scholar 

  • Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. University of Chicago Press, Chicago 221p

    Book  Google Scholar 

  • Colwell RK (1986) Community biology and sexual selection: lessons from hummingbird flower mites. In: Diamond J, Case TJ (eds) Community ecology. Harper & Row, New York, pp 406–424

    Google Scholar 

  • Dame EA, Petren K (2006) Behavioural mechanisms of invasion and displacement in Pacific island geckos (Hemidactylus). Anim Behav 71:1165–1173

    Article  Google Scholar 

  • Devictor V, Clavel J, Julliard R, Lavergne S, Mouillot D, Thuiller W, Venail P, Villéger S, Mouquet N (2010) Defining and measuring ecological specialization. J Appl Ecol 47:15–25

    Article  Google Scholar 

  • Egusa S, Nishida T, Sawada H, Fujisaki K (2008) Is selection of host plants by Plagiodera versicolora based on plant-related performance? Entomol Exp Appl 128:258–264

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Friberg M, Leimar O, Wiklund C (2013) Heterospecific courtship, minority effects and niche separation between cryptic butterfly species. J Evol Biol 26:971–979

    Article  CAS  PubMed  Google Scholar 

  • Fry JD (1996) The evolution of host specialization: are trade-offs overrated? Am Nat 148:S84–S107

    Article  Google Scholar 

  • Gröning J, Hochkirch A (2008) Reproductive interference between animal species. Q Rev Biol 83:257–282

    Article  PubMed  Google Scholar 

  • Hettyey A, Pearman PB (2003) Social environment and reproductive interference affect reproductive success in the frog Rana latastei. Behav Ecol 14:294–300

    Article  Google Scholar 

  • Hochkirch A, Gröning J, Bucker A (2007) Sympatry with the devil: reproductive interference could hamper species coexistence. J Anim Ecol 76:633–642

    Article  PubMed  Google Scholar 

  • Hutchinson GE (1957) Concluding remarks. Cold Spring Harb Symp Quant Biol 22:415–427

    Article  Google Scholar 

  • Iwao S (1977) Analysis of spatial association between two species based on the interspecies mean crowding. Res Popul Ecol 18:243–260

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Katakura H, Shioi M, Kira Y (1989) Reproductive isolation by host specificity in a pair of phytophagous ladybird beetles. Evolution 43:1045–1053

    Article  Google Scholar 

  • Kiritani K, Hokyo N, Yukawa J (1963) Co-existence of the two related stink bugs Nezara viridula and N. antennata under natural conditions. Res Popul Ecol 5:11–22

    Article  Google Scholar 

  • Kishi S, Tsubaki Y (2014) Avoidance of reproductive interference causes resource partitioning in bean beetle females. Popul Ecol 56:73–80

    Article  Google Scholar 

  • Kuno E (1992) Competitive exclusion through reproductive interference. Res Popul Ecol 34:275–284

    Article  Google Scholar 

  • Kyogoku D (2015) Reproductive interference: ecological and evolutionary consequences of interspecific promiscuity. Popul Ecol. doi:10.1007/s10144-015-0486-1

  • Kyogoku D, Nishida T (2012) The presence of heterospecific males causes an Allee effect. Popul Ecol 54:391–395

    Article  Google Scholar 

  • Lawton JH (1984) Non-competitive populations, non-convergent communities, and vacant niches: the herbivores of bracken. In: Strong D, Thistle AB (eds) Ecological communities: conceptual issues and the evidence. Princeton University Press, Princeton, pp 67–98

    Google Scholar 

  • Matsumoto K, Suzuki N (1995) The nature of mating plugs and the probability of reinsemination in Japanese Papilionidae. In: Scriber JM, Tsubaki Y, Lederhouse RC (eds) Swallowtail butterflies: their ecology and evolutionary biology. Scientific Publishers, Gainesville, pp 145–154

    Google Scholar 

  • Mayhew PJ (1997) Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79:417–428

    Article  Google Scholar 

  • McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185

    Article  PubMed  Google Scholar 

  • McLain D, Pratt A (1999) The cost of sexual coercion and heterospecific sexual harassment on the fecundity of a host-specific, seed-eating insect (Neacoryphus bicrucis). Behav Ecol Sociobiol 46:164–170

    Article  Google Scholar 

  • Nishida S, Kanaoka MM, Hashimoto K, Takakura K-I, Nishida T (2014) Pollen-pistil interactions in reproductive interference: comparisons of heterospecific pollen tube growth from alien species between two native Taraxacum species. Funct Ecol 28:450–457

    Article  Google Scholar 

  • Noriyuki S (2015) Host selection in insects: reproductive interference shapes behavior of ovipositing females. Population. doi:10.1007/s10144-015-0491-4

  • Noriyuki S, Osawa N, Nishida T (2012) Asymmetric reproductive interference between specialist and generalist predatory ladybirds. J Anim Ecol 81:1077–1085

    Article  PubMed  Google Scholar 

  • Ohsaki N, Sato Y (1994) Food plant choice of Pieris butterflies as a trade-off between parasitoid avoidance and quality of plants. Ecology 75:59–68

    Article  Google Scholar 

  • Rausher MD (1988) Is coevolution dead? Ecology 69:898–901

    Article  Google Scholar 

  • Ribeiro JMC, Spielman A (1986) The Satyr effect: a model predicting parapatry and species extinction. Am Nat 128:513–528

    Article  Google Scholar 

  • Strong DR (1982) Harmonious coexistence of hispine beetles on Heliconia in experimental and natural communities. Ecology 63:1039–1049

    Article  Google Scholar 

  • Strong DR (1984) Exorcising the ghost of competition past: phytophagous insects. In: Strong DR, Simberloff D, Abele LG, Thistle AB (eds) Ecological communities. Princeton University Press, Princeton, pp 28–42

    Google Scholar 

  • Suzuki N, Matsumoto K (1992) Lifetime mating success of males in a natural population of the papilionid butterfly, Atrophaneura alcinous (Lepidoptera: Papilionidae). Res Popul Ecol 34:397–407

    Article  Google Scholar 

  • Takakura K, Nishida T, Matsumoto T, Nishida S (2009) Alien dandelion reduces the seed-set of a native congener through frequency-dependent and one-sided effect. Biol Invasions 11:973–981

    Article  Google Scholar 

  • Takakura KI, Matsumoto T, Nishida S, Nishida T (2012) Analyses of the reproductive interference between native and invasive dandelions with individual based model. Jpn J Ecol 62:255–265 (in Japanese)

    Google Scholar 

  • Takakura KI, Nishida T, Iwao K (2015) Conflicting intersexual mate choices maintain interspecific sexual interactions. Popul Ecol. doi:10.1007/s10144-015-0492-3

  • Thompson JN (1994) The coevolutionary process. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Thum RA (2007) Reproductive interference, priority effects and the maintenance of parapatry in Skistodiaptomus copepods. Oikos 116:759–768

    Article  Google Scholar 

  • Valero A, Garcia CM, Magurran AE (2008) Heterospecific harassment of native endangered fishes by invasive guppies in Mexico. Biol Lett 4:149–152

    Article  PubMed Central  PubMed  Google Scholar 

  • Via S (1990) Ecological genetics and host adaptation in herbivorous insects: the experimental study of evolution in natural and agricultural systems. Ann Rev Entomol 35:421–446

    Article  CAS  Google Scholar 

  • Wilson W (2000) Simulating ecological and evolutionary systems in C. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Yoshimura J, Clark CW (1994) Population dynamics of sexual and resource competition. Theor Popul Biol 45:121–131

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Daisuke Kyogoku and Noriyuki Suzuki for their critical reading of the manuscript and helpful comments, and Hideki Yamamoto for using the source code for Mersenne twister random number generator ported to Object Pascal language. Thanks are also due to Shinji Fujii, David Hembry, Atsushi Honma, Kohmei Kadowaki, Kazutaka Kawatsu, Shigeki Kishi, Eizi Kuno, Takashi Matsumoto, Kenji Matuura, Reiichi Miura, Masashi Murakami, Sachiko Nishida, Naota Ohsaki, Ryusen Tajima, and Shingo Tanaka for stimulating discussion. This study was supported in part by Japanese Ministry of Education, Science, Sport and Culture (Nos. 16657008, 19770023 and 25650150).

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Correspondence to Takayoshi Nishida.

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Nishida, T., Takakura, K. & Iwao, K. Host specialization by reproductive interference between closely related herbivorous insects. Popul Ecol 57, 273–281 (2015). https://doi.org/10.1007/s10144-015-0490-5

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