Do differences in life-history traits and the timing of peak mating activity between host-associated populations of Chilo suppressalis have a genetic basis?

Abstract

The development of host races, genetically distinct populations of the same species with different hosts, is considered to be the initial stage of ecological speciation. Ecological and biological differences consistent with host race formation have been reported between water-oat and rice-associated populations of Chilo suppressalis. In order to confirm whether these differences have a genetic basis, we conducted experiments to determine the extent to which various life-history traits and the time of peak mating activity of these populations were influenced by the species of host plant larvae were raised on. Individuals from each population were reared for three consecutive generations on either water-oat fruit pulp or rice seedlings. Descendants of both populations had higher larval survival rates, shorter larval developmental periods, higher pupal weight, and longer adult forewings, when reared on water-oats than when reared on rice. The time of peak of mating activity differed between the descendants of each population, irrespective of whether they were raised on water-oats or rice. These results indicate that although some life-history traits of host-associated populations of C. suppressalis are influenced by the host plant larvae are raised on, time of peak mating activity is not. Because it is a stable, objective, phenotypic trait, further research on difference in the time of peak mating activity between host-associated populations of C. suppressalis should be conducted to clarify the mechanism responsible for host race formation in this species.

References Calcagno, V., Y. Thomas, and D. Bourguet. 2007. Sympatric host races of the European corn borer: adaptation to host plants and hybrid performance. J. Evol. Biol. 20:1720–1729. Chen, J. M., X. P. Yu, X. S. Zheng, H. X. Xu, Z. X. Lu, and J. F. Zhang. 2003. Biological performances of the striped stem borer, Chilo suppressalis Walker fed on Jiaobai, Zizania caduciflora, and rice plants. Acta Agric. Zhejiangensis 15:139–143. Diegisser, T., J. Johannesen, C. Lehr, and A. Seitz. 2004. Genetic and morphological differentiation in Tephritis bardanae (Diptera: Tephritidae): evidence for host-race formation. J. Evol. Biol. 17:83–93. Ding, N., P. Dalin, Q. H. Zhu, W. H. Ma, F. Zhu, and X. P. Wang. 2013. A comparison of the larval overwintering biology of the striped stem borer, Chilo suppressalis (Lepidoptera: Crambidae), in rice and water-oat fields. Appl. Entomol. Zool. 48:147–153. Dres, M., and J. Mallet. 2002. Host races in plant-feeding insects and their importance in sympatric speciation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357:471–492. Etges, W. J., and C. C. de Oliveira. 2014. Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. X. Age-specific dynamics of adult epicuticular hydrocarbon expression in response to different host plants. Ecol. Evol. 4:2033–2045. Feder, J. L., and K. E. Filchak. 1999. It's about time: the evidence for host plant-mediated selection in the apple maggot fly, Rhagoletis pomonella, and its implications for fitness trade-offs in phytophagous insects. Entomol. Exp. Appl. 91:211–225. Funk, D. J., K. E. Filchak, and J. L. Feder. 2002. Herbivorous insects: model systems for the comparative study of speciation ecology. Genetica 116:251–267. Geiselhardt, S., T. Otte, M. Hilker, and T. Turlings. 2012. Looking for a similar partner: host plants shape mating preferences of herbivorous insects by altering their contact pheromones. Ecol. Lett. 15:971–977. Gorur, G., C. Lomonaco, and A. Mackenzie. 2005. Phenotypic plasticity in host-plant specialisation in Aphis fabae. Ecol. Entomol. 30:657–664. Gould, K., and P. Wilson. 2015. Lack of evolution in a leaf beetle that lives on two contrasting host plants. Ecol. Evol. 5:3905–3913. Havens, J. A., and W. J. Etges. 2013. Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. IX. Host plant and population specific epicuticular hydrocarbon expression influences mate choice and sexual selection. J. Evol. Biol. 26:562–576. Hood, G. R., S. P. Egan, and J. L. Feder. 2012. Evidence for sexual isolation as a prezygotic barrier to gene flow between morphologically divergent species of Rhagoletis fruit flies. Ecol. Entomol. 37:521–528. Hou, M. L., W. Lin, and Y. Q. Han. 2009. Seasonal changes in supercooling points and glycerol content in overwintering larvae of the Asiatic rice borer from rice and water-oat plants. Environ. Entomol. 38:1182–1188. Hunter, M. D., and J. N. McNeil. 1997. Host-plant quality influences diapause and voltinism in a polyphagous insect herbivore. Ecology 78:977–986. Ishiguro, N., K. Yoshida, and K. Tsuchida. 2006. Genetic differences between rice and water-oat feeders in the rice stem borer, Chilo suppressalis (Walker) (Lepidoptera: Crambidae). Appl. Entomol. Zool. 41:585–593. Jiang, W. H., H. D. Li, X. F. Cheng, J. R. Ye, Y. B. Feng, and Z. J. Han. 2015. Study on host plants for reproduction of Chilo suppressalis. J. Asia Pac. Entomol. 18:591–595. Kanno, H. 1978. Mating behavior of the rice stem borer moth, Chilo suppressalis Walker (Lepidoptera: Pyralidae): I. Effects of moth age on mating activity. Appl. Entomol. Zool. 13:215–221. Kanno, H. 1980. Mating behavior of the rice stem borer moth, Chilo suppressalis Walker (Lepidoptera: Pyralidae): IV. Threshold-light-intensity for mating initiation under various temperatures. Appl. Entomol. Zool. 15:372–377. Konno, Y., and F. Tanaka. 1996. Mating time of the rice-feeding and water-oat-feeding strains of the rice stem borer, Chilo suppressalis (Walker) (Lepidoptera: Pyralidae). Jpn. J. Appl. Entomol. Zool. 40:245–247. Konno, Y., H. Honda, and Y. Matsumoto. 1981. Mechanisms of reproductive isolation between the fruit-feeding and the pinaceae-feeding types of the yellow peach moth, Dichocrocis punctiferalis Gueneé (Lepidoptera: Pyralidae). Jpn. J. Appl. Entomol. Zool. 25:253–258. Landolt, P. J., and T. W. Phillips. 1997. Host plant influences on sex pheromone behavior of phytophagous insects. Annu. Rev. Entomol. 42:371–391. Li, J., and D. Ó Foighil. 2012. Host-specific morphologies but no host races in the commensal bivalve Neaeromya rugifera. Invertebr. Biol. 131:197–203. Liu, Z. D., P. Y. Gong, K. J. Wu, W. Wei, J. H. Sun, and D. M. Li. 2007. Effects of larval host plants on over-wintering preparedness and survival of the cotton bollworm, Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae). J. Insect Physiol. 53:1016–1026. Maki, Y., and M. Yamashita. 1956. Ecological difference of rice stem borer, Chilo suppressalis Walker in the various host plants. Bull. Hyogo. Pref. Agric. Exp. Sta. 3:47–50. Matsukura, K., S. Hoshizaki, Y. Ishikawa, and S. Tatsuki. 2006. Morphometric differences between rice and water-oats population of the striped stem borer moth, Chilo suppressalis (Lepidoptera: Crambidae). Appl. Entomol. Zool. 41:529–535. Matsukura, K., S. Hoshizaki, Y. Ishikawa, and S. Tatsuki. 2009. Differences in timing of the emergence of the overwintering generation between rice and water-oats populations of the striped stem borer moth, Chilo suppressalis (Lepidoptera: Crambidae). Appl. Entomol. Zool. 44:485–489. Meng, F. X., K. M. Wu, and X. W. Gao. 2003. Evaluation of few-flower wildrice, chufa and rice as foods for rearing the striped stem borer, Chilo supperssalis. Entomol. Knowl. 40:469–472. Miyatake, T., A. Matsumoto, T. Matsuyama, H. R. Ueda, T. Toyosato, and T. Tanimura. 2002. The period gene and allochronic reproductive isolation in Bactrocera cucurbitae. Proc. Roy. Soc. B-Biol. Sci. 269:2467–2472. Monti, L., J. Génermont, C. Malosse, and B. Lalanne-Cassou. 1997. A genetic analysis of some components of reproductive isolation between two closely related species, Spodoptera latifascia (Walker) and S. descoinsi (Lalanne-Cassou and Silvain) (Lepidoptera: Noctuidae). J. Evol. Biol. 10:121–134. Nosil, P., B. J. Crespi, and C. P. Sandoval. 2002. Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature 417:440–443. Pashley, D. P., A. M. Hammond, and T. N. Hardy. 1992. Reproductive isolating mechanisms in fall armyworm host strains (Lepidoptera: Noctuidae). Ann. Entomol. Soc. Am. 85:400–405. Prokopy, R., S. Diehl, and S. Cooley. 1988. Behavioral evidence for host races in Rhagoletis pomonella flies. Oecologia 76:138–147. Qian, D. L., Y. L. Zheng, Q. G. Fan, H. Fang, Q. Lu, and G. C. Tao. 2007. Study on biological characteristics and occurrence regularity of striped stem borer from Zizania caduciflora habitats in north Zhejiang Province. Acta Agric. Jiangxi 19:57–59. Ragland, G. J., S. P. Egan, J. L. Feder, S. H. Berlocher, and D. A. Hahn. 2011. Developmental trajectories of gene expression reveal candidates for diapause termination: a key life-history transition in the apple maggot fly Rhagoletis pomonella. J. Exp. Biol. 214:3948–3960. Ragland, G. J., S. B. Sim, S. Goudarzi, J. L. Feder, and D. A. Hahn. 2012. Environmental interactions during host race formation: host fruit environment moderates a seasonal shift in phenology in host races of Rhagoletis pomonella. Funct. Ecol. 26:921–931. Sakai, T., and N. Ishida. 2001. Circadian rhythms of female mating activity governed by clock genes in Drosophila. Proc. Natl Acad. Sci. USA 98:9221–9225. Samudra, I. M., K. Emura, S. Hoshizaki, Y. Ishikawa, and S. Tatsuki. 2002. Temporal differences in mating behavior between rice- and water-oats-populations of the striped stem borer, Chilo suppressalis (Walker) (Lepidoptera: Crambidae). Appl. Entomol. Zool. 37:257–262. Sato, Y. 1964. A simple technique for mass rearing of the rice stem borer on rice seedlings. Jpn. J. Appl. Entomol. Zool. 8:6–10. Schöfl, G., D. G. Heckel, and A. T. Groot. 2009. Time-shifted reproductive behaviours among fall armyworm (Noctuidae: Spodoptera frugiperda) host strains: evidence for differing modes of inheritance. J. Evol. Biol. 22:1447–1459. Takasaki, T., M. Noda, and Z. Murata. 1969. Ecology of rice stem borer moth on Zizania latifolia. I. Occurrence of rice stem borer on Zizania latifolia. Proc. Assoc. Plant Prot. Kyusyu 15:118–121. Torres-Vila, L. M., and M. C. Rodríguez-Molina. 2013. Host plant-mediated reaction norms in the European grapevine moth: evidence for evolutionary host shift from daphne to vine. Arthropod Plant Interact. 7:125–136. Tsuchida, K., and H. Ichihashi. 1995. Estimation of monitoring range of sex pheromone trap for the rice stem borer moth, Chilo suppressalis (Walker) (Lepidoptera: Pyralidae) by male head width variation in relation to two host plants, rice and water oats. Appl. Entomol. Zool. 30:407–414. Ueno, H., S. Furukawa, and K. Tsuchida. 2006. Difference in the time of mating activity between host-associated populations of the rice stem borer, Chilo suppressalis (Walker). Entomol. Sci. 9:255–259. Via, S. 2001. Sympatric speciation in animals: the ugly duckling grows up. Trends Ecol. Evol. 16:381–390. Xiao, H. J., F. S. Xue, Y. Q. Liu, and X. F. Zhu. 2006. Comparison of photoperiodic response between rice- and water-oat-populations of Chilo suppressalis (Walker). Acta Entomol. Sin. 48:749–753. Yu, X. P., H. X. Xu, Z. X. Lu, J. M. Chen, X. S. Zheng, and L. Y. Tao. 2002. Differentiation of striped stem borer (SSB), Chilo suppressalis Walker from rice and Zizania caduciflora habitats. Acta Ecol. Sin. 22:341–345.