Abstract
Flexibility and variations in morphological and physiological traits are the key for insect herbivores to adapt to environments. The cotton–melon aphid Aphis gossypii Glover is a polyphagous insect which populations exhibit host specialization. Feeding experience on specific host plants converted host specialization in this aphid. However, adaptive changes of this aphids during the host conversion are still unclear. Here, we examined variations in body length, leg segments, and host preference of the cotton-specialized and cucurbit-specialized aphids, A. gossypii, induced by novel host plants. We found that on the original host plants, body, femur, tibia, and tarsus of the cucurbit-specialized aphids were significantly longer than these of the cotton-specialized aphids. However, feeding on zucchini or cowpea resulted in the short body and leg segments in the cucurbit-specialized aphids, whereas led to the long body and leg segments or no changes in the cotton-specialized aphids, and consequently, the tarsus lengths became equal between the cotton- and cucurbit-specialized aphids. Interestingly, the change trends of the relative lengths of leg segments to body length with the increase of reared generation on zucchini were almost different between the cucurbit-specialized and cotton-specialized aphids, especially the relative length of tarsus, but on cowpea, the trends were similar. Meanwhile, feeding on zucchini altered host preference of the cotton-specialized aphids, but not of the cucurbit-specialized aphids. Novel host plants induce adaptive changes in leg segments and host preference of aphids, suggesting the conversion of host specialization.
Similar content being viewed by others
References
Agarwala BK, Choudhury PR (2013) Host races of the cotton aphid, Aphis gossypii, in asexual populations from wild plants of taro and brinjal. J Insect Sci 13:34
Bhadra P, Agarwala BK (2012) On the morphological and genotypic variations of two congeneric species of banana aphid Pentalonia (Homoptera: Aphididae) from India. Adv Life Sci 2(3):75–81
Blackman RL, Eastop VF (2000) Aphids on the world’s crops. Wiley, New York
Blount JL, Buntin GD, Sparks AN Jr (2015) Host preference of Megacopta cribraria (Hemiptera: Plataspidae) on selected edible beans and soybean. J Econ Entomol 108(3):1094–1105
Braendle C, Davis GK, Brisson JA, Stern DL (2006) Wing dimorphism in aphids. Heredity 97:192–199
Brisson JA, Ishiawa A, Miura T (2010) Wing development genes of the pea aphid and differential gene expression between winged and unwinged morphs. Insect Mol Biol 19:63–73
Broberg CL, Borden JH (2005) Host preference by Saperda calcarata Say (Coleoptera: Cerambycidae). J Entomol Soc Br 102:27–34
Carroll SP, Boyd C (1992) Host race radiation in the soapberry bug: natural history with the history. Evolution 46:1052–1069
Collar DC, Schulter JA II, Losos JB (2011) Evolution of extreme body size disparity in monitor lizards (Varanus). Evolution 65:2664–2680
Denno RF, Roderick GK (1990) Population biology of planthoppers. Annu Rev Entomol 35:489–520
Dixon AFG (1998) Aphid Ecology. Chapman & Hall, London
Fang Y, Qiao GX, Zhang GX (2011) Morphological adaptation of aphid species on different host plant leaves. Acta Entomol Sin 54:157–178
Friedemann K, Kunert G, Gorb E, Gorb SN, Beutel RG (2015) Attachment foreces of pea aphids (Acyrthosiphon pisum) on different legume species. Ecol Entomol 40:732–740
Fuller SJ, Chavigny P, Lapchin L, Vanlerberghe-Masutti F (1999) Variation in clonal diversity in glasshouse infestations of the aphid, Aphis gossypii Glover in southern France. Mol Ecol 8:1867–1877
Gong L, Cui F, Sheng C, Lin Z, Reeck G, Xu J, Kang L (2012) Polymorphism and methylation of four genes expressed in salivary glands of Russian wheat aphid (Homoptera: Aphididae). J Econ Entomol 105:232–241
Kelly SA, Panhuis TM, Stoehr AM (2012) Phenotypic plasticity: molecular mechanisms and adaptive significance. Compr Physiol 2:1417–1439
Kong XQ, Liu JL, Zhang WJ, Qu YD (2015) Load-bearing ability of the mosquito tarsus on water surfaces arising from its flexibility. AIP Adv 5:037101
Liu XD, Zhang XX, Zhao NS, Yang XW, Chen XF, Zhang GX (2000) Ecological adaptation of Aphis gossypii (Homoptera: Aphididae) to cotton development stage and temperature. J Nanjing Agric Univ 23:29–32
Liu XD, Zhai BP, Zhang XX, Lu Y (2004) Differentiation in morphometrics and ecological adaptation of cotton and cucumber biotypes of the cotton aphid, Aphis gossypii (Homoptera: Aphididae). Acta Entomol Sin 47:768–773
Liu XD, Zhai BP, Zhang XX (2008) Specialized host plant performance of the cotton aphid is altered by experience. Ecol Res 23:919–925
Liu XD, Xu TT, Lei HX (2017) Refuges and host shift pathways of host-specialized aphids Aphis gossypii. Sci Rep 7:2008
Lombaert E, Carletto J, Piotte C, Fauvergue X, Lecoq H, Vanlerberghe-Masutti F, Lapchin L (2009) Response of the melon aphid, Aphis gossypii, to host-plant resistance: evidence for high adaptive potential despite low genetic variability. Entomol Exp Appl 133:46–56
Ma L, Li MY, Chang CY, Chen FF, Hu Y, Liu XD (2019) The host range of Aphis gossypii is dependent on aphid genetic background and feeding experience. PeerJ 7:e7774
Meng X, Hu J, Li Y, Dai J, Guo M, Ouyang G (2018) The preference choices of Conopomorpha sinensis Bradley (Lepidoptera: Gracilariidae) for litchi based on its host surface characteristics and volatiles. Sci Rep 8:2013
Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692
Mondor EB, Tremblay MN, Messing RH (2007) Morphological and ecological traits promoting aphid colonization of the Hawaiian Islands. Biol Invasions 9:87–100
Murdie G (1969) Some causes of size variation in the pea aphid, Acyrthosiphon pisum Harris. Trans R Entomol Soc Lond 121:423–442
Newby BD, Etges WJ (1998) Host preference among populations of Drosophila mojavensis (Diptera: Drosophilidae) that use different host cacti. J Insect Behav 11(5):691–712
Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F, van Kleunen M (2010) Plant phenotypic plasticity in a changing climate. Trends Plant Sci 15:684–692
Peppe FB, Lomônaco C (2003) Phenotypic plasticity of Myzus persicae (Hemiptera: Aphididae) raised on Brassica oleracea L. var. acephala (kale) and Raphanus sativus L. (radish). Genet and Mole Biol 26:189–194
Powell G, Maniar SP, Pickett JA, Hardie J (1999) Aphid responses to non-host epicuticular lipids. Entomol Exp Appl 91:115–123
Powell G, Tosh CR, Hardie J (2006) Host plant selection by aphids: behavioral, evolutionary and applied perspectives. Annu Rev Entomol 51:309–330
Richardson ML, Lagos DM, Mitchell RF, Hartman GL, Voegtlin DJ (2011) Life history and morphological plasticity of the soybean aphid, Aphis glycines. Entomol Exp Appl 140:139–145
Ruiz-Montoya L, Nùnez-Farfán J (2013) Testing local host adaptation and phenotypic plasticity in a herbivore when alternative related host plants occur sympatrically. PLoS ONE 8:e79070
Ruiz-Montoya L, Nùnez-Farfán J, Dominguez CA (2005) Changes in morphological traits of the cabbage aphid (Brevicoryne brassicae) associated with the use of different host plants. Ecol Res 20:591–598
Santana AFK, Zucoloto FS (2011) Influence of previous experience on the preference, food utilization and performance of Ascia monuste orseis wild larvae (Godart) (Lepidoptera: Pieridae) for three different hosts. Neotrop Entomol 40:631–638
Sarria E, Palomares-Rius FJ, Lopez-Sese AI, Heredia A, Gomez-Guillamon ML (2010) Role of leaf glandular trichomes of melon plants in deterrence of Aphis gossypii Glover. Plant Biol 12:503–511
Satar S, Kersting U, Yokomi R (2013) Presence of two host races of Aphis gossypii Glover (Hemiptera: Aphididae) collected in Turkey. Ann Appl Biol 162:41–49
Sylla S, Brevault T, Monticelli LS, Diarra K, Desneux N (2019) Geographic variation of host preference by the invasive tomato leaf miner Tuta absoluta: implications for host range expansion. J Pest Sci. https://doi.org/10.1007/s10340-019-01094-9
Tian PP, Chang CY, Miao NH, Li MY, Liu XD (2019) Infections with Arsenophonus facultative endosymbionts alter performance of aphids (Aphis gossypii) on an amino-acid deficient diet. Appl Environ Microbiol 85:e01407–e1419
Vanlerberghe-Masutti F, Chavigny P (1998) Host-based genetic differentiation in the aphid Aphis gossypii Glover, evidenced from RAPD fingerprints. Mol Ecol 7:905–914
Vanlerberghe-Masutti F, Chavigny P, Fuller SJ (1999) Characterization of microsatellite loci in the aphid species Aphis gossypii Glover. Mol Ecol 8:693–695
Vucetic A, Petrovic-obradovic O, Stanisavljevic LZ (2010) The morphological vaiation of Myzus persicae (Hemiptera: Aphididae) from peach and tobacco in Serbia and Montenegro. Arch Biol Sci 62(3):767–774
West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20:249–278
Wool D, Hales DF (1997) Phenotypic plasticity in Australian cotton aphid (Homoptera: Aphididae): host plant effects on morphological variation. Ann Entomol Soc Am 90:316–328
Wu W, Liang XL, Zhao HY, Xu TT, Liu XD (2013) Special plant species determines diet breadth of phytophagous insects: a study on host plant expansion of the host-specialized Aphis gossypii Glover. PLoS ONE 8:e60832
Xu TT, Ma TT, Liu XD (2014) How does the host-specialized aphid deal with food deficiency? Insect Sci 21:334–341
Yang LH (2000) Effects of body size and plant structure on the movement ability of a predaceous stinkbug, Podisus maculiventris (Heteroptera: Pentatomidae). Oecologia 125:85–90
Yeh PJ, Price TD (2004) Adaptive phenotypic plasticity and the successful colonization of a novel environment. Am Nat 164:531–542
Zhang S, Luo JY, Wang L, Wang CT, Lv LM, Zhang LJ, Zhu XZ, Cui JJ (2018) The biotypes and host shifts of cotton–melon aphids Aphis gossypii in northern China. J Integr Agric 17:2066–2073
Acknowledgements
We would like to thank Wei Wu for help with the host choice experiment. This study was supported by the National Natural Science Foundation of China (31672034, 31070377).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by XDL and LM. The first draft of the manuscript was written by XDL and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Handling editor: Stanislav Gorb.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ma, L., Liu, XD. Adaptive changes in morph and preference induced by novel host plants mediate host specialization of the cotton–melon aphid. Arthropod-Plant Interactions 14, 453–462 (2020). https://doi.org/10.1007/s11829-020-09756-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-020-09756-7