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Inheritance of key life-history traits in crosses between northern and southern populations of the cabbage beetle Colaphellus bowringi (Coleoptera: Chrysomelidae)

Published online by Cambridge University Press:  15 February 2021

Hai-Min He Open the ORCID record for Hai-Min He [Opens in a new window] ,
Jian-Jun Tang ,
Li-Li Huang ,
Shao-Hui Wu ,
Yuan Peng  and
Fang-Sen Xue Open the ORCID record for Fang-Sen Xue [Opens in a new window]
Hai-Min He
Affiliation:
Institute of Entomology, Jiangxi Agricultural University, Nanchang, China
Jian-Jun Tang
Affiliation:
College of Computer and Information Engineering, Jiangxi Agricultural University, Nanchang, China
Li-Li Huang
Affiliation:
Department of Ecology and Environment, YuZhang Normal University, Nanchang, China
Shao-Hui Wu
Affiliation:
Department of Entomology, University of Georgia, Tifton, GA31793, USA
Yuan Peng
Affiliation:
College of Computer and Information Engineering, Jiangxi Agricultural University, Nanchang, China
Fang-Sen Xue*
Affiliation:
Institute of Entomology, Jiangxi Agricultural University, Nanchang, China
*
Author for correspondence: Fang-Sen Xue, Email: [email protected]
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Abstract

A southern population (S) from Xiushui County (29°1′N, 114°4′E) and a northern population (N) from Shenyang city (41°48′N, 123°23′E) of the cabbage beetle, Colaphellus bowringi vary greatly in their life-history traits, and may serve as an excellent model with which to study the inheritance of life-history traits. In the present study, we performed intraspecific hybridization using the two populations, comparing the key life-history traits (fecundity, development time, body weight, growth rate, and sexual size dimorphism (SDD)) between the two populations (S♀ × S♂ and N♀ × N♂) and their two hybrid populations (S♀ × N♂ and N♀ × S♂ populations) at 19, 22, 25, and 28°C. Our results showed that there were significant differences in life-history traits between the two parental populations, with the S population having a significantly higher fecundity, shorter larval development time, larger body weight, higher growth rate, and greater weight loss during metamorphosis than the N population at almost all temperatures. However, these life-history traits in the two hybrid populations were intermediate between those of their parents. The life-history traits in the S × N and N × S populations more closely resembled those of the maternal S population and N population, respectively, showing maternal effects. Weight loss for both sexes was highest in the S population, followed by the S × N, N × S, and N populations at all temperatures, suggesting that larger pupae lost more weight during metamorphosis. The changes in SSD with temperature were similar between the S and the S × N populations and between the N and the N × S populations, also suggesting a maternal effect. Overall, our results showed no drastic effect of hybridization on C. bowringi, being neither negative (hybrid inferiority) nor positive (heterosis). Rather, the phenotypes of hybrids were intermediate between the phenotypes of their parents.

Keywords

Body weightColaphellus bowringidevelopment timefecunditygrowth rateintraspecific hybridizationtemperature
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 4 , August 2021 , pp. 420 - 428
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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Footnotes

*

Both authors contributed equally to the work.

References

Andres, JA and Arnqvist, G (2001) Genetic divergence of the seminal signal–receptor system in houseflies: the footprints of sexually antagonistic coevolution? Proceeding of the Royal of Society B-biological Science 268, 399–405.CrossRefGoogle ScholarPubMed
Atkinson, D (1994) Temperature and organism size-a biological law for ectotherms? Advances in Ecological Research 25, 1–58.CrossRefGoogle Scholar
Attia, FA and Tregenza, T (2004) Divergence revealed by population crosses in the red flour beetle Tribolium castaneum. Evolutionary Ecology Research 6, 927–935.Google Scholar
Barton, NH (2001) The role of hybridization in evolution. Molecular Ecology 10, 551–568.CrossRefGoogle Scholar
Barton, M, Sunnucks, P, Norgate, M, Murray, N and Kearney, M (2014) Co-gradient variation in growth rate and development time of a broadly distributed butterfly. PLoS ONE 9, 1–8.CrossRefGoogle ScholarPubMed
Benvenuto, C, Cheyppe-Buchmann, S, Bermond, G, Ris, N and Fauvergue, X (2012 a) Intraspecific hybridization, life history strategies and potential invasion success in a parasitoid wasp. Evolutionary Ecology 26, 1311–1329.CrossRefGoogle Scholar
Benvenuto, C, Tabone, E, Vercken, E, Sorbier, N, Colombel, E, Warot, S, Fauvergue, X and Ris, N (2012 b) Intraspecific variability in the parasitoid wasp Trichogramma chilonis: can we predict the outcome of hybridization? Evolutionary Applications 5, 498–510.CrossRefGoogle ScholarPubMed
Bidau, CJ and Martía, DA (2007) Dichroplus vittatus (Orthoptera: Acrididae) follows the converse to Bergmann's rule although male morphological variability increases with latitude. Bulletin of Entomological Research 96, 69–79.CrossRefGoogle Scholar
Bieri, J and Kawecki, T (2003) Genetic architecture of differences between populations of cowpea weevil (Callosobruchus maculatus) evolved in the same environment. Evolution 57, 274–287.CrossRefGoogle ScholarPubMed
Burke, JM and Arnold, ML (2001) Genetics and the fitness of hybrids. Annual Review Genetics 35, 31–52.CrossRefGoogle ScholarPubMed
Cayol, JP, Coronado, P and Taher, M (2002) Sexual compatibility in medfly (Diptera: Tephritidae). Florida Entomologist 85, 51–57.CrossRefGoogle Scholar
Chen, C, Xiao, L, He, HM, Xu, J and Xue, FS (2014) A genetic analysis of diapause in crosses of a southern and a northern strain of the cabbage beetle Colaphellus bowringi (Coleoptera: Chrysomelidae). Bulletin of Entomological Research 104, 586–591.CrossRefGoogle Scholar
Chen, C, Yang, H, Xue, F and Xia, Q (2019) Geographical variation in life-history traits suggests an environmental-dependent trade-off between juvenile growth rate and adult lifespan in a moth. Bulletin of Entomological Research 109, 626–632.CrossRefGoogle Scholar
Chown, SL and Gaston, KJ (2010) Body size variation in insects: a macroecological perspective. Biological Reviews 85, 139–169.CrossRefGoogle ScholarPubMed
Fischer, K and Fiedler, K (2000) Sex-related differences in reaction norms in the butterfly Lycaena tityrus (Lepidoptera: Lycaenidae). Oikos 90, 372–380.CrossRefGoogle Scholar
Fu, DM, He, HM, Zou, C, Xiao, HJ and Xue, FS (2016) Life-history responses of the rice stem borer Chilo suppressalis to temperature change: breaking the temperature-size rule. Journal of Thermal Biology 61, 115–118.CrossRefGoogle ScholarPubMed
Ghosh, SM and Joshi, A (2012) Evolution of reproductive isolation as a by-product of divergent life-history evolution in laboratory populations of Drosophila melanogaster. Ecology and Evolution 21, 3214–3226.CrossRefGoogle Scholar
Gotthard, K, Nylin, S and Wiklund, C (1994) Adaptive variation in growth rate: life history costs and consequences in the speckled wood butterfly, Pararge aegeria. Oecologia 99, 281–289.CrossRefGoogle ScholarPubMed
He, HM, Xiao, HJ and Xue, FS (2018) Parental effect of diapause in relation to photoperiod and temperature in the cabbage beetle, Colaphellus bowringi (Coleoptera: Chrysomelidae). Bulletin of Entomological Research 108, 773–780.CrossRefGoogle Scholar
He, HM, Tang, JJ, Huang, LL, Gao, YL and Xue, FS (2019) Inter-geographic hybridization in the corn borer Ostrinia furnacalis reduced the fitness of hybrids. Journal of Pest Science 92, 1027–1037.CrossRefGoogle Scholar
Hosken, DJ, Blanckenhorn, WU and Garner, TWJ (2002) Heteropopulation males have a fertilization advantage during sperm competition in the yellow dung fly (Scathophaga stercoraria). Proceeding of the Royal of Society B-biological Science 269, 1701–1707.CrossRefGoogle Scholar
Hu, ZF, Yu, HC, Sun, WP and Xue, FS (2008) The developmental duration and biological characteristics of Colaphellus bowringi in Harbin. Chinese Bulletin of Entomology 45, 909–912, (in Chinese).Google Scholar
Iranipour, S, BenaMolaei, P, Asgari, S and Michaud, JP (2015) Reciprocal crosses between two populations of Trissolcus vassilievi (Mayr) (Hymenoptera: Scelionidae) reveal maternal effects on thermal phenotypes. Bulletin of Entomological Research 105, 355–363.CrossRefGoogle ScholarPubMed
Jennings, JH, Mazzi, D, Ritchie, MG and Hoikkala, A (2011) Sexual and postmating reproductive isolation between allopatric Drosophila montana populations suggest speciation potential. BMC Evolutionary Biology 11, 68.CrossRefGoogle ScholarPubMed
Kivelä, SM, Välimä, P, Carrasco, D, Maenpaa, MI and Oksanen, J (2011) Latitudinal insect body size clines revisited: a critical evaluation of the saw-tooth model. Journal of Animal Ecology 80, 1184–1195.CrossRefGoogle ScholarPubMed
Lai, XT, Yang, D, Wu, SH, Zhu, XF and Xue, FS (2008) Diapause incidence of progeny in relation to parental geographic origin, host plant and rearing density in the cabbage beetle, Colaphellus bowringi. Entomologia Experimentalis et Applicata 129, 117–123.CrossRefGoogle Scholar
Langor, DW, Spence, JR and Pohl, GR (1990) Host effects on fertility and productive success of Dendroctonus ponderosae Hopkins (Coleoptera: Scolytidae). Evolution 44, 609–618.CrossRefGoogle Scholar
Liu, XP, Tu, XY, He, HM, Chen, C and Xue, FS (2014) Comparison of sexual compatibility in crosses between the southern and northern populations of the cabbage beetle Colaphellus bowringi. Insect Science 21, 775–784.CrossRefGoogle ScholarPubMed
Lovich, JE and Gibbons, JW (1992) A review of techniques for quantifying sexual size dimorphism. Growth, Development and Aging 56, 269–281.Google ScholarPubMed
Masaki, S (1967) Geographic variation and climatic adaptation in a field cricket (Orthopetera Gryllidae). Evolution 21, 725–741.CrossRefGoogle Scholar
Nylin, S and Gotthard, K (1998) Plasticity in life-history traits. Annual Review Entomology 43, 63–83.CrossRefGoogle ScholarPubMed
Parsons, PA and Joern, A (2014) Life history traits associated with body size covary along a latitudinal gradient in a generalist grasshopper. Oecologia 174, 379–391.CrossRefGoogle Scholar
Roff, DA (1980) Optimizing development time in a seasonal environment: the ‘ups and downs’ of clinical variation. Oecologia 45, 202–208.CrossRefGoogle Scholar
Schug, MD, Baines, JF, Killon-Atwood, A, Mohanty, S, Das, A, Grath, S, Smith, SG, Zargham, S and Mcevey, SF (2008) Evolution of mating isolation between populations of Drosophila ananassae. Molecular Ecology 17, 2706–2721.CrossRefGoogle ScholarPubMed
Tang, J, He, H, Chen, C, Fu, S and Xue, F (2017) Latitudinal cogradient variation of development time and growth rate and a negative latitudinal body weight cline in a widely distributed cabbage beetle. PLoS ONE 12, e0181030.CrossRefGoogle Scholar
Taret, G, Sevilla, M, Wornoayporn, V, Islam, A, Ahmad, S, Caceres, C, Robinson, AS and Vreysen, MJB (2010) Mating compatibility among populations of codling moth Cydia pomonella Linnaeus (Lepidoptera: Tortricidae) from different geographic origins. Journal of Applied Entomology 134, 207–215.CrossRefGoogle Scholar
Tauber, MJ, Tauber, CA and Masaki, S (1986) Seasonal Adaptations of Insects. New York and Oxford: Oxford University Press.Google Scholar
Testa, ND, Ghosh, SM and Shingleton, AW (2013) Sex-specific weight loss mediates sexual size dimorphism in Drosophila melanogaster. PLoS ONE 8, e58936.CrossRefGoogle ScholarPubMed
Tsuchiya, Y, Takami, Y, Okuzaki, Y and Sota, T (2012) Genetic differences and phenotypic plasticity in body size between high- and low-altitude populations of the ground beetle Carabus tosanus. Journal of Evolutionary Biology 25, 1835–1842.CrossRefGoogle ScholarPubMed
Xiao, L, He, HM, Huang, LL, Geng, T, Fu, S and Xue, FS (2016) Variation of life-history traits of the Asian corn borer, Ostrinia furnacalis in relation to temperature and geographical latitude. Ecology and Evolution 6, 5129–5143.CrossRefGoogle ScholarPubMed
Xue, FS, Li, AQ, Zhu, XF, Gui, AL, Jiang, PL and Liu, XF (2002 a) Diversity in life history of the leaf beetle, Colaphellus bowringi Baly. Acta Entomologica Sinica 45, 494–498.Google Scholar
Xue, FS, Spieth, HR, Li, AQ and Hua, A (2002 b) The role of photoperiod and temperature in determination of summer and winter diapause in the cabbage beetle, Colaphellus bowringi (Coleoptera: Chrysomelidae). Journal of Insect Physiology 48, 279–286.CrossRefGoogle Scholar
Zhang, SM and Zhao, YX (1996) Geographical Distribution of Agricultural and Forestry Insects in China. Beijing: China Agricultural Press, pp.168–169, (in Chinese).Google Scholar
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