Hostname: page-component-84b7d79bbc-tsvsl Total loading time: 0 Render date: 2024-07-30T17:15:06.025Z Has data issue: false hasContentIssue false
  • English
  • Français

The transgenerational consequences of maternal parasitism for aphid life history and suitability for subsequent parasitism

Published online by Cambridge University Press:  12 July 2021

A. Rasekh ,
M. R. Shahbazi-Gahrouhi  and
J. P. Michaud Open the ORCID record for J. P. Michaud [Opens in a new window]
A. Rasekh
Affiliation:
Department of Plant Protection, College of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran
M. R. Shahbazi-Gahrouhi
Affiliation:
Department of Plant Protection, College of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran
J. P. Michaud*
Affiliation:
Department of Entomology, Kansas State University, Agricultural Research Center-Hays, Hays, KS67601, USA
*
Author for correspondence: J. P. Michaud, Email: jpmi@ksu.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Aphids parasitized in later instars can give birth to several nymphs before their reproduction is curtailed by the developing parasitoid. We examined the life histories of Aphis fabae Scopoli born to mothers parasitized by Lysiphlebus fabarum Marshall, and their suitability as subsequent hosts, to test the ‘fecundity compensation’ hypothesis. Maternal parasitism negatively impacted life history parameters, resulting in reduced estimates of population increase (rm, R0, and λ), and increased generation time (GT) and doubling time (DT). These impacts were greater when the larva developing in the mother turned out to be female rather than male, and greater still when mothers were superparasitized. Maternal parasitism produced aphids with shorter hind tibia (HTL), at birth and at maturity, but their developmental time was unaffected. Although female L. fabarum readily accepted such aphids for oviposition, rates of mummification and wasp emergence were lower, and more so when the maternal parasitoid was female. The resulting parasitoids took longer to develop than progeny from control wasps, had shorter HTLs, lower egg loads, smaller eggs, and produced fewer mummies with lower rates of adult emergence, all differences that were more pronounced when the maternal parasitoid was female. The progeny of these wasps exhibited similar impairments to these biological parameters as their parents, demonstrating that the negative impacts of development in maternally parasitized hosts extended for at least two generations. Thus, our results do not support fecundity compensation, but suggest that any benefits of post-parasitism reproduction will be offset by reduced fitness in both aphid progeny and the parasitoids that develop in them.

Keywords

Aphis fabaehost suitabilitylife historyLysiphlebus fabarummaternal effects
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 1 , February 2022 , pp. 51 - 57
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ameri, M, Rasekh, A and Michaud, JP (2014) Body size affects host defensive behavior and progeny fitness in a parasitoid wasp, Lysiphlebus fabarum Marshall (Hymenoptera: Braconidae). Entomologia Experimentalis et Applicata 150, 259–268.CrossRefGoogle Scholar
Barribeau, SM, Sik, D and Gerardo, NM (2010) Aphid reproductive investment in response to mortality risks. BMC Evolutionary Ecology 10, 210.Google ScholarPubMed
Bayoumy, MH, Ramaswamy, P and Michaud, JP (2015) Comparative life histories of greenbugs and sugarcane aphids (Hemiptera: Aphididae) coinfesting susceptible and resistant sorghums. Journal of Economic Entomology 109, 385–391.CrossRefGoogle ScholarPubMed
Carey, JR (1993) Applied Demography for Biologists. New York, NY: Oxford University Press.Google Scholar
Casanovas, P, Goldson, SL and Tylianakis, JM (2018) Asymmetry in reproduction strategies drives evolution of resistance in biological control systems. PLoS ONE 13, e0207610.CrossRefGoogle ScholarPubMed
Charnov, EL (1982) The Theory of Sex Allocation. Princeton, NJ, USA: Princeton Univ. Press.Google ScholarPubMed
Chown, SL and Gaston, KJ (2010) Body size variation in insects: a macroecological perspective. Biological Reviews 85, 139–169.CrossRefGoogle ScholarPubMed
Crawley, MJ (1993) GLIM for Ecologists. Oxford, UK: Blackwell Scientific.Google Scholar
Cutler, C (2013) Insects, insecticides and hormesis: evidence and considerations for study. Dose-Response 11, 154–177.CrossRefGoogle ScholarPubMed
Dahlman, DL and Vinson, SB (1993) Teratocytes: developmental and biochemical characteristics. In Beckage, NE, Thompson, SN and Federici, BA (eds), Parasites and Pathogens of Insects. San Diego, CA, USA: Academic Press, pp. 145–165.CrossRefGoogle Scholar
Digilio, MC, Isidoro, N, Tremblay, E and Pennacchio, F (2000) Host castration by Aphidius ervi venom proteins. Journal of Insect Physiology 46, 1041–1050.CrossRefGoogle ScholarPubMed
Dupas, S, Carton, Y and Poirie, M (2003) Genetic dimension of the coevolution of virulence-resistance in Drosophila – parasitoid wasp relationships. Heredity 90, 84–89.CrossRefGoogle ScholarPubMed
English-Loeb, GM, Karban, R and Brody, AK (1990) Arctiid larvae survive attack by a tachinid parasitoid and produce viable offspring. Ecological Entomology 15, 361–362.CrossRefGoogle Scholar
Fairbairn, DJ (1997) Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annual Review of Ecology and Systematics 28, 659–687.CrossRefGoogle Scholar
Falabella, P, Tremblay, E and Pennacchio, F (2000) Host regulation by the aphid parasitoid Aphidius ervi: the role of teratocytes. Entomologia Experimentalis et Applicata 9, 1–9.CrossRefGoogle Scholar
Godfray, HCJ (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton, NJ: Princeton University Press.CrossRefGoogle Scholar
Guedes, RNC and Cutler, C (2013) Insecticide-induced hormesis and arthropod pest management. Journal of Pest Science 70, 690–697.Google ScholarPubMed
Kaiser, MC and Heimpel, GE (2016) Parasitoid-induced transgenerational fecundity compensation in an aphid. Entomologia Experimentalis et Applicata 159, 197–206.CrossRefGoogle Scholar
Leventhal, GE, Dunner, RP and Barribeau, SM (2014) Delayed virulence and limited costs promote fecundity compensation upon infection. American Naturalist 183, 480–493.CrossRefGoogle ScholarPubMed
Li, S, Falabella, P, Giannantonio, S, Fanti, P, Battaglia, D, Digilio, MC, Volkl, W, Sloggett, JJ, Weisser, W and Pennacchio, F (2002) Pea aphid clonal resistance to the endophagous parasitoid Aphidius ervi. Journal of Insect Physiology 48, 971–980.CrossRefGoogle Scholar
Mackauer, M (1983) Quantitative assessment of Aphidius smithi (Hymenoptera: Aphidiidae): fecundity, intrinsic rate of increase, and functional response. Canadian Entomologist 115, 399–415.CrossRefGoogle Scholar
Mackauer, M (1986) Growth and developmental interactions in aphids and some of their hymenopteran parasites. Journal of Insect Physiology 32, 278–280.CrossRefGoogle Scholar
Mackauer, M and Kambhampati, S (1984) Reproduction and longevity of cabbage aphid, Brevicoryne brassicae (Homoptera: Aphididae), parasitized by Diaeretiella rapae (Hymenoptera: Aphidiidae). Canadian Entomologist 116, 1605–1610.CrossRefGoogle Scholar
McLean, AHC and Parker, BJ (2020) Variation in intrinsic resistance of pea aphids to parasitoid wasps: a transcriptomic basis. PLoS ONE 15, e0242159.CrossRefGoogle ScholarPubMed
Michaud, JP (2012) Coccinellids in Biological Control. In Hodek, I, van Emden, HF and Honěk, A (eds), Ecology and Behaviour of the Ladybird Beetles (Coccinellidae). (John Wiley & Sons, Ltd), pp. 488–519. https://doi.org/10.1002/9781118223208.ch11CrossRefGoogle Scholar
Najafpour, P, Rasekh, A and Esfandiari, M (2018) Maternal rearing condition and age affect progeny fitness in the parasitoid wasp Lysiphlebus fabarum. Entomologia Experimentalis et Applicata 166, 24–31.CrossRefGoogle Scholar
Pennacchio, F and Mancini, D (2012) Aphid parasitoid venom and its role in host regulation. In Beckage, NE and Drezen, J-M (eds), Parasitoid Viruses: Symbionts and Pathogens. London, UK: Academic Press, pp. 247–254.CrossRefGoogle Scholar
Pennacchio, F, Diglio, MC and Tremblay, E (1995) Biochemical and metabolic alterations in Acyrthosiphon pisum parasitized by Aphidius ervi. Archives of Insect Biochemistry and Physiology 30, 351–367.CrossRefGoogle Scholar
Rakhshani, E, Talebi, AA, Kavallieratos, NG, Rezwani, A, Manzari, S and Tomanovic, Z (2005) Parasitoid complex (Hymenoptera, Braconidae, Aphidiinae) of Aphis craccivora Koch (Hemiptera: Aphidoidea) in Iran. Journal of Pest Science 78, 193–198.CrossRefGoogle Scholar
Rakhshani, E, Stary, P and Tomanovic, Z (2013) Tritrophic associations and taxonomic notes on Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae: Aphidiinae), a keystone aphid parasitoid in Iran. Archives of Biological Sciences 65, 667–680.CrossRefGoogle Scholar
Rasekh, A, Michaud, JP, Allahyari, H and Sabahi, Q (2010a) The foraging behavior of Lysiphlebus fabarum (Marshall), a thelytokous parasitoid of the black bean aphid in Iran. Journal of Insect Behavior 23, 165–179.CrossRefGoogle Scholar
Rasekh, A, Michaud, JP, Kharazi-Pakdel, A and Allahyari, H (2010b) Ant mimicry by an aphid parasitoid, Lysiphlebus fabarum (Marshall) (Hymenoptera: Aphidiidae). Journal of Insect Science 10, #126.CrossRefGoogle Scholar
Rasekh, A, Kharazi, PA, Michaud, JP, Allahyari, H and Rakhshani, E (2011) Report of a thelytokous population of Lysiphlebus fabarum (Hym.: Aphidiidae) from Iran. Journal of the Entomological Society of Iran 30, 83–84.Google Scholar
Sabri, A, Hance, T, Leroy, PD, Frere, I, Haubruge, E, Destain, J, Compere, P and Thonart, P (2011) Placenta-like structure of the aphid endoparasitic wasp Aphidius ervi: a strategy of optimal resources acquisition. PLoS One 6(4), e18847.CrossRefGoogle ScholarPubMed
Sequeira, R and Mackauer, M (1988) Effects of parasitism by Praon pequodorum on age-specific fecundity and population growth of the pea aphid, Acyrthosiphon pisum. Entomologia Experimentalis et Applicata 48, 179–185.CrossRefGoogle Scholar
Southwood, TRE and Henderson, PA (2000) Ecological Methods, 3rd edition. Blackwell Scientific.Google Scholar
SPSS Inc (1998) SPSS 8.0 for Windows. Prentice Hall, NJ: SPSS Inc.Google Scholar
Stary, P (1986) Specificity of parasitoids (Hymenoptera: Aphidiidae) to the black bean aphid Aphis fabae complex in agrosystems. Acta Entomologica Bohemoslovaca 83, 24–29.Google Scholar
Volkl, W (1992) Aphids or their parasitoids: who actually benefits from ant attendance? Journal of Animal Ecology 61, 273–281.CrossRefGoogle Scholar
Volkl, W and Stechmann, DH (1998) Parasitism of the black bean aphid (Aphis fabae) by Lysiphlebus fabarum (Hym., Aphidiidae): the influence of host plant and habitat. Journal of Applied Entomology 122, 201–206.CrossRefGoogle Scholar
Vorburger, C and Perlman, SJ (2018) The role of defensive symbionts in host-parasite coevolution. Biological Reviews 93, 1747–1764.CrossRefGoogle ScholarPubMed
Weisser, WW and Volkl, W (1997) Dispersal in the aphid parasitoid, Lysiphlebus cardui (Marshall) (Hymenoptera: Aphidiidae). Journal of Applied Entomology 121, 23–28.CrossRefGoogle Scholar