Register      Login
Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

Effects of larval diet quality on the growth and development of immature stages of Telostylinus angusticollis (Diptera : Neriidae)

Amy K. Hooper A and Russell Bonduriansky https://orcid.org/0000-0002-5786-6951 A B
+ Author Affiliations
- Author Affiliations

A School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia.

B Corresponding author. Email: r.bonduriansky@unsw.edu.au

Australian Journal of Zoology 66(6) 369-378 https://doi.org/10.1071/ZO19021
Submitted: 2 April 2019  Accepted: 16 September 2019   Published: 11 October 2019

Abstract

Nutrient abundance during development has profound effects on adult morphology, life history and behaviour in many insects, but effects of nutrition on juvenile development are less well known. We investigated how larval diet quality affects patterns of growth, development and survival of larvae and pupae in the neriid fly Telostylinus angusticollis (Enderlein). We reared flies on two larval diets varying in nutrient concentration (‘rich’ versus ‘poor’) that have been shown previously to affect a wide range of adult traits in this species. We found that nutrient concentration affected larval growth trajectories, with individuals reared on the rich diet exhibiting greatly accelerated growth and reaching a larger body size. By contrast, we found no evidence that diet affected timing of development at the pupal stage, suggesting that developmental constraints may prevent variation in pupal development rate. Although overall mortality during the immature stages was not affected by larval diet, we found some evidence that individuals reared on a poor diet might experience higher larval mortality, whereas individuals reared on a rich diet might experience higher mortality during emergence from the puparium. Our results enhance understanding of the effects of nutrition on growth, development, and life history.


References

Adler, M. I., Cassidy, E. J., Fricke, C., and Bonduriansky, R. (2013). The lifespan–reproduction trade-off under dietary restriction is sex-specific and context-dependent. Experimental Gerontology 48, 539–548.
The lifespan–reproduction trade-off under dietary restriction is sex-specific and context-dependent.Crossref | GoogleScholarGoogle Scholar | 23542072PubMed |

Adler, M. I., Telford, M., and Bonduriansky, R. (2016). Phenotypes optimized for early-life reproduction exhibit faster somatic deterioration with age, revealing a latent cost of high condition. Journal of Evolutionary Biology 29, 2436–2446.
Phenotypes optimized for early-life reproduction exhibit faster somatic deterioration with age, revealing a latent cost of high condition.Crossref | GoogleScholarGoogle Scholar | 27546615PubMed |

Ali, A., Luttrell, R. G., and Schneider, J. C. (1990). Effects of temperature and larval diet on development of the fall armyworm (Lepidoptera: Noctuidae). Annals of the Entomological Society of America 83, 725–733.
Effects of temperature and larval diet on development of the fall armyworm (Lepidoptera: Noctuidae).Crossref | GoogleScholarGoogle Scholar |

Alonso-Alvarez, C., Bertrand, S., Faivre, B., and Sorci, G. (2007). Increased susceptibility to oxidative damage as a cost of accelerated somatic growth in zebra finches. Functional Ecology 21, 873–879.
Increased susceptibility to oxidative damage as a cost of accelerated somatic growth in zebra finches.Crossref | GoogleScholarGoogle Scholar |

Arnqvist, G. (1994). The cost of male secondary sexual traits: developmental constraints during ontogeny in a sexually dimorphic water strider. American Naturalist 144, 119–132.
The cost of male secondary sexual traits: developmental constraints during ontogeny in a sexually dimorphic water strider.Crossref | GoogleScholarGoogle Scholar |

Awmack, C. S., and Leather, S. R. (2002). Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology 47, 817–844.
Host plant quality and fecundity in herbivorous insects.Crossref | GoogleScholarGoogle Scholar | 11729092PubMed |

Barros-Cordeiro, K. B., Pujol-Luz, J. R., and Name, K. P. O. (2016). Intra-puparial development of the Cochliomyia macellaria and Lucilia cuprina (Diptera, Calliphoridae). Entomologia 60, 334–340.

Bates, D., Maechler, M., Bolker, B., and Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |

Bentancourt, C. M., Scatoni, I. B., Gonzalez, A., and Franco, J. (2003). Effects of larval diet on the development and reproduction of Argyrotaenia sphaleropa (Meyrick) (Lepidoptera: Tortricidae). Neotropical Entomology 32, 551–557.
Effects of larval diet on the development and reproduction of Argyrotaenia sphaleropa (Meyrick) (Lepidoptera: Tortricidae).Crossref | GoogleScholarGoogle Scholar |

Berg, C. O. (1947). Biology and metamorphosis of some Solomon Islands Diptera. Part I: Micropezidae and Neriidae. Occasional Papers of the Museum of Zoology: University of Michigan 503:14.

Blanckenhorn, W. U. (2000). The evolution of body size: what keeps organisms small? The Quarterly Review of Biology 75, 385–407.
The evolution of body size: what keeps organisms small?Crossref | GoogleScholarGoogle Scholar | 11125698PubMed |

Boggs, C. L., and Freeman, K. D. (2005). Larval food limitation in butterflies: effects on adult resource allocation and fitness. Oecologia 144, 353–361.
Larval food limitation in butterflies: effects on adult resource allocation and fitness.Crossref | GoogleScholarGoogle Scholar | 15891831PubMed |

Boggs, C. L., and Niitepõld, K. (2016). Effects of larval dietary restriction on adult morphology, with implications for flight and life history. Entomologia Experimentalis et Applicata 159, 189–196.
Effects of larval dietary restriction on adult morphology, with implications for flight and life history.Crossref | GoogleScholarGoogle Scholar |

Bonduriansky, R. (2002). Leaping behaviour and responses to moisture and sound in larvae of piophilid carrion flies. Canadian Entomologist 134, 647–656.
Leaping behaviour and responses to moisture and sound in larvae of piophilid carrion flies.Crossref | GoogleScholarGoogle Scholar |

Bonduriansky, R. (2007). The evolution of condition-dependent sexual dimorphism. American Naturalist 169, 9–19.
The evolution of condition-dependent sexual dimorphism.Crossref | GoogleScholarGoogle Scholar | 17206580PubMed |

Bonduriansky, R., and Head, M. (2007). Maternal and paternal condition effects on offspring phenotype in Telostylinus angusticollis (Diptera: Neriidae). Journal of Evolutionary Biology 20, 2379–2388.
Maternal and paternal condition effects on offspring phenotype in Telostylinus angusticollis (Diptera: Neriidae).Crossref | GoogleScholarGoogle Scholar | 17956399PubMed |

Cassidy, E. J., Bath, E., Chenoweth, S. F., and Bonduriansky, R. (2014). Sex-specific patterns of morphological diversification: evolution of reaction norms and static allometries in neriid flies. Evolution 68, 368–383.
Sex-specific patterns of morphological diversification: evolution of reaction norms and static allometries in neriid flies.Crossref | GoogleScholarGoogle Scholar | 24111624PubMed |

Chapman, R. F. (1998). ‘The Insects: Structure and Function.’ (Cambridge University Press: Cambridge.)

Couret, J., Dotson, E., and Benedict, M. Q. (2014). Temperature, larval diet, and density effects on development rate and survival of Aedes aegypti (Diptera: Culicidae). PLoS One 9, e87468.
Temperature, larval diet, and density effects on development rate and survival of Aedes aegypti (Diptera: Culicidae).Crossref | GoogleScholarGoogle Scholar | 24498328PubMed |

Criscuolo, F., Monaghan, P., Nasir, L., and Metcalfe, N. B. (2008). Early nutrition and phenotypic development: ‘catch-up’ growth leads to elevated metabolic rate in adulthood. Proceedings of the Royal Society B: Biological Sciences 275, 1565–1570.
Early nutrition and phenotypic development: ‘catch-up’ growth leads to elevated metabolic rate in adulthood.Crossref | GoogleScholarGoogle Scholar | 18397870PubMed |

Davidowitz, G., and Nijhout, H. F. (2004). The physiological basis of reaction norms: the interaction among growth rate, the duration of growth and body size. Integrative and Comparative Biology 44, 443–449.
The physiological basis of reaction norms: the interaction among growth rate, the duration of growth and body size.Crossref | GoogleScholarGoogle Scholar | 21676730PubMed |

Denlinger, D. L., and Zdarek, J. (1994). Metamorphosis behavior of flies. Annual Review of Entomology 39, 243–266.
Metamorphosis behavior of flies.Crossref | GoogleScholarGoogle Scholar | 8135500PubMed |

Emlen, D. J. (2000). Integrating development with evolution: a case study with beetle horns. Bioscience 50, 403–418.
Integrating development with evolution: a case study with beetle horns.Crossref | GoogleScholarGoogle Scholar |

Fraenkel, G., and Bhaskaran, G. (1973). Pupariation and pupation in Cyclorrhaphous flies (Diptera): terminology and interpretation. Annals of the Entomological Society of America 66, 418–422.
Pupariation and pupation in Cyclorrhaphous flies (Diptera): terminology and interpretation.Crossref | GoogleScholarGoogle Scholar |

Fry, C. L. (2006). Juvenile hormone mediates a trade-off between primary and secondary sexual traits in stalk-eyed flies. Evolution & Development 8, 191–201.
Juvenile hormone mediates a trade-off between primary and secondary sexual traits in stalk-eyed flies.Crossref | GoogleScholarGoogle Scholar |

Heming, B. S. (2003). ‘Insect Development and Evolution.’ (Cornell University Press: New York.)

Hooper, A. K., Spagopoulou, F., Wylde, Z., Maklakov, A. A., and Bonduriansky, R. (2017). Ontogenetic timing as a condition-dependent life history trait: high-condition males develop quickly, peak early, and age fast. Evolution 71, 671–685.
Ontogenetic timing as a condition-dependent life history trait: high-condition males develop quickly, peak early, and age fast.Crossref | GoogleScholarGoogle Scholar | 28067402PubMed |

Hunt, J., and Simmons, W. L. (1997). Patterns of fluctuating asymmetry in beetle horns: an experimental examination of the honest signalling hypothesis. Behavioral Ecology and Sociobiology 41, 109–114.
Patterns of fluctuating asymmetry in beetle horns: an experimental examination of the honest signalling hypothesis.Crossref | GoogleScholarGoogle Scholar |

Hunt, J., Brooks, R., Jennions, M. D., Smith, M. J., Bentsen, C. L., and Bussiere, L. F. (2004). High-quality male field crickets invest heavily in sexual display but die young. Nature 432, 1024–1027.
High-quality male field crickets invest heavily in sexual display but die young.Crossref | GoogleScholarGoogle Scholar | 15616562PubMed |

James, A. C., and Partridge, L. (1995). Thermal evolution of rate of larval development in Drosophila melanogaster in laboratory and field populations. Journal of Evolutionary Biology 8, 315–330.
Thermal evolution of rate of larval development in Drosophila melanogaster in laboratory and field populations.Crossref | GoogleScholarGoogle Scholar |

Kaspi, R., Mossinson, S., Drezner, T., Kamensky, B., and Yuval, B. (2002). Effects of larval diet on development rates and reproductive maturation of male and female Mediterranean fruit flies. Physiological Entomology 27, 29–38.
Effects of larval diet on development rates and reproductive maturation of male and female Mediterranean fruit flies.Crossref | GoogleScholarGoogle Scholar |

Kingsolver, J. G., and Huey, R. B. (2008). Size, temperature, and fitness: three rules. Evolutionary Ecology Research 10, 251–268.

Klingenberg, C. P., and Nijhout, H. F. (1998). Competition among growing organs and developmental control of morphological asymmetry. Proceedings of the Royal Society of London. Series B, Biological Sciences 265, 1135–1139.
Competition among growing organs and developmental control of morphological asymmetry.Crossref | GoogleScholarGoogle Scholar |

Kuznetsova, A., Brockhoff, P. B., and Christensen, R. H. B. (2017). lmer test package: tests in linear mixed effects models. Journal of Statistical Software 82, 1–26.
lmer test package: tests in linear mixed effects models.Crossref | GoogleScholarGoogle Scholar |

Metcalfe, N. B., and Monaghan, P. (2003). Growth versus lifespan: perspectives from evolutionary ecology. Experimental Gerontology 38, 935–940.
Growth versus lifespan: perspectives from evolutionary ecology.Crossref | GoogleScholarGoogle Scholar | 12954479PubMed |

Moczek, A. P., and Nijhout, H. F. (2004). Trade‐offs during the development of primary and secondary sexual traits in a horned beetle. American Naturalist 163, 184–191.
Trade‐offs during the development of primary and secondary sexual traits in a horned beetle.Crossref | GoogleScholarGoogle Scholar | 14970921PubMed |

Nijhout, H. F. (1975). A threshold size for metamorphosis in the tobacco hornworm, Manduca sexta (L.). The Biological Bulletin 149, 214–225.
A threshold size for metamorphosis in the tobacco hornworm, Manduca sexta (L.).Crossref | GoogleScholarGoogle Scholar | 1138977PubMed |

Nijhout, H. F., and Emlen, D. J. (1998). Competition among body parts in the development and evolution of insect morphology. Proceedings of the National Academy of Sciences of the United States of America 95, 3685–3689.
Competition among body parts in the development and evolution of insect morphology.Crossref | GoogleScholarGoogle Scholar | 9520426PubMed |

Nijhout, H. F., and Williams, C. M. (1974). Control of moulting and metamorphosis in the tobacco hornworm, Manduca sexta (L.): growth of the last-instar larva and the decision to pupate. The Journal of Experimental Biology 61, 481–491.
| 4443740PubMed |

Nijhout, H. F., Roff, D. A., and Davidowitz, G. (2010). Conflicting processes in the evolution of body size and development time. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365, 567–575.
Conflicting processes in the evolution of body size and development time.Crossref | GoogleScholarGoogle Scholar | 20083633PubMed |

Olsen, L. E., and Ryckman, R. E. (1963). Studies on Odontoloxozus longicornis (Diptera: Neriidae). Part I. Life history and descriptions of immature stages. Annals of the Entomological Society of America 56, 454–469.
Studies on Odontoloxozus longicornis (Diptera: Neriidae). Part I. Life history and descriptions of immature stages.Crossref | GoogleScholarGoogle Scholar |

R Development Core Team (2008). R: a language and environment for statistical computing. R Foundation for Statistical computing, Vienna, Austria.

Raguso, R. A., Ojeda-Avila, T., Desai, S., Jurkiewicz, M. A., and Arthur Woods, H. (2007). The influence of larval diet on adult feeding behaviour in the tobacco hornworm moth, Manduca sexta. Journal of Insect Physiology 53, 923–932.
The influence of larval diet on adult feeding behaviour in the tobacco hornworm moth, Manduca sexta.Crossref | GoogleScholarGoogle Scholar | 17467729PubMed |

Robertson, C. W. (1936). The metamorphosis of Drosophila melanogaster, including an accurately timed account of the principal morphological changes. Journal of Morphology 59, 351–399.
The metamorphosis of Drosophila melanogaster, including an accurately timed account of the principal morphological changes.Crossref | GoogleScholarGoogle Scholar |

Robertson, F. W. (1963). The ecological genetics of growth in Drosophila. 6. The genetic correlation between the duration of the larval period and body size in relation to larval diet. Genetical Research 4, 74–92.
The ecological genetics of growth in Drosophila. 6. The genetic correlation between the duration of the larval period and body size in relation to larval diet.Crossref | GoogleScholarGoogle Scholar |

Schwab, D. B., Casasa, S., and Moczek, A. P. (2017). Evidence of developmental niche construction in dung beetles: effects on growth, scaling and reproductive success. Ecology Letters 20, 1353–1363.
Evidence of developmental niche construction in dung beetles: effects on growth, scaling and reproductive success.Crossref | GoogleScholarGoogle Scholar | 28942603PubMed |

Sentinella, A. T., Crean, A. J., and Bonduriansky, R. (2013). Dietary protein mediates a trade-off between larval survival and the development of male secondary sexual traits. Functional Ecology 27, 1134–1144.
Dietary protein mediates a trade-off between larval survival and the development of male secondary sexual traits.Crossref | GoogleScholarGoogle Scholar |

Shanower, T. G., Schulthess, F., and Bosque-Pérez, N. (1993). The effect of larval diet on the growth and development of Sesamia calamistis Hampson (Lepidoptera: Noctuidae) and Eldana Saccharina Walker (Lepidoptera: Pyralidae). International Journal of Tropical Insect Science 14, 681–685.
The effect of larval diet on the growth and development of Sesamia calamistis Hampson (Lepidoptera: Noctuidae) and Eldana Saccharina Walker (Lepidoptera: Pyralidae).Crossref | GoogleScholarGoogle Scholar |

Therneau, T. (2015). A package for survival analysis in S version 2.38. Available at: https://CRAN.R-project.org/package=survival

Tikkanen, O. P., Niemelä, P., and Keränen, J. (2000). Growth and development of a generalist insect herbivore, Operophtera brumata, on original and alternative host plants. Oecologia 122, 529–536.
Growth and development of a generalist insect herbivore, Operophtera brumata, on original and alternative host plants.Crossref | GoogleScholarGoogle Scholar | 28308346PubMed |

Tomkins, J. L., Kotiaho, J. S., and LeBas, N. R. (2005). Phenotypic plasticity in the developmental integration of morphological trade-offs and secondary sexual trait compensation. Proceedings of the Royal Society B: Biological Sciences 272, 543–551.
Phenotypic plasticity in the developmental integration of morphological trade-offs and secondary sexual trait compensation.Crossref | GoogleScholarGoogle Scholar | 15799950PubMed |

Valtonen, T. M., Kangassalo, K., Pölkki, M., and Rantala, M. J. (2012). Transgenerational effects of parental larval diet on offspring development time, adult body size and pathogen resistance in Drosophila melanogaster. PLoS One 7, e31611.
Transgenerational effects of parental larval diet on offspring development time, adult body size and pathogen resistance in Drosophila melanogaster.Crossref | GoogleScholarGoogle Scholar | 22359607PubMed |

Vijendravarma, R. K., Narasimha, S., and Kawecki, T. J. (2009). Effects of parental larval diet on egg size and offspring traits in Drosophila. Biology Letters 6, 238–241.
| 19875510PubMed |

Vinasco Mondragon, A. F., and Carrejo, N. S. G. (2016). Morphology and development rate of the immature stages of Glyphidops (Oncopsia) flavifrons (Bigot, 1886) (Diptera, Neriidae) under natural conditions. ZooKeys 603, 141–159.
Morphology and development rate of the immature stages of Glyphidops (Oncopsia) flavifrons (Bigot, 1886) (Diptera, Neriidae) under natural conditions.Crossref | GoogleScholarGoogle Scholar |

Wigglesworth, V. B. (1972). ‘The Principles of Insect Physiology.’ (Chapman and Hall: London.)

Ye, J., Dai, J., Li, J., Li, Z., Lu, Y., Han, S., and Zeng, L. (2015). Development and reproduction of Mallada basalis (Neuroptera: Chrysopidae) on artificial diets. The Florida Entomologist 98, 1072–1076.
Development and reproduction of Mallada basalis (Neuroptera: Chrysopidae) on artificial diets.Crossref | GoogleScholarGoogle Scholar |