Exoskeleton ageing and its relation to longevity and fecundity in female Australian leaf insects (Phyllium monteithi)
Russell Bonduriansky
A * and Caitlin Creak A
+ Author Affiliations
- Author Affiliations
A Evolution & Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia.
Australian Journal of Zoology 69(4) 158-165 https://doi.org/10.1071/ZO21052
Submitted: 10 December 2021 Accepted: 6 April 2022 Published: 13 May 2022
© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Senescence is a decline in reproduction and survival rate with advancing age resulting from deterioration of somatic tissues and systems throughout the body. Age-related somatic changes (somatic ageing) have been studied extensively in vertebrates but are less well known in other animals, including insects. Since adult insects have very limited ability to repair their exoskeleton, somatic ageing could involve deterioration and discolouration of the cuticle. We investigated age-related changes in wing pigmentation and abdominal cuticle necrosis in females of the Australian leaf insect Phyllium monteithi. Adult females varied markedly in the extent and pattern of pigmentation on their bodies, and we found that pigment spots on the forewings increased in size with age in most individuals. As females aged, most individuals also exhibited increasing levels of abdominal cuticle necrosis, resulting in the loss of abdominal cuticle along the margin of the abdomen. Neither the extent of pigmentation nor cuticle loss were clearly associated with reduced fecundity or longevity in the protected laboratory environment, but it remains unknown whether these age-related changes have functional implications in the wild. Our results show that the P. monteithi exoskeleton undergoes complex changes with age, with potential implications for functional traits and fitness.
Keywords: cuticle, exoskeleton, fecundity, longevity, necrosis, Phasmatodea, Phillium monteithi, senescence.
References
Adler, MI, 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 |
Baker, GT (1976). Insect flight muscle: maturation and senescence. Gerontology 22, 334–361.
| Insect flight muscle: maturation and senescence.Crossref | GoogleScholarGoogle Scholar | 1269938PubMed |
Barek, H, Sugumaran, M, Ito, S, and Wakamatsu, K (2018). Insect cuticular melanins are distinctly different from those of mammalian epidermal melanins. Pigment Cell & Melanoma Research 31, 384–392.
| Insect cuticular melanins are distinctly different from those of mammalian epidermal melanins.Crossref | GoogleScholarGoogle Scholar |
Bates, D, Mächler, 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 |
Beramendi, A, Peron, S, Casanova, G, Reggiani, C, and Cantera, R (2007). Neuromuscular junction in abdominal muscles of Drosophila melanogaster during adulthood and aging. The Journal of Comparative Neurology 501, 498–508.
| Neuromuscular junction in abdominal muscles of Drosophila melanogaster during adulthood and aging.Crossref | GoogleScholarGoogle Scholar | 17278125PubMed |
Brock, PD, and Hasenpusch, J (2002). Studies on the leaf insects (Phasmida: Phylliidae) of Australia. Journal of Orthoptera Research 11, 199–205.
| Studies on the leaf insects (Phasmida: Phylliidae) of Australia.Crossref | GoogleScholarGoogle Scholar |
Cartar, RV (1992). Morphological senescence and longevity: an experiment relating wing wear and life span in foraging wild bumble bees. Journal of Animal Ecology 61, 225–231.
| Morphological senescence and longevity: an experiment relating wing wear and life span in foraging wild bumble bees.Crossref | GoogleScholarGoogle Scholar |
Cortot, J, Farine, J-P, Ferveur, J-F, and Everaerts, C (2022). Aging-related variation of cuticular hydrocarbons in wild type and variant Drosophila melanogaster. Journal of Chemical Ecology 48, 152–164.
| Aging-related variation of cuticular hydrocarbons in wild type and variant Drosophila melanogaster.Crossref | GoogleScholarGoogle Scholar | 35022940PubMed |
Dell’Aglio, DD, Akkaynak, D, McMillan, WO, and Jiggins, CD (2017). Estimating the age of Heliconius butterflies from calibrated photographs. PeerJ 5, e3821.
| Estimating the age of Heliconius butterflies from calibrated photographs.Crossref | GoogleScholarGoogle Scholar |
Douglas, AE (2015). Multiorganismal insects: diversity and function of resident microorganisms. Annual Review of Entomology 60, 17–34.
| Multiorganismal insects: diversity and function of resident microorganisms.Crossref | GoogleScholarGoogle Scholar | 25341109PubMed |
Finch CE (1994) ‘Longevity, Senescence, and the Genome.’ (University of Chicago Press: Chicago, IL, USA)
Hartmann, C, Heinze, J, and Bernadou, A (2019). Age-dependent changes in cuticular color and pteridine levels in a clonal ant. Journal of Insect Physiology 118, 103943.
| Age-dependent changes in cuticular color and pteridine levels in a clonal ant.Crossref | GoogleScholarGoogle Scholar | 31518554PubMed |
Hawkins, GL, Hill, GE, and Mercadante, A (2012). Delayed plumage maturation and delayed reproductive investment in birds. Biological Reviews 87, 257–274.
| Delayed plumage maturation and delayed reproductive investment in birds.Crossref | GoogleScholarGoogle Scholar | 21790949PubMed |
Ishibashi, JR, Taslim, TH, and Ruohola-Baker, H (2020). Germline stem cell aging in the Drosophila ovary. Current Opinion in Insect Science 37, 57–62.
| Germline stem cell aging in the Drosophila ovary.Crossref | GoogleScholarGoogle Scholar | 32120010PubMed |
Jones, OR, Scheuerlein, A, Salguero-Gómez, R, Camarda, CG, Schaible, R, Casper, BB, Dahlgren, JP, Ehrlén, J, García, MB, Menges, ES, Quintana-Ascencio, PF, Caswell, H, Baudisch, A, and Vaupel, JW (2014). Diversity of ageing across the tree of life. Nature 505, 169–173.
| Diversity of ageing across the tree of life.Crossref | GoogleScholarGoogle Scholar | 35545393PubMed |
Kemp, DJ (2001). Age-related site fidelity in the territorial butterfly Hypolimnas bolina (L.) (Lepidoptera: Nymphalidae). Australian Journal of Entomology 40, 65–68.
| Age-related site fidelity in the territorial butterfly Hypolimnas bolina (L.) (Lepidoptera: Nymphalidae).Crossref | GoogleScholarGoogle Scholar |
Koch, JB, Love, B, Klinger, E, and Strange, JP (2014). The effect of photobleaching on bee (Hymenoptera: Apoidea) setae color and its implications for studying aging and behavior. Journal of Melittology 38, 1–9.
| The effect of photobleaching on bee (Hymenoptera: Apoidea) setae color and its implications for studying aging and behavior.Crossref | GoogleScholarGoogle Scholar |
Křemenová, J, Balvín, O, Otti, O, Pavonič, M, Reinhardt, K, Šimek, Z, and Bartonička, T (2020). Identification and age-dependence of pteridines in bed bugs (Cimex lectularius) and bat bugs (C. pipistrelli) using liquid chromatography-tandem mass spectrometry. Scientific Reports 10, 10146.
| Identification and age-dependence of pteridines in bed bugs (Cimex lectularius) and bat bugs (C. pipistrelli) using liquid chromatography-tandem mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 32576867PubMed |
Kubiak M (2017) Investigating the pathways of pathogen defence senescence in Drosophila melanogaster. MPhil, University of Stirling, Stirling, UK.
Kuznetsova, A, Brockhoff, PB, and Christensen, RHB (2017). lmerTest package: tests in linear mixed effects models. Journal of Statistical Software 82, 1–26.
| lmerTest package: tests in linear mixed effects models.Crossref | GoogleScholarGoogle Scholar |
Liao, S, Broughton, S, and Nässel, DR (2017). Behavioral senescence and aging-related changes in motor neurons and brain neuromodulator levels are ameliorated by lifespan-extending reproductive dormancy in Drosophila. Frontiers in Cellular Neuroscience 11, 111.
| Behavioral senescence and aging-related changes in motor neurons and brain neuromodulator levels are ameliorated by lifespan-extending reproductive dormancy in Drosophila.Crossref | GoogleScholarGoogle Scholar | 28503133PubMed |
Lim, MLM, and Li, D (2006). Effects of age and feeding history on structure-based UV ornaments of a jumping spider (Araneae: Salticidae). Proceedings of the Royal Society of London B: Biological Sciences 274, 569–575.
| Effects of age and feeding history on structure-based UV ornaments of a jumping spider (Araneae: Salticidae).Crossref | GoogleScholarGoogle Scholar |
Malek, SRA (1958). The appearance and histological structure of the cuticle of the desert locust, Schistocerca gregaria (Forskal). Proceedings of the Royal Society of London B: Biological Sciences 149, 557–570.
| The appearance and histological structure of the cuticle of the desert locust, Schistocerca gregaria (Forskal).Crossref | GoogleScholarGoogle Scholar |
Marden, JH (2000). Variability in the size, composition, and function of insect flight muscles. Annual Review of Physiology 62, 157–178.
| Variability in the size, composition, and function of insect flight muscles.Crossref | GoogleScholarGoogle Scholar | 10845088PubMed |
Miguel-Aliaga, I, Jasper, H, and Lemaitre, B (2018). Anatomy and physiology of the digestive tract of Drosophila melanogaster. Genetics 210, 357–396.
| Anatomy and physiology of the digestive tract of Drosophila melanogaster.Crossref | GoogleScholarGoogle Scholar | 30287514PubMed |
Molleman, F, Ding, J, Carey, JR, and Wang, J-L (2009). Nutrients in fruit increase fertility in wild-caught females of large and long-lived Euphaedra species (Lepidoptera, Nymphalidae). Journal of Insect Physiology 55, 375–383.
| Nutrients in fruit increase fertility in wild-caught females of large and long-lived Euphaedra species (Lepidoptera, Nymphalidae).Crossref | GoogleScholarGoogle Scholar | 19186186PubMed |
Mueller, UG, and Wolf-Mueller, B (1993). A method for estimating the age of bees: age-dependent wing wear and coloration in the wool-carder bee Anthidium manicatum (Hymenoptera: Megachilidae). Journal of Insect Behavior 6, 529–537.
| A method for estimating the age of bees: age-dependent wing wear and coloration in the wool-carder bee Anthidium manicatum (Hymenoptera: Megachilidae).Crossref | GoogleScholarGoogle Scholar |
Münch, D, Amdam, GV, and Wolschin, F (2008). Ageing in a eusocial insect: molecular and physiological characteristics of life span plasticity in the honey bee. Functional Ecology 22, 407–421.
| Ageing in a eusocial insect: molecular and physiological characteristics of life span plasticity in the honey bee.Crossref | GoogleScholarGoogle Scholar | 18728759PubMed |
Muthukrishnan, S, Mun, S, Noh, MY, Geisbrecht, ER, and Arakane, Y (2020). Insect cuticular chitin contributes to form and function. Current Pharmaceutical Design 26, 3530–3545.
| Insect cuticular chitin contributes to form and function.Crossref | GoogleScholarGoogle Scholar | 32445445PubMed |
O’Neill, M, DeLandro, D, and Taylor, D (2019). Age-related responses to injury and repair in insect cuticle. Journal of Experimenal Biology 222, jeb182253.
| Age-related responses to injury and repair in insect cuticle.Crossref | GoogleScholarGoogle Scholar |
Parle, E, and Taylor, D (2017). The effect of aging on the mechanical behaviour of cuticle in the locust Schistocerca gregaria. Journal of the Mechanical Behavior of Biomedical Materials 68, 247–251.
| The effect of aging on the mechanical behaviour of cuticle in the locust Schistocerca gregaria.Crossref | GoogleScholarGoogle Scholar | 28219850PubMed |
Parle, E, Dirks, J-H, and Taylor, D (2016). Bridging the gap: wound healing in insects restores mechanical strength by targeted cuticle deposition. Journal of the Royal Society Interface 13, 20150984.
| Bridging the gap: wound healing in insects restores mechanical strength by targeted cuticle deposition.Crossref | GoogleScholarGoogle Scholar | 27053653PubMed |
Parle, E, Dirks, J-H, and Taylor, D (2017). Damage, repair and regeneration in insect cuticle: the story so far, and possibilities for the future. Arthropod Structure & Development 46, 49–55.
| Damage, repair and regeneration in insect cuticle: the story so far, and possibilities for the future.Crossref | GoogleScholarGoogle Scholar |
Partridge, L, and Barton, NH (1996). On measuring the rate of ageing. Proceedings of the Royal Society of London B: Biological Sciences 263, 1365–1371.
| On measuring the rate of ageing.Crossref | GoogleScholarGoogle Scholar |
Promislow, DEL, Flatt, T, and Bonduriansky, R (2022). The biology of aging in insects: from Drosophila to other insects and back. Annual Review of Entomology 67, 83–103.
| The biology of aging in insects: from Drosophila to other insects and back.Crossref | GoogleScholarGoogle Scholar | 34590891PubMed |
R_Core_Team (2013) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria)
Rajabi, H, Dirks, J-H, and Gorb, SN (2020). Insect wing damage: causes, consequences and compensatory mechanisms. Journal of Experimental Biology 223, jeb215194.
| Insect wing damage: causes, consequences and compensatory mechanisms.Crossref | GoogleScholarGoogle Scholar | 32366698PubMed |
Ridgel, AL, and Ritzmann, RE (2005). Insights into age-related locomotor declines from studies of insects. Ageing Research Reviews 4, 23–39.
| Insights into age-related locomotor declines from studies of insects.Crossref | GoogleScholarGoogle Scholar | 15619468PubMed |
Schneider, CA, Rasband, WS, and Eliceiri, KW (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.
| NIH Image to ImageJ: 25 years of image analysis.Crossref | GoogleScholarGoogle Scholar | 22930834PubMed |
Seid, MA, Harris, KM, and Traniello, JF (2005). Age-related changes in the number and structure of synapses in the lip region of the mushroom bodies in the ant Pheidole dentata. The Journal of Comparative Neurology 488, 269–277.
| Age-related changes in the number and structure of synapses in the lip region of the mushroom bodies in the ant Pheidole dentata.Crossref | GoogleScholarGoogle Scholar | 15952165PubMed |
Sepil, I, Hopkins, BR, Dean, R, Bath, E, Friedman, S, Swanson, B, Ostridge, HJ, Harper, L, Buehner, NA, Wolfner, MF, Konietzny, R, Thézénas, M-L, Sandham, E, Charles, PD, Fisher, R, Steinhauer, J, Kessler, BM, and Wigby, S (2020). Male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 117, 17094–17103.
| Male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable in Drosophila.Crossref | GoogleScholarGoogle Scholar | 32611817PubMed |
Sugimoto, M (2002). Morphological color changes in fish: regulation of pigment cell density and morphology. Microscopy Research and Technique 58, 496–503.
| Morphological color changes in fish: regulation of pigment cell density and morphology.Crossref | GoogleScholarGoogle Scholar | 12242707PubMed |
Taylor, LA, Clark, DL, and McGraw, KJ (2014). From spiderling to senescence: ontogeny of color in the jumping spider, Habronattus pyrrithrix. Journal of Arachnology 42, 268–276.
| From spiderling to senescence: ontogeny of color in the jumping spider, Habronattus pyrrithrix.Crossref | GoogleScholarGoogle Scholar |
Technau, GM (1984). Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience. Journal of Neurogenetics 1, 113–126.
| Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience.Crossref | GoogleScholarGoogle Scholar | 6085635PubMed |
Therneau TM (2022) A package for survival analysis in R, R package version 3.3-1. Available at https://CRAN.R-project.org/package=survival
Tobin, DJ (2009). Aging of the hair follicle pigmentation system. International Journal of Trichology 1, 83–93.
| Aging of the hair follicle pigmentation system.Crossref | GoogleScholarGoogle Scholar | 20927229PubMed |
Wang, L-Y, Rajabi, H, Ghoroubi, N, Lin, C-P, and Gorb, SN (2018). Biomechanical strategies underlying the robust body armour of an aposematic weevil. Frontiers in Physiology 9, 1410.
| Biomechanical strategies underlying the robust body armour of an aposematic weevil.Crossref | GoogleScholarGoogle Scholar | 30356766PubMed |
Wehmann, H-N, Engels, T, and Lehmann, F-O (2022). Flight activity and age cause wing damage in house flies. Journal of Experimenal Biology 225, jeb242872.
| Flight activity and age cause wing damage in house flies.Crossref | GoogleScholarGoogle Scholar |
