Abiotic Factors as Game Changer in Sex Ratio Distortion of Insects

Sweta Verma

Division of Entomology, ICAR-Indian Agricultural Research Institute, New Delhi- 110012, India.

Doddachowdappa Sagar *

Division of Entomology, ICAR-Indian Agricultural Research Institute, New Delhi- 110012, India and Division of Genomic Resources, ICAR- National Bureau of Agricultural Insect Resources, Bengaluru-560024, India.

Hemant Kumar

Division of Entomology, ICAR-Indian Agricultural Research Institute, New Delhi- 110012, India.

Sujatha G S

Division of Entomology, ICAR-Indian Agricultural Research Institute, New Delhi- 110012, India.

*Author to whom correspondence should be addressed.


Abstract

Sex ratios in insect populations are critical in shaping their reproductive dynamics, genetic diversity, and ecological interactions. While genetic factors often determine sex, abiotic factors have emerged as important influencers of sex ratios in insects. The influence of abiotic factors on sex ratios in insects is of scientific interest and holds practical implications for insect conservation and management. As environmental conditions change due to global warming, understanding how sex ratios respond to these changes can aid in predicting population dynamics and designing effective conservation strategies for biocontrol agents as well as the management of insect pests. Abiotic stressors, including fluctuations in temperature, humidity variations, altitude & latitude, nutrition and chemical exposure have been shown to disrupt the precise balance of hormonal and genetic cues governing sex determination in insects. Insects being ectothermic, body temperature depends on the surrounding environmental conditions and are highly vulnerable to the change in climate. This review explores the intricate relationship between abiotic stress and sex determination mechanisms in insects, highlighting recent advances in our understanding of how stress-induced alterations especially environment in hormone signaling, gene expression, and epigenetic modifications can lead to skewed sex ratios and developmental anomalies. Regardless of the advances in this area, notable research gaps are still present. Future studies on the multiple abiotic factors and their synergistic effects will give a more detailed study of insect populations, and their ecosystems. This comprehensive review delves into the multifaceted interactions between abiotic factors and sex differentiation in insects. In conclusion, the abiotic factors especially temperature are indeed game changers in the insect sex ratio dynamics.

Keywords: Abiotic factors, sex ratio, epigenetics, juvenile hormone, metamorphosis


How to Cite

Verma, Sweta, Doddachowdappa Sagar, Hemant Kumar, and Sujatha G S. 2024. “Abiotic Factors As Game Changer in Sex Ratio Distortion of Insects”. International Journal of Environment and Climate Change 14 (7):332-42. https://doi.org/10.9734/ijecc/2024/v14i74274.

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References

Singh A, Kumar V, Majumdar M, Guha L, Neog K. A comprehensive review of insect pest management in muga silkworm (Antheraea assamensis Helfer): Current scenario and future prospects. J Exp Agric Int. 2024;46(5):47-55. DOI:org/10.9734/jeai/2024/v46i52355

Devi Gitanjali. Influence of abiotic factors on efficacy of entomopathogenic nematodes. International Journal of Plant & Soil Science. 2024;36(3):283-90. DOI:org/10.9734/ijpss/2024/v36i34425.

Salz HK. Sex determination in insects: A binary decision based on alternative splicing. Current Opinion in Genetics & Development. 2011;21(4):395-400. DOI:org/10.1016/j.gde.2011.03.001

Yamanaka N. Ecdysteroid signalling in insects—From biosynthesis to gene expression regulation. In Advances in Insect Physiology. Academic Press. 2021; 60:1-36. DOI:org/10.1016/bs.aiip.2021.03.002

Shyu E, Caswell H. A demographic model for sex ratio evolution and the effects of sex‐biased offspring costs. Ecol Evol. 2016;6(5):1470-92.

Mukai A, Mano G, Des ML, Shinada T, Goto SG. Juvenile hormone as a causal factor for maternal regulation of diapause in a wasp. Insect Biochem. Mol. Biol. 2022; 144:103758. DOI:10.1016/j.ibmb.2022.103758

Sánchez L. Sex-determining mechanisms in insects based on imprinting and elimination of chromosomes. Sex Dev. 2014;8(1-3):83-103. DOI:org/10.1159/000356709

Lee IH, Nong W, So WL, Cheung CK, Xie Y, Baril T et al. The genome and sex-dependent responses to temperature in the common yellow butterfly, Eurema hecabe. BMC Boil. 2023;21(1):1-15. DOI:org/10.1186/s12915-023-01703-1.

Kennedy P. Haplodiploidy. In Encyclopedia of social insects. Cham: Springer International Publishing. 2021;31:477- 489. DOI:org/10.1007/978-3-030-28102-1_56

Bradshaw WE, Holzapfel CM. Light, tim e, and the physiology of biotic response to rapid climate change in animals. Annu Rev Physiol. 2010;72:147-166. DOI:org/10.1146/annurev-physiol-021909-135837

Salminen TS, Hoikkala A. Effect of temperature on the duration of sensitive period and on the number of photoperiodic cycles required for the induction of reproductive diapause in Drosophila montana. J Insect Physiol. 2013;59(4):450-457. DOI:org/10.1016/j.jinsphys.2013.02.005

Tougeron K. Diapause research in insects: Historical review and recent work perspectives. Entomol Exp Appl. 2019;167(1):27-36. DOI.org/10.1111/eea.12753

Gill HK, Goyal G, Chahil G. Insect diapause: A review. J. Agric. Sci. Technol. 2017;7:454-73. DOI:10.17265/2161-6256/2017.07.002

Snell-Rood EC, Kobiela ME, Sikkink KL, Shephard AM. Mechanisms of plastic rescue in novel environments. Annu Rev Ecol Evol Syst. 2018;49:331-354. DOI:org/10.1146/annurev-ecolsys-110617-062622

Numata H. General Features of Photoperiodism. In Insect Chronobiology. Singapore: Springer Nature Singapore. 2023;251-269.DOI:org/10.1007/978-981-99-0726-7_12

Goto SG. Photoperiodic time measurement, photoreception, and circadian clocks in insect photoperiodism. Applied Entomology and Zoology. 2022; 57(3):193-212. DOI:org/10.1007/s13355-022-00785-7

Miki T, Shinohara T, Chafino S, Noji S, Tomioka K. Photoperiod and temperature separately regulate nymphal development through JH and insulin/TOR signaling pathways in an insect. Proceedings of the National Academy of Sciences. 2020; 117(10):5525-5531. DOI:org/10.1073/pnas.1922747117

Skendžić S, Zovko M, Živković IP, Lešić V, Lemić D. The impact of climate change on agricultural insect pests. Insects. 2021; 12(5):440. DOI:org/10.3390/insects12050440

Lahondère C. Recent advances in insect thermoregulation. J Exp Biol. 2023; 226(18):jeb245751. DOI:org/10.1242/jeb.245751

Pathania M, Verma A, Singh M, Arora PK, Kaur N. Influence of abiotic factors on the infestation dynamics of whitefly, Bemisia tabaci (Gennadius 1889) in cotton and its management strategies in North-Western India. Int. J. Trop. Insect Sci. 2020;40:969-981. DOI:org/10.1007/s42690-020-00155-2

McCain CM, Garfinkel CF. Climate change and elevational range shifts in insects. Current Opinion in Insect Science. 2021; 47:111-8. DOI:org/10.1016/j.cois.2021.06.003

Naidu SJ, Arangasamy A, Selvaraju S, Binsila BK, Reddy IJ, Ravindra JP, Bhatta R. Maternal influence on the skewing of offspring sex ratio: A review. Anim Prod Sci. 2022;62(6):501-10. DOI:org/10.1071/AN21086

Verma S, Ramani R, Sachan A, Chandra R. The role of Wolbachia and the environment on sex determination of the Indian lac insect, Kerria lacca (Coccoidea: Tachardiidae). J. AsiaPac. Entomol. 2023; 26(1):102019. DOI:org/10.1016/j.aspen.2022.102019

Quezada-García R, Pureswaran D, Bauce É. Nutritional stress causes male-biased sex ratios in eastern spruce budworm (Lepidoptera: Tortricidae). Can. Entomol. 2014;146(2):219-223. DOI:10.4039/tce.2013.72

Quezada García R, Seehausen ML, Bauce É. Adaptation of an outbreaking insect defoliator to chronic nutritional stress. J Evol Biol. 2015;28(2):347-55. DOI:org/10.1111/jeb.12571

Whipple AV, Cobb NS, Gehring CA, Mopper S, Flores-Rentería L, Whitham TG. Long-term studies reveal differential responses to climate change for trees under soil-or herbivore-related stress. Front Plant Sci. 2019;10:411390. DOI:org/10.3389/fpls.2019.00132

Lockley EC, Eizaguirre C. Effects of global warming on species with temperature‐dependent sex determination: Bridging the gap between empirical research and management. Evo. Appl. 2021;14(10):2361-2377. DOI:org/10.1111/eva.13226

Van Doorn GS. Evolutionary transitions between sex-determining mechanisms: A review of theory. Sexual Development. 2014;8(1-3):7-19. DOI:org/10.1159/000357023

Edmands S. Sex ratios in a warming world: Thermal effects on sex-biased survival, sex determination, and sex reversal. J Hered. 2021;112(2):155-164. DOI:org/10.1093/jhered/esab006

Steele AL, Wibbels T, Warner DA. Revisiting the first report of temperature‐dependent sex determination in a vertebrate, the African redhead agama. J Zool. 2018;306(1):16-22. DOI:org/10.1111/jzo.12560

Golizadeh ALI, Kamali K, Fathipour Y, Abbasipour H. Temperature‐dependent development of diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) on two brassicaceous host plants. Insect Sci. 2007;14(4):309-316. Doi:org/10.1111/j.1744-7917.2007.00157.x

Bronikowski AM, Meisel RP, Biga PR, Walters JR, Mank JE, Larschan et al. Sex‐specific aging in animals: Perspective and future directions. Aging Cell. 2022; 21(2):e13542. DOI:org/10.1111/acel.13542

Bachtrog D, Mank JE, Peichel CL, Kirkpatrick M, Otto SP, Ashman TL, Hahn MW, Kitano J, Mayrose I, Ming R, Perrin N. Sex determination: why so many ways of doing it? Plos Biology. 2014;12(7): e1001899. DOI:org/10.1371/journal.pbio.1001899

Darwish YA, Ali AM, Mohamed RA, Khalil NM. Effect of extreme low and high temperatures on the almond moth, Ephestia cautella (Walker) (Lepidoptera: Pyralidae). Journal of Phytopathology and Disease Management. 2015;7:36-46. DOI:org/10.1016/j.aspen.2022.102019

Reshma R, Sagar D, Subramanian S, Kalia VK, Kuma H, Muthusamy V. Transgenerational effects of thermal stress on reproductive physiology of fall armyworm, Spodoptera frugiperda. J Pest Sci. 2023;96(4):1465-1481. DOI:org/10.1007/s10340-023-01660-2

Vaught RC, Voigt S, Dobler R, Clancy DJ, Reinhardt K, Dowling DK. Interactions between cytoplasmic and nuclear genomes confer sex‐specific effects on lifespan in Drosophila melanogaster. J of Evol Biol. 2020;33(5):694-713. DOI:org/10.1111/jeb.13605

Islam MS, Rahman S. Temperature and Relative humidity-mediated immature development and adult emergence in the mulberry silkworm Bombyx mori L. Elixir Appl Zoology. 2018;118:50852-50856.

Eberhart-Phillips LJ, Küpper C, Carmona-Isunza MC, Vincze O, Zefania S, Cruz-López M, et al. Demographic causes of adult sex ratio variation and their consequences for parental cooperation. Nat Commun. 2018;9(1):1651. DOI:org/10.1038/s41467-018-03833-5

Godwin JL, Lumley AJ, Michalczyk Ł, Martin OY, Gage MJ. Mating patterns influence vulnerability to the extinction vortex. Glob Change Biol. 2020;26(8): 4226-4239. DOI:org/10.1111/gcb.15186.

Boyle M, Schwanz L, Hone J, Georges A. Dispersal and climate warming determine range shift in model reptile populations. Ecol Modell. 2016;32:34-43. DOI:org/10.1016/j.ecolmodel.2016.02.011

West, Stuart. Sex Allocation, Princeton: Princeton University Press; 2010. DOI:org/10.1515/9781400832019

Zhang W, Zhao F, Hoffmann AA, Ma C-S. A single hot event that does not affect survival but decreases reproduction in the diamondback moth, Plutella xylostella. Plos One 2013;8(10):e75923. DOI:org/10.1371/journal.pone.0075923

Walsh BS, Mannion NL, Price TA, Parratt SR. Sex-specific sterility caused by extreme temperatures is likely to create cryptic changes to the operational sex ratio in Drosophila virilis. Curr Zool. 2021; 67(3):341-343. DOI:org/10.1093/cz/zoaa067

Moiroux J, Brodeur J, Boivin G. Sex ratio variations with temperature in an egg parasitoid: Behavioural adjustment and physiological constraint. Anim Behav. 2014;91:61–66. DOI:org/10.1016/j.anbehav.2014.02.021

Pandey AK, Tripathi CPM. Effect of temperature on the development, fecundity, progeny sex ratio and life-table of Campoletis chlorideae, an endolarval parasitoid of the pod borer, Helicoverpa armigera. BioControl. 2008;53:461–471.

DOI:org/10.1007/s10526-007-9083-3

Limbu S, Keena M, Chen F, Cook G, Nadel H, Hoover K. Effects of temperature on development of Lymantria dispar asiatica and Lymantria dispar japonica (Lepidoptera: Erebidae). Environ Entomol. 2017;46(4):1012-23. DOI:org/10.1093/ee/nvx111

Engelmann F. The physiology of insect reproduction: International series of monographs in pure and applied biology: Zoology. Elsevier; 2013.

Grath S, Parsch J. Sex-biased gene expression. Annu Rev Genet. 2016;50:29-44. DOI:org/10.1146/annurev-genet-120215-035429

Sonoda S, Ashfaq M, Tsumuki H. Cloning and nucleotide sequencing of three heat shock protein genes (hsp90, hsc70, and hsp19. 5) from the diamondback moth, Plutella xylostella (L.) and their expression in relation to developmental stage and temperature. Arch Insect Biochem Physiol. 2006;62(2):80-90. DOI:org/10.1002/arch.20124

Hu J, Medison RG, Zhang S, Ma P, Shi C. Impacts of Non-Lethal High-Temperature Stress on the Development and Reproductive Organs of Bradysia odoriphaga. Insects. 2022;13(1):74. DOI:org/10.3390/insects13010074

Bressan RA, Zhu JK, Van Oosten MJ, Maggio A, Bohnert HJ, Chinnusamy V. Epigenetics connects the genome to its environment. Plant Breeding Reviews. 2014;38:69-142. DOI:org/10.1002/9781118916865.ch03

Brock HW, Fisher CL. Maintenance of gene expression patterns. Developmental dynamics: an official publication of the American Association of Anatomists. 2005;232(3):633-655.

DOI:org/10.1002/dvdy.20298

Mukherjee K, Twyman RM, Vilcinskas A. Insects as models to study the epigenetic basis of disease. Prog. Biophys. Mol Biol. 2015;118(1-2):69-78.

DOI:org/10.1016/j.pbiomolbio.2015.02.009

Glastad KM, Hunt BG, Goodisman MA. Epigenetics in insects: genome regulation and the generation of phenotypic diversity. Annu Rev Entomol. 2019;64:185-203.

DOI:org/10.1146/annurev-ento-011118-111914

Loison L. Lamarckism and epigenetic inheritance: A clarification. Biology & Philosophy. 2018; 33:1-7.

DOI:org/10.1007/s10539-018-9642-2

Heard E, Martienssen RA. Transgenerational epigenetic inheritance: Myths and mechanisms. Cell. 2014;157(1): 95-109.

DOI:org/10.1016/j.cell.2014.02.045

Berger SL, Kouzarides T, Shiekhattar R, Shilatifard A. An operational definition of epigenetics. Genes Dev. 2009,23(7):781-783. DOI:10.1101/gad.1787609

Piferrer F. Epigenetic mechanisms in sex determination and in the evolutionary transitions between sexual systems. Philosophical Transactions of the Royal Society B. 2021;376(1832): 20200110. DOI:org/10.1098/rstb.2020.0110

Piferrer F. Epigenetics of sex determination and gonadogenesis. Developmental Dynamics. 2013, Apr; 242(4):360-70. DOI:org/10.1002/dvdy.23924

James H, Renard J P. Epigénétique et construction du phénotype, un enjeu pour les productions animales? (Epigenetics and construction of the phenotype: A challenge for animal production). INRA Prod Anim. 2010;23:23-42. DOI:org/10.20870/productions-animales.2010.23.1.3283

Gotoh H, Miyakawa H, Ishikawa A, Ishikawa Y, Sugime Y, Emlen DJ et al. Developmental link between sex and nutrition; doublesex regulates sex-specific mandible growth via juvenile hormone signaling in stag beetles. Plos Genetics. 2014;10(1): e1004098. DOI:org/10.1371/journal.pgen.1004098