Early life starvation has stronger intra-generational than transgenerational effects on key life-history traits and consumption measures in a sawfly
Autoři:
Sarah Catherine Paul aff001; Rocky Putra aff001; Caroline Müller aff001
Působiště autorů:
Chemical Ecology, Bielefeld University, Bielefeld, Germany
aff001; Hawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW, Australia
aff002
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0226519
Souhrn
Resource availability during development shapes not only adult phenotype but also the phenotype of subsequent offspring. When resources are absent and periods of starvation occur in early life, such developmental stress often influences key life-history traits in a way that benefits individuals and their offspring when facing further bouts of starvation. Here we investigated the impacts of different starvation regimes during larval development on life-history traits and measures of consumption in the turnip sawfly, Athalia rosae (Hymenoptera: Tenthredinidae). We then assessed whether offspring of starved and non-starved parents differed in their own life-history if reared in conditions that either matched that of their parents or were a mismatch. Early life starvation effects were more pronounced within than across generations in A. rosae, with negative impacts on adult body mass and increases in developmental time, but no effects on adult longevity in either generation. We found some evidence of higher growth rates in larvae having experienced starvation, although this did not ameliorate the overall negative effect of larval starvation on adult size. However, further work is necessary to disentangle the effects of larval size and instar from those of starvation treatment. Finally, we found weak evidence for transgenerational effects on larval growth, with intra-generational larval starvation experience being more decisive for life-history traits. Our study demonstrates that intra-generational effects of starvation are stronger than transgenerational effects on life-history traits and consumption measures in A. rosae.
Klíčová slova:
Phenotypes – Diet – Food – Leaves – Food consumption – Flowering plants – Larvae – Starvation
Zdroje
1. Lindström J. Early development and fitness in birds and mammals. Trends Ecol Evol. 1999; 14(9):343–348. doi: 10.1016/s0169-5347(99)01639-0 10441307
2. Gilbert SF. Mechanisms for the environmental regulation of gene expression: Ecological aspects of animal development. J Biosci. 2005; 30(1):65–74. doi: 10.1007/bf02705151 15824442
3. Taborsky B. Developmental plasticity: preparing for life in a complex world. Adv Study Behav. 2017; 49:49–99.
4. Scofield HN, Mattila HR. Honey bee workers that are pollen stressed as larvae become poor foragers and waggle dancers as adults. PLoS One. 2015; 10(4):1–19.
5. Royle NJ, Lindström J, Metcalfe NB. A poor start in life negatively affects dominance status in adulthood independent of body size in green swordtails Xiphophorus helleri. Proc R Soc B Biol Sci. 2005; 272(1575):1917–1922.
6. Nowicki S, Searcy WA, Peters S. Brain development, song learning and mate choice in birds: A review and experimental test of the “nutritional stress hypothesis.” J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2002; 188(11–12):1003–1014. doi: 10.1007/s00359-002-0361-3 12471497
7. Monaghan P. Early growth conditions, phenotypic development and environmental change. Philos Trans R Soc B. 2008; 363(1497):1635–1645.
8. Bateson P, Gluckman P, Hanson M. The biology of developmental plasticity and the Predictive Adaptive Response hypothesis. J Physiol. 2014; 592(11):2357–2368. doi: 10.1113/jphysiol.2014.271460 24882817
9. Burton T, Metcalfe NB. Can environmental conditions experienced in early life influence future generations? Proc R Soc B Biol Sci. 2014; 281(1785):20140311.
10. Bonduriansky R, Day T. Nongenetic inheritance and its evolutionary implications. Annu Rev Ecol Evol Syst. 2009; 40(1):103–125.
11. Bonduriansky R, Crean AJ. What are parental condition-transfer effects and how can they be detected? Methods Ecol Evol. 2017; 9(3):450–456.
12. McCue MD, Terblanche JS, Benoit JB. Learning to starve: impacts of food limitation beyond the stress period. J Exp Biol. 2017; 220(23):4330–4338.
13. Barbosa P, Letourneau DK, Agrawal AA, editors. Insect outbreaks revisited. Oxford: Wiley-Blackwell; 2012.
14. Stearns SC. The Evolution of Life Histories. Oxford University Press; 1992.
15. Wang Y, Kaftanoglu O, Brent CS, Page RE, Amdam G V. Starvation stress during larval development facilitates an adaptive response in adult worker honey bees (Apis mellifera L.). J Exp Biol. 2016; 219(7):949–959.
16. Zwaan BJ, Bijlsma R, Hoekstra RF. On the developmental theory of ageing. I. starvation resistance and longevity in Drosophila melanogaster in relation to pre-adult breeding conditions. Heredity. 1991; 66(1):29–39.
17. Dmitriew C, Rowe L. Effects of early resource limitation and compensatory growth on lifetime fitness in the ladybird beetle (Harmonia axyridis). J Evol Biol. 2007; 20(4):1298–1310. doi: 10.1111/j.1420-9101.2007.01349.x 17584225
18. Jobson MA, Jordan JM, Sandrof MA, Hibshman JD, Lennox AL, Baugh LR. Transgenerational effects of early life starvation on growth, reproduction, and stress resistance in Caenorhabditis elegans. Genetics. 2015; 201(1):201–212. doi: 10.1534/genetics.115.178699 26187123
19. Hibshman JD, Hung A, Baugh LR. Maternal diet and insulin-like signaling control intergenerational plasticity of progeny size and starvation resistance. PLoS Genet. 2016; 12(10):1–22.
20. Webster AK, Jordan JM, Hibshman JD, Chitrakar R, Ryan Baugh L. Transgenerational effects of extended dauer diapause on starvation survival and gene expression plasticity in Caenorhabditis elegans. Genetics. 2018; 210(1):263–274. doi: 10.1534/genetics.118.301250 30049782
21. Saastamoinen M, Rantala MJ. Influence of developmental conditions on immune function and dispersal-related traits in the glanville fritillary (Melitaea cinxia) butterfly. PLoS One. 2013; 8(11):1–11.
22. Hales CN, Barker DJP. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992; 2(35):595–601.
23. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 2008; 359(1):61–73. doi: 10.1056/NEJMra0708473 18596274
24. Marshall DJ, Uller T. When is a maternal effect adaptive? Oikos. 2007; 116(12):1957–1963.
25. Jablonka E, Oborny B, Molnar I, Kisdi E, Hofbauer J, Czaran T. The adaptive advantage of phenotypic memory in changing environments. Philos Trans R Soc B Biol Sci. 1995; 350(1332):133–141.
26. Boggs CL, Freeman KD. Larval food limitation in butterflies: Effects on adult resource allocation and fitness. Oecologia. 2005; 144(3):353–361. doi: 10.1007/s00442-005-0076-6 15891831
27. Wang Y, Campbell JB, Kaftanoglu O, Page RE, Amdam G V., Harrison JF. Larval starvation improves metabolic response to adult starvation in honey bees (Apis mellifera L.). J Exp Biol. 2016; 219(7):960–968.
28. Dmitriew C, Carroll J, Rowe L. Effects of early growth conditions on body composition, allometry, and survival in the ladybird beetle Harmonia axyridis. Can J Zool. 2009; 87(2):175–182.
29. Rosa E, Saastamoinen M. Sex-dependent effects of larval food stress on adult performance under semi-natural conditions: only a matter of size? Oecologia. 2017; 184(3):633–642. doi: 10.1007/s00442-017-3903-7 28685203
30. Benrey B, Denno RF. The slow-growth-high-mortality hypothesis: A test using the cabbage butterfly. Ecology. 1997; 78(4):987–999.
31. Häggström H, Larsson S. Slow larval growth on a suboptimal willow results in high predation mortality in the leaf beetle Galerucella lineola. Oecologia. 1995; 104(3):308–315. doi: 10.1007/BF00328366 28307587
32. Saastamoinen M, Ikonen S, Wong SC, Lehtonen R, Hanski I. Plastic larval development in a butterfly has complex environmental and genetic causes and consequences for population dynamics. J Anim Ecol. 2013; 82(3):529–539. doi: 10.1111/1365-2656.12034 23347450
33. Metcalfe NB, Monaghan P. Compensation for a bad start: grow now, pay later. Trends Ecol Evol. 2001; 16(5):254–260. doi: 10.1016/s0169-5347(01)02124-3 11301155
34. Hector KL, Nakagawa S. Quantitative analysis of compensatory and catch-up growth in diverse taxa. J Anim Ecol. 2012; 81(3):583–593. doi: 10.1111/j.1365-2656.2011.01942.x 22269070
35. Kahn AT, Livingston JD, Jennions MD. Do females preferentially associate with males given a better start in life? Biol Lett. 2012; 8(3):362–364. doi: 10.1098/rsbl.2011.1106 22237504
36. Holmgren K. Omitted spawning in compensatory-growing perch. J Fish Biol. 2003; 62(4):918–927.
37. Metcalfe NB, Monaghan P. Growth versus lifespan: Perspectives from evolutionary ecology. Exp Gerontol. 2003; 38(9):935–940. doi: 10.1016/s0531-5565(03)00159-1 12954479
38. Crean AJ, Bonduriansky R. What is a paternal effect? Trends Ecol Evol. 2014; 29(10):554–559. doi: 10.1016/j.tree.2014.07.009 25130305
39. Vega-Trejo R, Kruuk LEB, Jennions MD, Head ML. What happens to offspring when parents are inbred, old or had a poor start in life? Evidence for sex-specific parental effects. J Evol Biol. 2018; 31(8):1138–1151. doi: 10.1111/jeb.13292 29791044
40. Zirbel K, Eastmond B, Alto BW. Parental and offspring larval diets interact to influence life-history traits and infection with dengue virus in Aedes aegypti. R Soc Open Sci. 2018; 5(7):180539. doi: 10.1098/rsos.180539 30109101
41. Zizzari ZV., van Straalen NM, Ellers J. Transgenerational effects of nutrition are different for sons and daughters. J Evol Biol. 2016; 29(7):1317–1327. doi: 10.1111/jeb.12872 27018780
42. Riggert E. Untersuchungen über die Rübenblattwespe Athalia colobri Christ (A. spinarum F.). Zeitschr Angew Entomol. 1939; 26:462–516.
43. Sáringer G. Problems of Athalia rosae L. (Hymenoptera-Tenthredinidae) in Hungary. Acta Agron Acad Sci Hungaricae. 1976; 25:153–156.
44. Sawa M, Akihiro F, Naito T, Oishi K. Studies on the Sawfly, Athalia rosae (Insecta, Hymenoptera, Tenthredinidae). I. General Biology. Zoolog Sci. 1989; 6(3):541–547.
45. Groothuis TGG, Taborsky B. Introducing biological realism into the study of developmental plasticity in behaviour. Front Zool. 2015; 12(1):S6.
46. Crawley MJ. The R book. John Wiley & Sons; 2012.
47. Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biometrical J. 2008; 50(3):346–363.
48. Therneau T. A Package for Survival Analysis in S. version 2.38. 2019. p. https://CRAN.R-project.org/package=survival.
49. Castagneyrol B, Moreira X, Jactel H. Drought and plant neighbourhood interactively determine herbivore consumption and performance. Sci Rep. 2018; 8(1):1–11. doi: 10.1038/s41598-017-17765-5
50. Raubenheimer D, Simpson SJ. Analysis of covariance an alternative to indices. Entomol Exp Appl. 1992; 62(3):221–231.
51. Raubenheimer D. Problems with ratio analysis in nutritional studies. Funct Ecol. 1995; 9(1):21–29.
52. Tremmel M, Müller C. The consequences of alternating diet on performance and food preferences of a specialist leaf beetle. J Insect Physiol. 2013; 59(8):840–847. doi: 10.1016/j.jinsphys.2013.05.009 23727303
53. Fordyce JA, Shapiro AM. Another perspective on the slow-growth/high-mortality hypothesis: Chilling effects on swallowtail larvae. Ecology. 2003; 84(1):263–268.
54. Berner D, Blanckenhorn WU. Grasshopper ontogeny in relation to time constraints: Adaptive divergence and stasis. J Anim Ecol. 2006; 75(1):130–139. doi: 10.1111/j.1365-2656.2005.01028.x 16903050
55. Zonneveld C. Being big or emerging early? Polyandry and the trade-off between size and emergence in male butterflies. Am Nat. 1996; 147(6):946–965.
56. Brown S, Soroker V, Ribak G. Effect of larval growth conditions on adult body mass and long-distance flight endurance in a wood-boring beetle: Do smaller beetles fly better? J Insect Physiol. 2017; 98:327–335. doi: 10.1016/j.jinsphys.2017.02.008 28237580
57. Boggs CL, Niitepõld K. Effects of larval dietary restriction on adult morphology, with implications for flight and life history. Entomol Exp Appl. 2016; 159(2):189–196.
58. Saastamoinen M, van der Sterren D, Vastenhout N, Zwaan BJ, Brakefield PM. Predictive adaptive responses: condition‐dependent impact of adult nutrition and flight in the tropical butterfly Bicyclus anynana. Am Nat. 2010; 176(6):686–698. doi: 10.1086/657038 20955012
59. Nicieza AG, Álvarez D. Statistical analysis of structural compensatory growth: How can we reduce the rate of false detection? Oecologia. 2009; 159(1):27–39. doi: 10.1007/s00442-008-1194-8 18975008
60. Nakagawa S, Lagisz M, Hector KL, Spencer HG. Comparative and meta-analytic insights into life extension via dietary restriction. Aging Cell. 2012; 11(3):401–409. doi: 10.1111/j.1474-9726.2012.00798.x 22268691
61. English S, Uller T. Does early-life diet affect longevity? A meta-analysis across experimental studies. Biol Lett. 2016; 12(9):2016–2019.
62. Cooper EB, Kruuk LEB. Ageing with a silver-spoon: A meta-analysis of the effect of developmental environment on senescence. Evol Lett. 2018; 2(5):460–471. doi: 10.1002/evl3.79 30283695
63. Geiger S, Le Vaillant M, Lebard T, Reichert S, Stier A, Le Maho Y, et al. Catching-up but telomere loss: Half-opening the black box of growth and ageing trade-off in wild king penguin chicks. Mol Ecol. 2012; 21(6):1500–1510. doi: 10.1111/j.1365-294X.2011.05331.x 22117889
64. Nettle D, Monaghan P, Gillespie R, Brilot B, Bedford T, Bateson M. An experimental demonstration that early-life competitive disadvantage accelerates telomere loss. Proc R Soc B Biol Sci. 2015; 282(1798).
65. Reichert S, Criscuolo F, Zahn S, Arrive M, Bize P, Massemin S. Immediate and delayed effects of growth conditions on ageing parameters in nestling zebra finches. J Exp Biol. 2014; 218(3):491–499.
66. Cram DL, Monaghan P, Gillespie R, Clutton-Brock T. Effects of early-life competition and maternal nutrition on telomere lengths in wild meerkats. Proc R Soc B Biol Sci. 2017; 284(1861).
67. Eyck HJF, Buchanan KL, Crino OL, Jessop TS. Effects of developmental stress on animal phenotype and performance: a quantitative review. Biol Rev. 2019; 94(3):1143–1160. doi: 10.1111/brv.12496 30609279
68. Mestre L, Bonte D. Food stress during juvenile and maternal development shapes natal and breeding dispersal in a spider. Behav Ecol. 2012; 23(4):759–764.
69. Boggs CL. Understanding insect life histories and senescence through a resource allocation lens. Funct Ecol. 2009; 23:27–37.
70. Krist M. Egg size and offspring quality: A meta-analysis in birds. Biol Rev. 2011; 86(3):692–716. doi: 10.1111/j.1469-185X.2010.00166.x 21070586
71. Rollinson N, Hutchings JA. Environmental quality predicts optimal egg size in the wild. Am Nat. 2013; 182(1):76–90. doi: 10.1086/670648 23778228
72. Fox CW, Thakar MS, Mousseau TA. Egg size plasticity in a seed beetle: an adaptive maternal effect. Am Nat. 1997; 149(1):149–163.
73. Smith CC, Fretwell SD. The optimal balance between size and number of offspring. Am Nat. 2002; 108(962):499–506.
74. Franzke A, Reinhold K. Transgenerational effects of diet environment on life-history and acoustic signals of a grasshopper. Behav Ecol. 2013; 24(3):734–739.
75. Valtonen TM, Kangassalo K, Pölkki M, Rantala MJ. Transgenerational effects of parental larval diet on offspring development time, adult body size and pathogen resistance in Drosophila melanogaster. PLoS One. 2012; 7(2):32–40.
76. Saastamoinen M, Hirai N, van Nouhuys S. Direct and trans-generational responses to food deprivation during development in the Glanville fritillary butterfly. Oecologia. 2013; 171(1):93–104. doi: 10.1007/s00442-012-2412-y 22814878
77. Krause ET, Naguib M. Effects of parental and own early developmental conditions on the phenotype in zebra finches (Taeniopygia guttata). Evol Ecol. 2014; 28(2):263–275.
78. Engqvist L, Reinhold K. Adaptive trans-generational phenotypic plasticity and the lack of an experimental control in reciprocal match / mismatch experiments. Methods Ecol Evol. 2016; 7:1482–1488.
Článok vyšiel v časopise
PLOS One
2019 Číslo 12
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Úspěšná resuscitativní thorakotomie v přednemocniční neodkladné péči
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Methylsulfonylmethane increases osteogenesis and regulates the mineralization of the matrix by transglutaminase 2 in SHED cells
- Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay
- The characteristic of patulous eustachian tube patients diagnosed by the JOS diagnostic criteria
- Parametric CAD modeling for open source scientific hardware: Comparing OpenSCAD and FreeCAD Python scripts