Abstract
The last reproductive event of a female is often associated with major changes in terms of both maternal and offspring life-history traits. However, the nature of these changes and the importance of population-specific environmental constraints in shaping their expression are difficult to predict and, as a consequence, poorly understood. Here, we investigated whether and how life-history traits vary between reproductive events and whether this variation is population-dependent in the European earwig Forficula auricularia. In this insect species, females produce up to two clutches during their lifetime and express extensive forms of maternal care. We conducted a common garden experiment, in which we measured 11 life-history traits of the first and second clutches of 132 females originating from three populations. Our results showed that clutch size was higher and the level of care expressed towards juveniles lower in second as compared to the first clutches in all three populations. In contrast, we found a population-specific effect on whether and how the reproductive event shaped juvenile quality and a trade-off between egg developmental time and female weight at hatching. Overall, these findings emphasise that the last reproductive event of a female entails both positive and negative effects on various life-history traits of the female herself and her clutch of juveniles. Moreover, our study stresses the importance of population idiosyncrasies on the expression and nature of such cohort-specific effects.
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References
Boos S, Meunier J, Pichon S, Kölliker M (2014) Maternal care provides antifungal protection to eggs in the European earwig. Behav Ecol 25:754–761. doi:10.1093/beheco/aru046
Bowen WD, Iverson SJ, McMillan JI, Boness DJ (2006) Reproductive performance in grey seals: age-related improvement and senescence in a capital breeder. J Anim Ecol 75:1340–1351. doi:10.1111/j.1365-2656.2006.01157.x
Brommer JE (2000) The evolution of fitness in life-history theory. Biol Rev 75:377–404. doi:10.1111/j.1469-185X.2000.tb00049.x
Brown CA, Formanowicz DR (1995) Variation in reproductive investment among and within populations of the scorpion Centruroides vittatus. Oecologia 103:140–147. doi:10.1007/BF00329073
Clutton-Brock TH (1984) Reproductive effort and terminal investment in iteroparous animals. Am Nat 123:212–229
Cotter SC, Ward RJS, Kilner RM (2011) Age-specific reproductive investment in female burying beetles: independent effects of state and risk of death. Funct Ecol 25:652–660. doi:10.1111/j.1365-2435.2010.01819.x
Creighton JC, Heflin ND, Belk MC (2009) Cost of reproduction, resource quality, and terminal investment in a burying beetle. Am Nat 174:673–684. doi:10.1086/605963
Descamps S, Boutin S, Berteaux D, Gaillard J-M (2007) Female red squirrels fit Williams’ hypothesis of increasing reproductive effort with increasing age. J Anim Ecol 76:1192–1201. doi:10.1111/j.1365-2656.2007.01301.x
Diamantidis AD, Carey JR, Nakas CT, Papadopoulos NT (2011) Population-specific demography and invasion potential in medfly. Ecol Evol 1:479–488. doi:10.1002/ece3.33
Diehl JM, Körner M, Pietsch M, Meunier J (2015) Feces production as a form of social immunity in an insect with facultative maternal care. BMC Evol Biol 15(15):40. doi:10.1186/s12862-015-0330-4
Dobler R, Kölliker M (2010) Kin-selected siblicide and cannibalism in the European earwig. Behav Ecol 21:257–263. doi:10.1093/beheco/arp184
Flatt T, Heyland A (2011) Mechanisms of life history evolution: the genetics and physiology of life history traits and trade-offs. Oxford University Press, Oxford
Fox CW, Czesak ME (2000) Evolutionary ecology of progeny size in arthropods. Annu Rev Entomol 45:341–369
Gómez Y, Kölliker M (2013) Maternal care, mother-offspring aggregation and age-dependent coadaptation in the European earwig. J Evol Biol 26:1903–1911. doi:10.1111/jeb.12184
Hasselquist D, Nilsson J-A (2009) Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Philos Trans R Soc Lond B Biol Sci 364:51–60. doi:10.1098/rstb.2008.0137
Husson F, Le S, Pagès J (2011) Exploratory multivariate analysis by example using R. Chapman and Hall/CRC Press, London
Javoiš J (2013) A two-resource model of terminal investment. Theory Biosci 132:123–132. doi:10.1007/s12064-013-0176-5
Koch LK, Meunier J (2014) Mother and offspring fitness in an insect with maternal care: phenotypic trade-offs between egg number, egg mass and egg care. BMC Evol Biol 14:125. doi:10.1186/1471-2148-14-125
Kölliker M (2007) Benefits and costs of earwig (Forficula auricularia) family life. Behav Ecol Sociobiol 61:1489–1497. doi:10.1007/s00265-007-0381-7
Kölliker M, Boos S, Wong JWY et al (2015) Parent-offspring conflict and the genetic trade-offs shaping parental investment. Nat Commun 6:6850. doi:10.1038/ncomms7850
Kowald A, Kirkwood TBL (2015) Evolutionary significance of ageing in the wild. Exp Gerontol 71:89–94. doi:10.1016/j.exger.2015.08.006
Kramer J, Meunier J (2016) Maternal condition determines offspring behavior toward family members in the European earwig. Behav Ecol 27:494–500. doi:10.1093/beheco/arv181
Kramer J, Thesing J, Meunier J (2015) Negative association between parental care and sibling cooperation in earwigs: a new perspective on the early evolution of family life? J Evol Biol 28:1299–1308. doi:10.1111/jeb.12655
Krams IA, Krama T, Moore FR et al (2015) Resource availability as a proxy for terminal investment in a beetle. Oecologia 178:339–345. doi:10.1007/s00442-014-3210-5
Lamb RJ (1976) Parental behavior in the dermaptera with special reference to Forficula auricularia (Dermaptera: Forficulidae). Can J Entomol 108:609–619
Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18. doi:10.1016/j.envint.2008.06.007
Mason THE, Chirichella R, Richards SA et al (2011) Contrasting life histories in neighbouring populations of a large mammal. PLoS One 6:e28002. doi:10.1371/journal.pone.0028002
McNamara JM, Houston AI (1996) State-dependent life histories. Nature 380:215–221
Meunier J, Kölliker M (2012) Parental antagonism and parent-offspring co-adaptation interact to shape family life. Proc R Soc B Biol Sci 279:3981–3988. doi:10.1098/rspb.2012.1416
Meunier J, Wong JWY, Gómez Y et al (2012) One clutch or two clutches? Fitness correlates of coexisting alternative female life-histories in the European earwig. Evol Ecol 26:669–682. doi:10.1007/s10682-011-9510-x
Nussey DH, Froy H, Lemaitre J-F et al (2013) Senescence in natural populations of animals: Widespread evidence and its implications for bio-gerontology. Ageing Res Rev 12:214–225. doi:10.1016/j.arr.2012.07.004
Nylin S, Gotthard K (1998) Plasticity in life-history traits. Annu Rev Entomol 43:63–83. doi:10.1146/annurev.ento.43.1.63
Part T, Gustafsson L, Moreno J (1992) Terminal investment and a sexual conflict in the collared flycatcher (Ficedula albicollis). Am Nat 140:868–882
Reznick D, Nunney L, Tessier A (2000) Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol Evol 15:421–425. doi:10.1016/S0169-5347(00)01941-8
Roff DA (1992) The evolution of life histories: theory and analysis. Chapman and Hall, New York
Royle NJ, Smiseth PT, Kölliker M (2012) The evolution of parental care. Oxford University Press, Oxford
Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352. doi:10.1111/j.1461-0248.2004.00715.x
Sandrin L, Meunier J, Raveh S et al (2015) Multiple paternity and mating group size in the European earwig, Forficula auricularia. Ecol Entomol 40:159–166. doi:10.1111/een.12171
Santos ESA, Nakagawa S (2012) The costs of parental care: a meta-analysis of the trade-off between parental effort and survival in birds. J Evol Biol 25:1911–1917. doi:10.1111/j.1420-9101.2012.02569.x
Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16:372–380. doi:10.1016/S0169-5347(01)02198-X
Southwood TRE (1977) Habitat, the templet for ecological strategies? J Anim Ecol 46:337–365. doi:10.2307/3817
Staerkle M, Kölliker M (2008) Maternal food regurgitation to nymphs in earwigs (Forficula auricularia). Ethology 114:844–850. doi:10.1111/j.1439-0310.2008.01526.x
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Thesing J, Kramer J, Koch LK, Meunier J (2015) Short-term benefits, but transgenerational costs of maternal loss in an insect with facultative maternal care. Proc R Soc B Biol Sci 282:20151617. doi:10.1098/rspb.2015.1617
Velando A, Drummond H, Torres R (2006) Senescent birds redouble reproductive effort when ill: confirmation of the terminal investment hypothesis. Proc R Soc B Biol Sci 273:1443–1448. doi:10.1098/rspb.2006.3480
Vincze O, Székely T, Küpper C et al (2013) Local environment but not genetic differentiation influences biparental care in ten plover populations. PLoS One 8:e60998. doi:10.1371/journal.pone.0060998
Williams GC (1966) Natural selection, the costs of reproduction, and the refinement of Lack’s principle. Am Nat 100:687–690
Wirth T, Le Guellec R, Vancassel M, Veuille M (1998) Molecular and reproductive characterization of sibling species in the European earwig (Forficula auricularia). Evolution 52:260
Wong JWY, Kölliker M (2012) The effect of female condition on maternal care in the European earwig. Ethology 118:450–459. doi:10.1111/j.1439-0310.2012.02030.x
Wong JWY, Kölliker M (2014) Effects of food restriction across stages of juvenile and early adult development on body weight, survival and adult life history. J Evol Biol 27:2420–2430. doi:10.1111/jeb.12484
Acknowledgments
We thank all members of the “Team Earwig” at the University of Mainz for their help in the maintenance of animals in the laboratory. We also thank Arnaud Suwalski from the EPHE for species determination, Xavier Espalader for his help with earwig sampling, Jessica Purcell for her help in obtaining climatic data for the three tested populations and two anonymous reviewers for their comments on a previous version of this manuscript. This research was supported by the German Science Foundation (DFG; ME4179/1-1 to JM) and the ARP-EVOL grant from EPHE obtained by Claudie Doums.
Author contribution statement
TR, JK, MV and JM designed the experiment. MV collected the individuals in the field. TR and JK conducted the experiment. TR and JM analysed the data. JM wrote the first version of the manuscript, which was then commented and corrected by all co-authors.
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Communicated by Sylvain Pincebourde.
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Ratz, T., Kramer, J., Veuille, M. et al. The population determines whether and how life-history traits vary between reproductive events in an insect with maternal care. Oecologia 182, 443–452 (2016). https://doi.org/10.1007/s00442-016-3685-3
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DOI: https://doi.org/10.1007/s00442-016-3685-3