Mother and offspring fitness in an insect with maternal care: phenotypic trade-offs between egg number, egg mass and egg care

BMC Evolutionary Biology

Joël Meunier¹  Lisa K Koch¹ 

[1] Department of Evolutionary Biology, Institute of Zoology, Johannes Gutenberg University of Mainz, Mainz, Germany

关键词: Earwig;    Insect;    Cost;    Reciprocal causation;    Egg cannibalism;    Parental care;    Reproduction;   

Others  :  855383
DOI  :  10.1186/1471-2148-14-125

 received in 2014-04-02, accepted in 2014-06-03,  发布年份 2014

【 摘 要 】

Background

Oviparous females have three main options to increase their reproductive success: investing into egg number, egg mass and/or egg care. Although allocating resources to either of these three components is known to shape offspring number and size, potential trade-offs among them may have key impacts on maternal and offspring fitness. Here, we tested the occurrence of phenotypic trade-offs between egg number, egg mass and maternal expenditure on egg care in the European earwig, Forficula auricularia, an insect with pre- and post-hatching forms of maternal care. In particular, we used a series of laboratory observations and experiments to investigate whether these three components non-additively influenced offspring weight and number at hatching, and whether they were associated with potential costs to females in terms of future reproduction.

Results

We found negative associations between egg number and mass as well as between egg number and maternal expenditure on egg care. However, these trade-offs could only be detected after statistically correcting for female weight at egg laying. Hatchling number was not determined by single or additive effects among the three life-history traits, but instead by pairwise interactions among them. In particular, offspring number was positively associated with the number of eggs only in clutches receiving high maternal care or consisting of heavy eggs, and negatively associated with mean egg mass in clutches receiving low care. In contrast, offspring weight was positively associated with egg mass only. Finally, maternal expenditure on egg care reduced their future reproduction, but this effect was only detected when mothers were experimentally isolated from their offspring at egg hatching.

Conclusions

Overall, our study reveals simultaneous trade-offs between the number, mass and care of eggs. It also demonstrates that these factors interact in their impact on offspring production, and that maternal expenditure on egg care possibly shapes female future reproduction. These findings emphasize that studying reproductive success requires consideration of phenotypic trade-offs between egg-number, egg mass and egg care in oviparous species.

【 授权许可】

   
2014 Koch and Meunier; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Stearns SC: The Evolution of Life Histories. Oxford: Oxford University Press; 1992.
• [2]Krist M: Egg size and offspring quality: a meta-analysis in birds. Biol Rev Camb Philos Soc 2011, 86:692-716.
• [3]Smiseth PT, Kölliker M, Royle NJ: What is Parental Care? In The Evolution of Parental Care. Oxford Uni. Oxford: Oxford University Press; 2012.
• [4]Berrigan D: The allometry of egg size and number in insects. Oikos 1991, 60:313-321.
• [5]Fox CW, Czesak ME: Evolutionary ecology of progeny size in arthropods. Annu Rev Entomol 2000, 45:341-369.
• [6]Hendry AP, Day T, Cooper AB: Optimal size and number of propagules: allowance for discrete stages and effects of maternal size on reproductive output and offspring fitness. Am Nat 2001, 157:387-407.
• [7]Smiseth PT, Andrews CP, Mattey SN, Mooney R: Phenotypic variation in resource acquisition influences trade-off between number and mass of offspring in a burying beetle. J Zool 2014, 293:80-83.
• [8]Shine R: Alternative models for the evolution of offspring size. Am Nat 1989, 134:311-317.
• [9]Shine R: Propagule size and parental care: the “safe harbor” hypothesis. J Theor Biol 1978, 75:417-424.
• [10]Nussbaum RA, Schultz DL: Coevolution of parental care and egg size. Am Nat 1989, 133:591-603.
• [11]Sargent RC, Taylor PD, Gross MR: Parental care and the evolution of egg size in fishes. Am Nat 1987, 129:32-46.
• [12]Summers K, Sea McKeon C, Heying H: The evolution of parental care and egg size: a comparative analysis in frogs. Proc R Soc B Biol Sci 2006, 273:687-692.
• [13]Simpson MR: Convariation of spider egg and clutch size: the influence of foraging and parental care. Ecology 1995, 76:795-800.
• [14]Gilbert JDJ, Manica A: Parental care trade-offs and life-history relationships in insects. Am Nat 2010, 176:212-226.
• [15]De Fraipont M, Clobert J, Barbault R: The evolution of oviparity with egg guarding and viviparity in lizards and snakes: a phylogenetic analysis. Evolution 1996, 50:391-400.
• [16]Oliveira RF, Taborsky M, Brockmann HJ: Alternative Reproductive Tactics: An Integrative Approach. Cambridge: Cambridge University Press; 2008.
• [17]Lock JE, Smiseth PT, Moore PJ, Moore AJ: Coadaptation of prenatal and postnatal maternal effects. Am Nat 2007, 170:709-718.
• [18]Kölliker M: Benefits and costs of earwig (Forficula auricularia) family life. Behav Ecol Sociobiol 2007, 61:1489-1497.
• [19]Meunier J, Wong JWY, Gómez Y, Kuttler S, Röllin L, Stucki D, Kölliker M: One clutch or two clutches? Fitness correlates of coexisting alternative female life-histories in the European earwig. Evol Ecol 2012, 26:669-682.
• [20]Boos S, Meunier J, Pichon S, Kolliker M: Maternal care provides antifungal protection to eggs in the European earwig. Behav Ecol(doi:10.1093/beheco/aru046)
• [21]Costa JT: Dermaptera. Earwig Mothers. In The Other Insect Societies. Cambridge, Massachusetts & London, England: The Belknap Press of Harvard University Press; 2006:49-80.
• [22]Meunier J, Kölliker M: When it is costly to have a caring mother: food limitation erases the benefits of parental care in earwigs. Biol Lett 2012, 8:547-550.
• [23]Kölliker M, Vancassel M: Maternal attendance and the maintenance of family groups in common earwigs (Forficula auricularia): a field experiment. Ecol Entomol 2007, 32:24-27.
• [24]Dobler R, Kölliker M: Influence of weight asymmetry and kinship on siblicidal and cannibalistic behaviour in earwigs. Anim Behav 2011, 82:667-672.
• [25]Falk J, Wong JWY, Kölliker M, Meunier J: Sibling cooperation in earwig families provides insights into the early evolution of social life. Am Nat 2014, 183:547-557.
• [26]Van Noordwijk AJ, de Jong G: Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 1986, 128:137-142.
• [27]Smith CC, Fretwell SD: The optimal balance between size and number of offspring. Am Nat 1974, 108:499-506.
• [28]Parker GA, Begon M: Optimal egg size and clutch size: effects of environment and maternal phenotype. Am Nat 1986, 128:573-592.
• [29]Wheatley KE, Bradshaw CJ a, Davis LS, Harcourt RG, Hindell M a: Influence of maternal mass and condition on energy transfer in Weddell seals. J Anim Ecol 2006, 75:724-733.
• [30]Jamieson SE: Body mass dynamics during incubation and duration of parental care in Pacific Dunlins Calidris alpina pacifica: a test of the differential parental capacity hypothesis. Ibis 2012, 154:838-845.
• [31]Wong JWY, Kölliker M: The effect of female condition on maternal care in the European earwig. Ethology 2012, 118:450-459.
• [32]Miehls ALJ, McAdam AG, Bourdeau PE, Peacor SD: Plastic response to a proxy cue of predation risk when direct cues are unreliable. Ecology 2013, 94:2237-2248.
• [33]Meunier J, Kölliker M: Parental antagonism and parent-offspring co-adaptation interact to shape family life. Proc R Soc B Biol Sci 2012, 279:3981-3988.
• [34]Miller JS, Zink AG: Parental care trade-offs and the role of filial cannibalism in the maritime earwig, Anisolabis maritima. Anim Behav 2012, 83:1387-1394.
• [35]Dobler R, Kölliker M: Kin-selected siblicide and cannibalism in the European earwig. Behav Ecol 2010, 21:257-263.
• [36]Wong JWY, Lucas C, Kölliker M: Cues of maternal condition influence offspring selfishness. PLoS One 2014, 9:e87214.
• [37]Elgar MA, Crespi BJ: Cannibalism: Ecology and Evolution among Diverse Taxa. Oxford: Oxford University Press; 1992.
• [38]Mock DW, Parker GA: The Evolution of Sibling Rivalry. Oxford: Oxford University Press; 1997.
• [39]Klug H, Bonsall MB: When to care for, abandon, or eat your offspring: the evolution of parental care and filial cannibalism. Am Nat 2007, 170:886-901.
• [40]Manica A: Filial cannibalism in teleost fish. Biol Rev Camb Philos Soc 2002, 77:261-277.
• [41]Meunier J, Kölliker M: Inbreeding depression in an insect with maternal care: influences of family interactions, life stage and offspring sex. J Evol Biol 2013, 26:2209-2220.
• [42]Carroll CR, Janzen DH: Ecology of foraging by ants. Annu Rev Ecol Syst 1973, 4:231-257.
• [43]Steiger S: Bigger mothers are better mothers: disentangling size-related prenatal and postnatal maternal effects. Proc R Soc B Biol Sci 2013, 280:20131225.
• [44]Monteith KM, Andrews C, Smiseth PT: Post-hatching parental care masks the effects of egg size on offspring fitness: a removal experiment on burying beetles. J Evol Biol 2012, 25:1815-1822.
• [45]Laland KN, Sterelny K, Odling-Smee J, Hoppitt W, Uller T: Cause and effect in biology revisited: is Mayr’s proximate-ultimate dichotomy still useful? Science 2011, 334:1512-1516.
• [46]Benjamini Y, Hochberg Y: Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 1995, 57:289-300.
• [47]Fox J: Effect displays in R for generalised linear models. J Stat Softw 2003, 8:1-9.
• [48]Koch LK, Meunier J: Mother and offspring fitness in an insect with maternal care: phenotypic trade-offs between egg number, egg mass and egg care. Dryadhttp://doi:10.5061/dryad.p9t05 webcite