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Factors promoting maternal trophic egg provisioning in non-eusocial animals

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Population Ecology

Abstract

The adaptive function of trophic egg-laying is generally regarded as extended parental investment to the offspring. However, the evolutionary factors promoting trophic egg-laying are still unclear, because the amount of maternal investment per offspring should be ideally equal between smaller offspring with trophic eggs and larger offspring without any additional investment. Several authors have suggested that trophic egg-laying should evolve only when egg size is constrained, but this hypothesis has not been evaluated. We investigated the evolutionary mechanisms of trophic egg-laying by two different approaches. First, we evaluated morphological constraints on egg size in two sibling ladybird species, Harmonia axyridis, which is known to produce trophic eggs, and H. yedoensis. Second, we theoretically predicted the optimal proportion of trophic eggs to total eggs and egg size in relation to environmental heterogeneity, predictability of environmental quality, and investment efficiency of trophic egg consumption. The intra- and interspecific morphological comparisons suggest that morphological constraints on the evolutionary determination of egg size are weak at best in the two ladybird species. Moreover, we theoretically showed that small egg size and trophic egg-laying are favoured in heterogeneous environments when mothers cannot adjust egg size plastically. We also showed that even a small reduction in investment efficiency makes a trophic egg strategy unlikely, despite relatively high environmental predictability. We conclude that trophic egg provisioning may be a flexible maternal adaptation to a highly heterogeneous environment rather than a response to a morphological constraint on egg size.

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References

  • Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383

    Article  Google Scholar 

  • Bauerfeind SS, Fischer K (2008) Maternal body size as a morphological constraint on egg size and fecundity in butterflies. Basic Appl Ecol 9:443–451

    Article  Google Scholar 

  • Baur B (1988) Repeated mating and female fecundity in the simultaneously hermaphroditic land snail Arianta arbustorum. Int J Invertebr Reprod Dev 14:197–204

    Article  Google Scholar 

  • Baur B (1990) Possible benefits of egg cannibalism in the land snail Arianta arbustorum (L.). Funct Ecol 4:679–684

    Article  Google Scholar 

  • Baur B, Raboud C (1988) Life history of the land snail Arianta arbustorum along an altitudinal gradient. J Anim Ecol 57:71–87

    Article  Google Scholar 

  • Berrigan D, Scheiner SM (2004) Modeling the evolution of phenotypic plasticity. In: DeWitt TJ, Scheiner SM (eds) Phenotypic plasticity: functional and conceptual approaches. Oxford University Press, Oxford, pp 82–97

    Google Scholar 

  • Christians JK (2002) Avian egg size: variation within species and inflexibility within individuals. Biol Rev 77:1–26

    Article  PubMed  Google Scholar 

  • Clark PJ, Ewert MA, Nelson CE (2001) Physical apertures as constraints on egg size and shape in the common musk turtle, Sternotherus odoratus. Funct Ecol 15:70–77

    Article  Google Scholar 

  • Congdon JD, Gibbons JW (1987) Morphological constraint on egg size: a challenge to optimal egg size theory? Proc Natl Acad Sci USA 84:4145–4147

    Article  PubMed  CAS  Google Scholar 

  • Crean AJ, Marshall DJ (2009) Coping with environmental uncertainty: dynamic bet hedging as a maternal effect. Philos Trans R Soc B 364:1087–1096

    Article  Google Scholar 

  • Crespi BJ (1992) Cannibalism and trophic egg in subsocial and eusocial insects. In: Elgar MA, Crespi BJ (eds) Cannibalism: ecology and evolution among diverse taxa. Oxford University Press, Oxford, pp 176–213

    Google Scholar 

  • Crump ML (1981) Variation in propagule size as a function of environmental uncertainty for tree frogs. Am Nat 117:724–737

    Article  Google Scholar 

  • Dall SRX, Giraldeau LA, Olsson O, McNamara JM, Stephens DW (2005) Information and its use by animals in evolutionary ecology. Trends Ecol Evol 20:187–193

    Article  PubMed  Google Scholar 

  • Dixon AFG (1998) Aphid ecology. Chapman and Hall, London

    Google Scholar 

  • Dixon AFG (2000) Insect predator–prey dynamics: ladybird beetles and biological control. Cambridge University Press, Cambridge

    Google Scholar 

  • Dixon AFG, Guo Y (1993) Egg and cluster size in ladybird beetles (Coleoptera: Coccinellidae): the direct and indirect effects of aphid abundance. Eur J Entomol 90:457–463

    Google Scholar 

  • Einum S, Fleming IA (2004) Environmental unpredictability and offspring size: conservative versus diversified bet-hedging. Evol Ecol Res 6:443–455

    Google Scholar 

  • Elgar MA, Crespi BJ (1992) Cannibalism: ecology and evolution among diverse taxa. Oxford University Press, Oxford

    Google Scholar 

  • Fischer K, Zwaan BJ, Brakefield PM (2002) How does egg size relate to body size in butterflies? Oecologia 131:375–379

    Article  Google Scholar 

  • Fischer B, Taborsky B, Kokko H (2011) How to balance the offspring quality–quantity tradeoff when environmental cues are unreliable. Oikos 120:258–270

    Article  Google Scholar 

  • Fox CW, Czesak ME (2000) Evolutionary ecology of progeny size in arthropods. Annu Rev Entomol 45:341–369

    Article  PubMed  CAS  Google Scholar 

  • Fox CW, Thakar MS, Mousseau TA (1997) Egg size plasticity in a seed beetle: an adaptive maternal effect. Am Nat 149:149–163

    Article  Google Scholar 

  • Gibson RC, Buley KR (2004) Maternal care and obligatory oophagy in Leptodactylus fallax: a new reproductive mode in frogs. Copeia 2004:128–135

    Article  Google Scholar 

  • Gilbert F (1990) Size, phylogeny and life-history in the evolution of feeding specialization in insect predators. In: Gilbert F (ed) Insect life cycles: genetics, evolution and co-ordination. Springer, New York, pp 101–124

    Google Scholar 

  • Gobin B, Peeters C, Billen J (1998) Production of trophic eggs by virgin workers in the ponerine ant Gnamptogenys menadensis. Physiol Entomol 23:329–336

    Article  Google Scholar 

  • Hemptinne JL, Dixon AFG, Coffin J (1992) Attack strategy of ladybird beetles (Coccinellidae): factors shaping their numerical response. Oecologia 90:238–245

    Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Massachusetts

    Google Scholar 

  • Ji X, Du WG, Li H, Lin LH (2006) Experimentally reducing clutch size reveals a fixed upper limit to egg size in snakes, evidence from the king ratsnake, Elaphe carinata. Comp Biochem Physiol A 144:474–478

    Article  Google Scholar 

  • Kam YC, Lin CF, Lin YS, Tsal YF (1998) Density effects of oophagous tadpoles of Chirixalus eiffingeri (Anura: Rhacophoridae): importance of maternal brood care. Herpetologica 54:425–433

    Google Scholar 

  • Kawai A (1978) Sibling cannibalism in the first instar larvae of Harmonia axyridis Pallas (Coleoptera: Coccinelidae). Kontyû 46:14–19

    Google Scholar 

  • Kawecki TJ (1995) Adaptive plasticity of egg size in response to competition in the cowpea weevil, Callosobruchus maculatus (Coleoptera: Bruchidae). Oecologia 102:81–85

    Google Scholar 

  • Kudo S, Nakahira T (2004) Effects of trophic-eggs on offspring performance and rivalry in a sub-social bug. Oikos 107:28–35

    Article  Google Scholar 

  • Kudo S, Nakahira T (2005) Trophic-egg production in a subsocial bug: adaptive plasticity in response to resource conditions. Oikos 111:459–464

    Article  Google Scholar 

  • Kudo S, Nakahira T, Saito Y (2006) Morphology of trophic eggs and ovarian dynamics in the subsocial bug Adomerus triguttulus (Heteroptera: Cydnidae). Can J Zool 84:723–728

    Article  Google Scholar 

  • Leather SR, Burnand AC (1987) Factors affecting life-history parameters of the pine beauty moth, Panolis flammea (D & S): the hidden costs of reproduction. Funct Ecol 1:331–338

    Article  Google Scholar 

  • Majerus TMO, Majerus MEN, Knowles B, Wheeler J, Bertrand D, Kuznetzov VN, Ueno H, Hurst GDD (1998) Extreme variation in the prevalence of inherited male-killing microorganisms between three populations of Harmonia axyridis (Coleoptera: Coccinellidae). Heredity 81:683–691

    Article  Google Scholar 

  • Marshall DJ, Uller T (2007) When is a maternal effect adaptive? Oikos 116:1957–1963

    Article  Google Scholar 

  • Marshall DJ, Bonduriansky R, Bussière LF (2008) Offspring size variation within broods as a bet-hedging strategy in unpredictable environments. Ecology 89:2506–2517

    Article  PubMed  Google Scholar 

  • McGinley MA, Temme DH, Geber MA (1987) Parental investment in offspring in variable environments: theoretical and empirical considerations. Am Nat 130:370–398

    Article  Google Scholar 

  • Mizumoto M, Nakasuji F (2007) Egg size manipulation in the migrant skipper Parnara guttata guttata (Lepdoptera: Hesperiidae), in response to different host plants. Popul Ecol 49:135–140

    Article  Google Scholar 

  • Mock DW, Parker GA (1997) The evolution of sibling rivalry. Oxford University Press, Oxford

    Google Scholar 

  • Nomakuchi S, Filippi L, Hironaka M (2001) Nymphal occurrence pattern and predation risk in the subsocial shield bug, Parastrachia japonensis (Heteroptera: Cydnidae). Appl Entomol Zool 36:209–212

    Article  Google Scholar 

  • Noriyuki S, Kishi S, Nishida T (2010) Seasonal variation of egg size and shape in Ypthima multistriata (Lepidoptera: Satyridae) in relation to maternal body size as a morphological constraint. Ann Entomol Soc Am 103:580–584

    Article  Google Scholar 

  • Noriyuki S, Osawa N, Nishida T (2011) Prey capture performance in hatchlings of two sibling Harmonia ladybird species in relation to maternal investment through sibling cannibalism. Ecol Entomol 36:282–289

    Article  Google Scholar 

  • Osawa N (1989) Sibling and non-sibling cannibalism by larvae of a lady beetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in the field. Res Popul Ecol 31:153–160

    Article  Google Scholar 

  • Osawa N (1992a) Sibling cannibalism in the ladybird beetle Harmonia axyridis Pallas: fitness consequences for mothers and offspring. Res Popul Ecol 34:45–55

    Article  Google Scholar 

  • Osawa N (1992b) A life table of the ladybird beetle Harmonia axyridis Pallas (Coleoptera, Coccinellidae) in relation to the aphid abundance. Jap J Entomol 60:575–579

    Google Scholar 

  • Osawa N (2000) Population field studies on the aphidophagous ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae): resource tracking and population characteristics. Popul Ecol 42:115–127

    Article  Google Scholar 

  • Osawa N, Ohashi K (2008) Sympatric coexistence of sibling species Harmonia yedoensis and H. axyridis (Coleoptera: Coccinellidae) and the roles of maternal investment through egg and sibling cannibalism. Eur J Entomol 105:445–454

    Google Scholar 

  • Osawa N, Yoshinaga A (2009) The presence of micropyles in the shells of developing and undeveloped eggs of the ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 106:607–610

    Google Scholar 

  • Parker GA, Begon M (1986) Optimal egg size and clutch size: effects of environment and maternal phenotype. Am Nat 128:573–592

    Article  Google Scholar 

  • Parker GA, Royle NJ, Hartley IR (2002) Intrafamilial conflict and parental investment: a synthesis. Philos Trans R Soc B 357:295–307

    Article  Google Scholar 

  • Perry JC, Roitberg BD (2005a) Ladybird mothers mitigate offspring starvation risk by laying trophic eggs. Behav Ecol Sociobiol 58:578–586

    Article  Google Scholar 

  • Perry JC, Roitberg BD (2005b) Games among cannibals: competition to cannibalize and parent-offspring conflict lead to increased sibling cannibalism. J Evol Biol 18:1523–1533

    Article  PubMed  CAS  Google Scholar 

  • Perry JC, Roitberg BD (2006) Trophic egg laying: hypotheses and tests. Oikos 112:706–714

    Article  Google Scholar 

  • Polis GA (1984) Intraspecific predation and “infant killing” among invertebrates. In: Hausfater G, Hrdy SB (eds) Infanticide: comparative and evolutionary perspectives. Aldine De Gruyter, Berlin, pp 87–104

    Google Scholar 

  • Rollinson N, Brooks R (2008) Optimal offspring provisioning when egg size is “constrained”: a case study with the painted turtle Chrysemys picta. Oikos 117:144–151

    Article  Google Scholar 

  • Sakagami SF (1982) Stingless bees. In: Hermann HR (ed) Social insects, vol 3. Academic Press, Massachusetts, pp 362–424

    Google Scholar 

  • Sakai S, Harada Y (2001) Why do large mothers produce large offspring? Theory and a test. Am Nat 157:348–359

    Article  PubMed  CAS  Google Scholar 

  • Sasaji H (1998) Natural history of the ladybirds. University of Tokyo Press, Tokyo (in Japanese)

    Google Scholar 

  • Sinervo B, Licht P (1991) Hormonal and physiological control of clutch size, egg size, and egg shape in side-blotched lizards (Uta stansburiana): constraints on the evolution of lizard life histories. J Exp Zool 257:252–264

    Article  CAS  Google Scholar 

  • Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108:499–506

    Article  Google Scholar 

  • Soares AO, Coderre D, Schanderl H (2001) Fitness of two phenotypes of Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 98:287–293

    Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. Freeman, New York

    Google Scholar 

  • Stewart LA, Hemptinne JL, Dixon AFG (1991a) Reproductive tactics of ladybird beetles: relationship between egg size, ovariole number and developmental time. Funct Ecol 5:380–385

    Article  Google Scholar 

  • Stewart LA, Dixon AFG, Ruzicka Z, Iperti G (1991b) Clutch and egg size in ladybird beetles. Entomophaga 36:93–97

    Article  Google Scholar 

  • Takakura K (2004) Variation in egg size within and among generations of the bean weevil, Bruchidius dorsalis (Coleoptera, Bruchidae): effects of host plant quality and paternal nutritional investment. Ann Entomol Soc Am 97:346–352

    Article  Google Scholar 

  • Trivers RL (1974) Parent-offspring conflict. Am Zool 14:249–264

    Google Scholar 

  • Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320

    Article  Google Scholar 

  • Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size structures populations. Annu Rev Ecol Syst 15:393–425

    Article  Google Scholar 

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Acknowledgments

We thank T. Nishida and N. Baba for valuable discussions, Y. Harada for advice on mathematical analyses, S. Seiter for improving English version, and M. Tokeshi and J.-Y. Ide for comments on the manuscript. We are grateful to the staff at the Botanical Garden of Kyoto University for permission to collect ladybirds. This study was supported by a Research Fellowship for Young Scientists from the Japan Society for the Promotion of Science to S. Noriyuki and K. Kawatsu, and a Grant-in-Aid for Scientific Research (Ministry of Education, Culture, Sports, Science and Technology of Japan; No. 20405047) to N. Osawa.

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Noriyuki, S., Kawatsu, K. & Osawa, N. Factors promoting maternal trophic egg provisioning in non-eusocial animals. Popul Ecol 54, 455–465 (2012). https://doi.org/10.1007/s10144-012-0317-6

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