• This record comes from PubMed

Mothers matter too: benefits of temperature oviposition preferences in newts

. 2011 ; 6 (8) : e23842. [epub] 20110824

Language English Country United States Media print-electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

The maternal manipulation hypothesis states that ectothermic females modify thermal conditions during embryonic development to benefit their offspring (anticipatory maternal effect). However, the recent theory suggests that the ultimate currency of an adaptive maternal effect is female fitness that can be maximized also by decreasing mean fitness of individual offspring. We evaluated benefits of temperature oviposition preferences in Alpine newts (Ichthyosaura [formerly Triturus] alpestris) by comparing the thermal sensitivity of maternal and offspring traits across a range of preferred oviposition temperatures (12, 17, and 22°C) and by manipulating the egg-predation risk during oviposition in a laboratory thermal gradient (12-22°C). All traits showed varying responses to oviposition temperatures. Embryonic developmental rates increased with oviposition temperature, whereas hatchling size and swimming capacity showed the opposite pattern. Maternal oviposition and egg-predation rates were highest at the intermediate temperature. In the thermal gradient, females oviposited at the same temperature despite the presence of caged egg-predators, water beetles (Agabus bipustulatus). We conclude that female newts prefer a particular temperature for egg-deposition to maximize their oviposition performance rather than offspring fitness. The evolution of advanced reproductive modes, such as prolonged egg-retention and viviparity, may require, among others, the transition from selfish temperature preferences for ovipositon to the anticipatory maternal effect.

See more in PubMed

Mousseau TA, Fox CW, editors. New York: Oxford University Press; 1998. Maternal effects as adaptations.390

Marshall DJ, Uller T. When is a maternal effect adaptive? Oikos. 2007;116:1957–1963.

Fox CW, Thakar MS, Mousseau TA. Egg size plasticity in a seed beetle: an adaptive maternal effect. American Naturalist. 1997;149:149–163.

Einum S, Fleming IA. Highly fecund mothers sacrifice offspring survival to maximize fitness. Nature. 2000;405:565–567. PubMed

Einum S, Fleming IA. Environmental unpredictability and offspring size: conservative versus diversified bet-hedging. Evolutionary Ecology Research. 2004;6:443–455.

Crean AJ, Marshall DJ. Coping with environmental uncertainty: dynamic bet hedging as a maternal effect. Philosophical Transactions of the Royal Society B. 2009;364:1087–1096. PubMed PMC

Mayhew PJ. Herbivore host choice and optimal bad motherhood. Trends in Ecology & Evolution. 2001;16:165–167. PubMed

Kingsolver JG. Thermal and hydric aspects of environmental heterogeneity in the pitcher plant mosquito. Ecological Monographs. 1979;49:357–376.

Shine R, Harlow PS. Maternal manipulation of offspring phenotypes via nest-site selection in an oviparous lizard. Ecology. 1996;77:1808–1817.

Angilletta MJ, Sears MW, Pringle RM. Spatial dynamics of nesting behavior: Lizards shift microhabitats to construct nests with beneficial thermal properties. Ecology. 2009;90:2933–2939. PubMed

Feder ME, Blair N, Figueras H. Oviposition site selection: Unresponsiveness of Drosophila to cues of potential thermal stress. Animal Behaviour. 1997;53:585–588.

Webb JK, Shine R, Christian KA. The adaptive significance of reptilian viviparity in the tropics: Testing the maternal manipulation hypothesis. Evolution. 2006;60:115–122. PubMed

Gotthard K, Berger D, Walters R. What keeps insects small? Time limitation during oviposition reduces the fecundity benefit of female size in a butterfly. American Naturalist. 2007;169:768–779. PubMed

Carriére Y, Boivin G. Evolution of thermal sensitivity of parasitization capacity in egg parasitoids. Evolution. 1997;51:2028–2032. PubMed

Binckley CA, Resetarits WJ. Oviposition behavior partitions aquatic landscapes along predation and nutrient gradients. Behavioral Ecology. 2008;19:552–557.

Dvořák J, Gvoždík L. Oviposition preferences in newts: Does temperature matter? Ethology. 2009;115:533–539.

Garner TWJ, Schmidt BR. Relatedness, body size and paternity in the alpine newt, Triturus alpestris. Proceedings of the Royal Society of London Series B. 2003;270:619–624. PubMed PMC

Bauwens D, Thoen C. Escape tactics and vulnerability to predation associated with reproduction in the lizard Lacerta vivipara. Journal of Animal Ecology. 1981;50:733–743.

Seigel RA, Huggins MM, Ford NB. Reduction in locomotor ability as a cost of reproduction in snakes. Oecologia. 1987;73:480–485. PubMed

Plaut I. Does pregnancy affect swimming performance of female mosquitofish, Gambusia affinis?. Functional Ecology. 2002;16:290–295.

Dvořák J, Gvoždík L. Adaptive accuracy of temperature oviposition preferences in newts. Evolutionary Ecology. 2010;24:1115–1127.

Resetarits WJ, Jr, Wilbur HM. Choice of oviposition site by Hyla chrysoscelis role of predators and competitors. Ecology. 1989;70:220–228.

Hopey ME, Petranka JW. Vol. 1994. Copeia; 1994. Restriction of wood frogs to fish-free habitats: how important is adult choice? pp. 1023–1025.

Rieger JF, Binckley CA, Resetarits WJ. Larval performance and oviposition site preference along a predation gradient. Ecology. 2004;85:2094–2099.

Griffiths RA. London: Academic Press; 1996. Newts and salamanders of Europe.224

Miaud C. Predation of newt eggs (Triturus alpestris and T. helveticus) - Identification of predators and protective role of oviposition behavior. Journal of Zoology. 1993;231:575–582.

Orizaola G, Braña F. Oviposition behaviour and vulnerability of eggs to predation in four newt species (genus Triturus). Herpetological Journal. 2003;13:121–124.

Quinn GP, Keough MJ. Cambridge: Cambridge University Press; 2002. Experimental design and data analysis for biologists.556

Faraway JJ. Boca Raton, FL: Chapman&Hall/CRC; 2006. Extending the linear model with R.312

Blaustein L, Kiflawi M, Eitam A, Mangel M, Cohen JE. Oviposition habitat selection in response to risk of predation in temporary pools: mode of detection and consistency across experimental venue. Oecologia. 2004;138:300–305. PubMed

Kingsolver JG, Gomulkiewicz R. Environmental variation and selection on performance curves. Integrative and Comparative Biology. 2003;43:470–477. PubMed

Wolf JB, Brodie ED. The coadaptation of parental and offspring characters. Evolution. 1998;52:299–308. PubMed

Wolf JB, Wade MJ, Brodie ED . The genotype-environment interaction and evolution when the environment contains genes. In: DeWitt TJ, Scheiner SM, editors. Phenotypic plasticity. Functional and conceptual approaches. Oxford: Oxford University Press; 2004. pp. 173–190.

Měráková E, Gvoždík L. Thermal acclimation of swimming performance in newt larvae: the influence of diel temperature fluctuations during embryogenesis. Functional Ecology. 2009;23:989–995.

Pivnick KA, McNeil JN. Sexual difterences in the thermoregulation of Thymelicus lineola adults (Lepidoptera: Hesperiidae). Ecology. 1986;67:1024–1035.

Jaenike J. On optimal oviposition behavior in phytophagous insects. Theoretical Population Biology. 1978;14:350–356. PubMed

Mangel M. Oviposition site selection and clutch size in insects. Journal of Mathematical Biology. 1987;25:1–22.

Doak P, Kareiva PM, Kingsolver JG. Fitness consequences of choosy oviposition for a time-limited butterfly. Ecology. 2006;87:395–408. PubMed

Packard GC, Elinson RP, Gavaud J, Guillete JR, Lombardi J, et al. How are reproductive systems integrated and how has viviparity evolved? In: Wake DB, Roth G, editors. Complex organismal functions: integration and evolution in vertebrates. Chichester: John Wiley and Sons; 1989. pp. 281–293.

Blackburn DG. Reptilian viviparity: past research, future directions, and appropriate models. Comparative Biochemistry and Physiology A. 2000;127:391–409. PubMed

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...