Carefully controlled gas exchange across the eggshell is essential for the development of the avian embryo. Water vapour conductance (G(H2O)) across the shell, typically measured as mass loss during incubation, has been demonstrated to optimally ensure the healthy development of the embryo while avoiding desiccation. Accordingly, eggs exposed to sub-optimal gas exchange have reduced hatching success. We tested the association between eggshell G(H2O) and putative life-history correlates of adult birds, ecological nest parameters and physical characteristics of the egg itself to investigate how variation in G(H2O) has evolved to maintain optimal water loss across a diverse set of nest environments. We measured gas exchange through eggshell fragments in 151 British breeding bird species and fitted phylogenetically controlled, general linear models to test the relationship between G(H2O) and potential predictor parameters of each species. Of our 17 life-history traits, only two were retained in the final model: wet-incubating parent and nest type. Eggs of species where the parent habitually returned to the nest with wet plumage had significantly higher G(H2O) than those of parents that returned to the nest with dry plumage. Eggs of species nesting in ground burrows, cliffs and arboreal cups had significantly higher G(H2O) than those of species nesting on the ground in open nests or cups, in tree cavities and in shallow arboreal nests. Phylogenetic signal (measured as Pagel's λ) was intermediate in magnitude, suggesting that differences observed in the G(H2O) are dependent upon a combination of shared ancestry and species-specific life history and ecological traits. Although these data are correlational by nature, they are consistent with the hypothesis that parents constrained to return to the nest with wet plumage will increase the humidity of the nest environment, and the eggs of these species have evolved a higher G(H2O) to overcome this constraint and still achieve optimal water loss during incubation. We also suggest that eggs laid in cup nests and burrows may require a higher G(H2O) to overcome the increased humidity as a result from the confined nest microclimate lacking air movements through the nest. Taken together, these comparative data imply that species-specific levels of gas exchange across avian eggshells are variable and evolve in response to ecological and physical variation resulting from parental and nesting behaviours.

Department of Animal and Plant Sciences University of Sheffield Sheffield S10 2TN UK

Department of Psychology Hunter College and the Graduate Center of the City University of New York 695 Park Avenue New York NY 10065 USA

Department of Zoology and Laboratory of Ornithology Palacký University Olomouc CZ 771 46 Czech Republic

School of Earth and Environmental Sciences University of Adelaide SA 5005 Australia

Structure and Motion Laboratory The Royal Veterinary College University of London North Mymms Hatfield Herts AL9 7TA UK

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Ackerman R. A., Platter-Reiger M. (1979). Water loss by pied-billed grebe (

Andersen O., Steen J. B. (1986). Water economy in bird nests.

Ar A., Rahn H. (1978). Interdependence of gas exchange conductance, incubation length and weight of the avian egg. In

Ar A., Rahn H. (1980). Water in the avian egg: overall budget of incubation.

Ar A., Paganelli C. V., Reeves R. B., Greene D. G., Rahn H. (1974). The avian egg: water vapour conductance, shell thickness and functional pore area.

Arad Z., Gavrieli-Levin I., Marder J. (1988). Adaptation of the pigeon egg to incubation in dry hot environments.

Barrott H. G. (1937). Effect of temperature, humidity, and other factors on hatch of hens' eggs and on energy metabolism of chick embryos. Technical Bulletin, Vol. 553 Washington, DC: USDA;

Benson D. A., Karsch-Mizrachi I., Lipman D. J., Ostell J., Wheeler D. L. (2007). GenBank. PubMed PMC

Board R. G. (1982). Properties of avian eggshells and their adaptive value.

Booth D. T., Seymour R. S. (1987). Effect of eggshell thinning on water vapour conductance of malleefowl eggs.

Brulez K., Choudhary P. K., Maurer G., Portugal S. J., Boulton R. L., Webber S. L., Cassey P. (2014). A note on the repeatability of visually scoring eggshell patterns.

Buhr R. J. (1995). Incubation relative humidity effects on allantoic fluid volume and hatchability. PubMed

Carey C. (1980). Physiology of the avian egg.

Carey C. (1994). Structural and physiological differences between montane and lowland avian eggs and embryos.

Carey C., Leon-Velarde F., Dunin-Borkowski O., Bucher T. L., de la Torre G., Espinoza D., Monge C. (1989). Variation in eggshell characteristics and gas exchange of montane and lowland coot eggs.

Carey C., Leon-Velarde F., Monge C. (1990). Eggshell conductance and other physical characteristics of avian eggs laid in the Peruvian Andes.

Cassey P., Portugal S. J., Maurer G., Ewen J. G., Boulton R. L., Hauber M. E., Blackburn T. M. (2010). Variability in avian eggshell colour: a comparative study of museum eggshells. PubMed PMC

Cassey P., Thomas G., Portugal S. J., Maurer G., Hauber M., Grim T., Lovell G., Miksik I. (2012). Why are birds' eggs colourful? Eggshell pigments co-vary with life-history and nesting ecology among British breeding non-passerine birds.

Cramp S., Simmons K. E. L., Perrins C. (1977-1994).

Davis T. A., Ackerman R. A. (1985). Adaptations of black tern (

Davis T. A., Platter-Reiger M. F., Ackerman R. A. (1984). Incubation water loss by pied-billed grebe eggs: adaptation to a hot, wet nest.

Deeming D. C. (2002).

Del Hoyo J., Elliot A., Sargatal J. (1992-2010).

Drummond A. J., Rambaut A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. PubMed PMC

Drummond A. J., Ashton B., Cheung M., Heled J., Kearse M., Moir R., Stones-Havas S., Thierer T., Wilson A. (2009). Geneious v4.8. Available at: http://www.geneious.com/

Dunning J. B., Jr (2007).

DuRant S. E., Hepp G. R., Moore I. T., Hopkins B. C., Hopkins W. A. (2010). Slight differences in incubation temperature affect early growth and stress endocrinology of wood duck ( PubMed

Fernandez M. S., Araya M., Arias J. L. (1997). Eggshells are shaped by a precise spatio-temporal arrangement of sequentially deposited macromolecules. PubMed

Haftorn S. (1994). The act of tremble-thrusting in tit nests, performance and possible functions.

Handrich Y. (1989). Incubation water loss in King penguin eggs. II. Does the brood patch interfere with eggshell conductance?

Hauber M. E. (2014).

Hoyt D. F., Board R. G., Rahn H., Paganelli C. V. (1979). The eggs of the Anatidae: conductance, pore structure and metabolism.

Lomholt J. P. (1976). Relationship of weight loss to ambient humidity of birds eggs during incubation.

Lomholt J. P. (1984). A preliminary study of local oxygen tensions inside bird eggs and gas exchange during early stages of embryonic development. In

Maurer G., Russell D. G. D., Cassey P. (2010). Interpreting the lists and equations of egg dimensions in Schönwetter's ‘Handbuch der Oologie’.

Maurer G., Portugal S. J., Cassey P. (2011). Speckles of cryptic black-headed gull eggs show no mechanical or conductance structural function.

Maurer G., Portugal S. J., Cassey P. (2012). A comparison of indices and measured values of eggshell thickness of different shell regions using museum eggs of 230 European bird species.

Maurer G., Portugal S. J., Hauber M. E., Mikšík I., Russell D. G. D., Cassey P. (2014). First light for avian embryos: eggshell thickness and pigmentation mediate variation in development and UV exposure in wild bird eggs.

McNaught M., Owens I. P. F. (2002). Interspecific variation in plumage colour among birds: species isolation or light environment?

Morgan S. M., Ashley-Ross M. A., Anderson D. J. (2003). Foot-mediated incubation: Nazca booby ( PubMed

Orme C. D. L., Davies R. G., Burgess M., Eigenbrod F., Pickup N., Olson V., Webster A. J., Ding T. S., Rasmussen P. C., Ridgely R. S., et al. (2005). Global hotspots of species richness are not congruent with endemism or threat. PubMed

Orme C. D. L., Davies R. G., Olson V. A., Thomas G. H., Ding T. S., Rasmussen P. C., Ridgely R. S., Stattersfield A. J., Bennett P. M., Owens I. P., et al. (2006). Global patterns of geographic range size in birds. PubMed PMC

Paganelli C. V. (1980). The physics of gas exchange across the avian eggshell.

Pagel M. (1997). Inferring evolutionary processes from phylogenies.

Pagel M. (1999). The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies.

Paradis E., Claude J., Strimmer K. (2004). APE: analyses of phylogenetics and evolution in R language. PubMed

Pérez J. H., Ardia D. R., Chad E. K., Clotfelter E. D. (2008). Experimental heating reveals nest temperature affects nestling condition in tree swallows ( PubMed PMC

Portugal S. J., Maurer G., Cassey P. (2010a). Eggshell permeability: a standard technique for determining interspecific rates of water vapor conductance. PubMed

Portugal S. J., Cooper H. J., Zampronio C. G., Wallace L. L., Cassey P. (2010b). Can museum egg specimens be used for proteomic analyses? PubMed PMC

Portugal S. J., Hauber M. E., Maurer G., Stokke B. G., Grim T., Cassey P. (2014). Rapid development of brood-parasitic cuckoo embryos cannot be explained by increased gas exchange through the eggshell.

Rahn H., Hammel H. T. (1982). Incubation water loss, shell conductance, and pore dimensions in Adelie penguin eggs.

Rahn H., Paganelli C. V. (1990). Gas fluxes in avian eggs: driving forces and the pathway for exchange.

Rahn H., Carey C., Balmas K., Bhatia B., Paganelli C. (1977). Reduction of pore area of the avian eggshell as an adaptation to altitude. PubMed PMC

Rambaut A. (2002). Se-AI: Sequence alignment editor program, Version 2.0a11. Available at http://tree.bio.ed.ac.uk/software/seal/

Ricklefs R. E. (1969). An analysis of nesting mortality in birds.

Romijn C., Roos J. (1938). The air space of the hen's egg and its changes during the period of incubation. PubMed PMC

Russell D. G. D., White J., Maurer G., Cassey P. (2010). Data-poor egg collections: tapping an important research resource.

Shackleton M., Shipman R., Ebner M. (2000). An investigation of redundant genotype-phenotype mappings and their role in evolutionary search. In

Sibley C. G., Monroe B. L. (1990).

Skutch A. F. (1976).

Sotherland P. R., Packard G. C., Taigen T. L., Boardman T. J. (1980). An altitudinal cline in conductance of cliff swallow (

Sotherland D. P., Ashen R. M., Shuman D., Tracy C. R. (1984). The water balance of bird eggs incubated in water.

Thomas G. H. (2008). Phylogenetic distributions of British birds of conservation concern. PubMed PMC

Thomas G. H., Freckleton R. P., Székely T. (2006). Comparative analyses of the influence of developmental mode on phenotypic diversification rates in shorebirds. PubMed PMC

Visschedijk A. H. J. (1980). Effects of barometric pressure and abnormal gas mixtures on gaseous exchange by the avian embryo.

Vleck C. M. (1981). Hummingbird incubation: female attentiveness and egg temperature. PubMed

Vleck C. M., Vleck D., Rahn H., Paganelli C. V. (1983). Nest microclimate, water-vapour conductance, and water loss in heron and tern eggs.

Walsberg G. E., Schmidt C. A. (1992). Effects of variable humidity on embryonic development and hatching success of mourning doves.

Yildirim I., Yetisir R. (2004). Effects of different hatcher temperatures on hatching traits of broiler embryos during the last five days of incubation.

Highly virulent avian brood-parasitic species show elevated embryonic metabolic rates at specific incubation stages compared to less virulent and non-parasitic species

Estimation of the external quality characteristics of goose eggs of known breadth and length

Adjusting risk-taking to the annual cycle of long-distance migratory birds