The evolution of eggshell cuticle in relation to nesting ecology

Abstract

Avian eggs are at risk of microbial infection prior to and during incubation. A large number of defence mechanisms have evolved in response to the severe costs imposed by these infections. The eggshell's cuticle is an important component of antimicrobial defence, and its role in preventing contamination by microorganisms in domestic chickens is well known. Nanometer-scale cuticular spheres that reduce microbial attachment and penetration have recently been identified on eggs of several wild avian species. However, whether these spheres have evolved specifically for antimicrobial defence is unknown. Here, we use comparative data on eggshell cuticular structure and nesting ecology to test the hypothesis that birds nesting in habitats with higher risk of infection (e.g. wetter and warmer) are more likely to evolve cuticular nanospheres on their eggshells than those nesting in less risky habitats. We found that nanostructuring, present in 54 of 296 analysed species, is the ancestral condition of avian eggshells and has been retained more often in taxa that nest in humid infection-prone environments, suggesting that they serve critical roles in antimicrobial egg defence.

Eggshells as hosts of bacterial communities: An experimental test of the antimicrobial egg coloration hypothesis

“…Such factors could include natural and nest‐specific humidity, nest material composition, and environmental and nest‐specific temperatures. All of these could affect the intrinsic growth of bacteria on eggshells, the effectiveness of antimicrobial defenses, and, ultimately, embryonic viability due to trans‐shell infections (Brandl et al., 2014; Cook et al., 2003; D'Alba et al., 2016; Ruiz‐Castellano, Tomás, Ruiz‐Rodríguez, Martín‐Gálvez, & Soler, 2016). …”

“…In birds, which are exclusively oviparous, the eggshell surface and calcium carbonate matrix are host to a diverse bacterial fauna (Baggott & Graeme-Cook, 2002;Grizard, Dini-Andreote, Tieleman, & Salles, 2014;Kobayashi, Gutierrez, & Hatta, 1996), and trans-shell penetration by some microbes can be lethal to the developing embryo (Cook, Beissinger, Toranzos, Rodriguez, & Arendt, 2005;Godard, Morgan Wilson, Frick, Siegel, & Bowers, 2007). Consequently, diverse antimicrobial barriers and defenses have evolved on and within the avian egg (D'Alba, Maia, Hauber, & Shawkey, 2016;D'alba & Shawkey, 2015). Those defenses that are interior to the egg include lysozyme, ovotransferrin, and other antimicrobial proteins in the albumen and the vitelline membrane (Guyot et al, 2016;Wellman-Labadie, Picman, & Hincke, 2008).…”

A rare mineral, vaterite, acts as a shock absorber in the eggshell of a communally nesting bird

“…Furthermore, a subsequent study found that cuticular nanospheres occur most commonly on the eggs of species that nest in warm, humid environments, suggesting an antimicrobial function (D'Alba et al . ). These nanospheres are most commonly formed of hydroxyapatite or other forms of calcium phosphate (D'Alba et al .…”

“…These nanospheres are most commonly formed of hydroxyapatite or other forms of calcium phosphate (D'Alba et al . ), but vaterite may play a similar role.…”

“…In support of this hypothesis, D'Alba et al (2014) found that cuticular nanospheres of hydroxyapatite (Ca 10 (PO 4 ) 6 (OH) 2 ) had a hydrophobic effect, reducing the likelihood of bacterial attachment on the eggshells of the Australian Brushturkey Alectura lathami. Furthermore, a subsequent study found that cuticular nanospheres occur most commonly on the eggs of species that nest in warm, humid environments, suggesting an antimicrobial function (D'Alba et al 2016). These nanospheres are most commonly formed of hydroxyapatite or other forms of calcium phosphate (D'Alba et al 2016), but vaterite may play a similar role.…”