Convergence in biomineralization patterns across animal eggshells

Faraday Discussions, vol. 261, pp. 212–230

Abstract

Shelled eggs are key components of animal reproduction on land, evolving independently in distant lineages of terrestrial animals including nematodes, gastropods, annelids, arthropods and chordates. They perform critical functions such as the exchange of gases between embryo and the environment, desiccation avoidance and protection from harmful radiation, microbial infection and mechanical damage. A core mechanism behind eggshell multifunctionality is the incorporation of biominerals (mainly calcium carbonate and calcium phosphate) into the shell. Very little is known about eggshell structure in invertebrates, but some recent pioneering studies have proposed that similar mineralization patterns may have evolved convergently in eggshells of pulmonate gastropods, some insects, and vertebrates. However, because a detailed characterization of the structural and chemical composition of invertebrate eggshells is not available, it has not been possible to test this hypothesis. Here, we use computed tomography, electron microscopy, electron backscatter diffraction analyses, atomic force microscopy, spectroscopy, and histochemistry to characterize and compare microstructure and chemical composition of pulmonate gastropod, insect and vertebrate eggshells. These techniques revealed the universal presence of an organic matrix in mineralized eggshells. However, disparities in the distribution of calcium throughout the shell, crystallographic orientation that appears random in invertebrates (but not vertebrates), and presence of different calcium types including the rare and unstable vaterite highlight divergence whose functional significance should be the subject of future study.

Authors 8

1. Gerben Debruyn corresponding

   Ghent University

   Affiliation as printed

   Department of Biology, Evolution and Optics of Nanostructures Group, Ghent University, Karel Lodewijk Ledeganckstraat 35, 9000 Gent, Belgium

2. Seung Hyun Choi

   Seoul National University

   Affiliation as printed

   Research Institute of Basic Sciences, Seoul National University, Seoul 08826, South Korea

3. Jessica L. Dobson

   Ghent University

   Affiliation as printed

   Department of Biology, Evolution and Optics of Nanostructures Group, Ghent University, Karel Lodewijk Ledeganckstraat 35, 9000 Gent, Belgium

4. Yana Maudens

   Ghent University

   Affiliation as printed

   Center for Textile Science and Engineering, Faculty of Engineering and Architecture, Ghent University, Tech Lane Science Park 70a, B-9052 Ghent, Belgium

5. Karen De Clerck

   Ghent University

   Affiliation as printed

   Center for Textile Science and Engineering, Faculty of Engineering and Architecture, Ghent University, Tech Lane Science Park 70a, B-9052 Ghent, Belgium

6. Matthew D. Shawkey

   Ghent University

   Affiliation as printed

   Department of Biology, Evolution and Optics of Nanostructures Group, Ghent University, Karel Lodewijk Ledeganckstraat 35, 9000 Gent, Belgium

7. Shukang Zhang

   Chinese Academy of Sciences · Institute of Vertebrate Paleontology and Paleoanthropology

   Affiliation as printed

   Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China

8. Liliana D’Alba corresponding Aachen Naturalis Biodiversity Center

   Naturalis Biodiversity Center

   Affiliation as printed

   Naturalis Biodiversity Center, Darwinweg 2, 2333 CR Leiden, Netherlands