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Convergent evolution of reduced eggshell conductance in avian brood parasites.

ABSTRACT: Brood parasitism has evolved independently in several bird lineages, giving rise to strikingly similar behavioural adaptations that suggest convergent evolution. By comparison, convergence of physiological traits that optimize this breeding strategy has received much less attention, yet these species share many similar physiological traits that optimize this breeding strategy. Eggshell structure is important for embryonic development as it controls the flux of metabolic gases, such as O2, CO2 and H2O, into and out of the egg; in particular, water vapour conductance ( GH2O) is an essential process for optimal development of the embryo. Previous work has shown that common cuckoos ( Cuculus canorus) have a lower than expected eggshell GH2O compared with their hosts. Here, we sought to test whether this is a trait found in other independently evolved avian brood parasites, and therefore reflects a general adaptation to a parasitic lifestyle. We analysed GH2O for seven species of brood parasites from four unique lineages as well as for their hosts, and combined this with species from the literature. We found lower than expected GH2O among all our observed brood parasites both compared with hosts (except for brown-headed cowbirds ( Molothrus ater)) and compared with the expected rates given their phylogenetic positions. These findings suggest that a lowered GH2O may be a general adaptation for brood parasitism, perhaps helping the parasite nestling to develop greater aerobic fitness. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

SUBMITTER: McClelland SC

PROVIDER: S-EPMC6388047 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Convergent evolution of reduced eggshell conductance in avian brood parasites.

McClelland Stephanie C SC Jamie Gabriel A GA Waters Katy K Caldas Lara L Spottiswoode Claire N CN Portugal Steven J SJ

Philosophical transactions of the Royal Society of London. Series B, Biological sciences 20190401 1769

Brood parasitism has evolved independently in several bird lineages, giving rise to strikingly similar behavioural adaptations that suggest convergent evolution. By comparison, convergence of physiological traits that optimize this breeding strategy has received much less attention, yet these species share many similar physiological traits that optimize this breeding strategy. Eggshell structure is important for embryonic development as it controls the flux of metabolic gases, such as O<sub>2</s ...[more]

PMID: 30967076

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Project description:The avian eggshell is a remarkable biomineral, which is essential for avian reproduction; its properties permit embryonic development in the desiccating terrestrial environment, and moreover, are critically important to preserve unfertilized egg quality for human consumption. This calcium carbonate (CaCO3) bioceramic is made of 95% calcite and 3.5% organic matrix; it protects the egg contents against microbial penetration and mechanical damage, allows gaseous exchange, and provides calcium for development of the embryonic skeleton. In vertebrates, eggshell occurs in the Sauropsida and in a lesser extent in Mammalia taxa; avian eggshell calcification is one of the fastest known CaCO3 biomineralization processes, and results in a material with excellent mechanical properties. Thus, its study has triggered a strong interest from the researcher community. The investigation of eggshell biomineralization in birds over the past decades has led to detailed characterization of its protein and mineral constituents. Recently, our understanding of this process has been significantly improved using high-throughput technologies (i.e., proteomics, transcriptomics, genomics, and bioinformatics). Presently, more or less complete eggshell proteomes are available for nine birds, and therefore, key proteins that comprise the eggshell biomineralization toolkit are beginning to be identified. In this article, we review current knowledge on organic matrix components from calcified eggshell. We use these data to analyze the evolution of selected matrix proteins and underline their role in the biological toolkit required for eggshell calcification in avian species. Amongst the panel of eggshell-associated proteins, key functional domains are present such as calcium-binding, vesicle-binding and protein-binding. These technical advances, combined with progress in mineral ultrastructure analyses, have opened the way for new hypotheses of mineral nucleation and crystal growth in formation of the avian eggshell, including transfer of amorphous CaCO3 in vesicles from uterine cells to the eggshell mineralization site. The enrichment of multi-omics datasets for bird species is critical to understand the evolutionary context for development of CaCO3 biomineralization in metazoans, leading to the acquisition of the robust eggshell in birds (and formerly dinosaurs).

Dataset Information

Convergent evolution of reduced eggshell conductance in avian brood parasites.

Publications

Convergent evolution of reduced eggshell conductance in avian brood parasites.

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