Abstract

Vertebrates evolved in concert with bacteria and have developed essential mutualistic relationships. Gut bacteria are vital for the postnatal development of most organs and the immune and metabolic systems and may likewise play a role during prenatal development. Prenatal transfer of gut bacteria is shown in four mammalian species, including humans. For the 92% of the vertebrates that are oviparous, prenatal transfer is debated, but it has been demonstrated in domestic chicken. We hypothesize that also non-domestic birds can prenatally transmit gut bacteria. We investigated this in medium-sized Rock pigeon (Columba livia), ensuring neonates producing fair-sized first faeces. The first faeces of 21 neonate rock pigeons hatched in an incubator, contained a microbiome (bacterial community) the composition of which resembled the cloacal microbiome of females sampled from the same population (N = 5) as indicated by multiple shared phyla, orders, families, and genera. Neonates and females shared 16.1% of the total number of OTUs present (2881), and neonates shared 45.5% of their core microbiome with females. In contrast, the five females shared only 0.3% of the 1030 female OTUs present. These findings suggest that prenatal gut bacterial transfer may occur in birds. Our results support the hypothesis that gut bacteria may be important for prenatal development and present a heritability pathway of gut bacteria in vertebrates.

Highlights

  • Gut microbes have complex symbiotic relationships with their hosts

  • Prenatal transfer ensures a direct route to new hosts, which may be especially significant for bacteria that are adapted to living in the gut and survive poorly outside a host

  • Our study shows that prenatal transfer of gut bacteria does occur in birds, supporting our hypothesis that prenatal transfer occurs in oviparous vertebrates and confirming findings in chicken [20], passerines, and fence lizards [55]

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Summary

Introduction

Gut microbes (i.e., bacteria, fungi, viruses, protists) have complex symbiotic relationships with their hosts. These relationships can be mutualistic: gut bacteria exert profound beneficial effects on host nutrition and metabolism and play a vital role in immune functioning, while they benefit from a relative constant habitat with a continuous food flow provided by the host [1,2,3,4,5]. Gut bacteria are essential for proper postnatal development [1,2,3,6,7,8], and the initial gut microbiome has life-long effects on the immunity, metabolism, and health of the host [1,9,10,11]. Host-bacteria co-evolution may have selected for gut bacteria capable of prenatal transfer and hosts controlling this prenatal process

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