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Association between the gut microbiome and carotenoid plumage phenotype in an avian hybrid zone

The Royal Society
Proceedings of the Royal Society B
Authors:
Marcella Baiz at Pennsylvania State University
Marcella Baiz
Andrew W. Wood at Pennsylvania State University
Andrew W. Wood
David Toews at Pennsylvania State University
David Toews
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Abstract

Vertebrates host complex microbiomes that impact their physiology. In many taxa, including colourful wood-warblers, gut microbiome similarity decreases with evolutionary distance. This may suggest that as host populations diverge, so do their microbiomes, because of either tight coevolutionary dynamics, or differential environmental influences, or both. Hybridization is common in wood-warblers, but the effects of evolutionary divergence on the microbiome during secondary contact are unclear. Here, we analyse gut microbiomes in two geographically disjunct hybrid zones between blue-winged warblers (Vermivora cyanoptera) and golden-winged warblers (Vermivora chrysoptera). We performed 16S faecal metabarcoding to identify species-specific bacteria and test the hypothesis that host admixture is associated with gut microbiome disruption. Species identity explained a small amount of variation between microbiomes in only one hybrid zone. Co-occurrence of species-specific bacteria was rare for admixed individuals, yet microbiome richness was similar among admixed and parental individuals. Unexpectedly, we found several bacteria that were more abundant among admixed individuals with a broader deposition of carotenoid-based plumage pigments. These bacteria are predicted to encode carotenoid biosynthesis genes, suggesting birds may take advantage of pigments produced by their gut microbiomes. Thus, host admixture may facilitate beneficial symbiotic interactions which contribute to plumage ornaments that function in sexual selection.
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Research
Cite this article: Baiz MD, Wood AW, Toews
DPL. 2024 Association between the gut
microbiome and carotenoid plumage
phenotype in an avian hybrid zone.
Proc. R. Soc. B 291: 20240238.
https://doi.org/10.1098/rspb.2024.0238
Received: 13 February 2024
Accepted: 18 March 2024
Subject Category:
Evolution
Subject Areas:
evolution, ecology
Keywords:
microbiome, carotenoids, 16S, hybridization,
speciation, Vermivora
Author for correspondence:
Marcella D. Baiz
e-mail: mbaiz@buffalo.edu
Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
c.7159234.
Association between the gut microbiome
and carotenoid plumage phenotype in an
avian hybrid zone
Marcella D. Baiz
1
, Andrew W. Wood
2
and David P. L. Toews
2
1
Department of Biological Sciences, University at Buffalo, Buffalo, NY 14260, USA
2
Department of Biology, Pennylvania State University, University Park, PA 16802, USA
MDB, 0000-0002-1629-6737
Vertebrates host complex microbiomes that impact their physiology. In
many taxa, including colourful wood-warblers, gut microbiome similarity
decreases with evolutionary distance. This may suggest that as host
populations diverge, so do their microbiomes, because of either tight
coevolutionary dynamics, or differential environmental influences, or both.
Hybridization is common in wood-warblers, but the effects of evolutionary
divergence on the microbiome during secondary contact are unclear. Here,
we analyse gut microbiomes in two geographically disjunct hybrid zones
between blue-winged warblers (Vermivora cyanoptera) and golden-winged
warblers (Vermivora chrysoptera). We performed 16S faecal metabarcoding
to identify species-specific bacteria and test the hypothesis that host admix-
ture is associated with gut microbiome disruption. Species identity
explained a small amount of variation between microbiomes in only one
hybrid zone. Co-occurrence of species-specific bacteria was rare for admixed
individuals, yet microbiome richness was similar among admixed and par-
ental individuals. Unexpectedly, we found several bacteria that were more
abundant among admixed individuals with a broader deposition of caroten-
oid-based plumage pigments. These bacteria are predicted to encode
carotenoid biosynthesis genes, suggesting birds may take advantage of pig-
ments produced by their gut microbiomes. Thus, host admixture may
facilitate beneficial symbiotic interactions which contribute to plumage orna-
ments that function in sexual selection.
1. Introduction
Vertebrates occupy environments teeming with microscopic organisms. Moreover,
individual animals themselves serve as an ecological niche occupied by diverse
microbial communities that vary in diversity across body sites and over time
[1]. Microbiome variation between individuals can also be great; however, vari-
ation between conspecifics is often less than variation between heterospecific
individuals [2,3]. In many host taxa, the extent of gut microbiome differentiation
is positively associated with evolutionary distance, an observation called phylo-
symbiosis [4]. This may suggest that as host populations diverge, so do their
microbiomes, either as a result of tight coevolutionary dynamics with their
hosts, or reflecting differential environmental influences in allopatry, or both.
A question that has been under-explored is, what happens to these
divergent microbiomes when host populations come into secondary contact?
During allopatric divergence, differentiation of host-associated microbiomes
may lead to species-specificity. If hybridization occurs upon secondary contact,
hybrid microbiomes could include influence from both parental taxa. Because
bacteria can form intimate associations with their host and carry out important
physiological functions, hybrid offspring may carry deleterious combinations of
species-specific microbes or suffer incompatible interactions involving diver-
gent host alleles. This framework is an extension of the Dobzhansky–Muller
model of hybrid incompatibilities [5,6], which accounts for differentiation
between parental species’microbiomes [7,8].
© 2024 The Author(s) Published by the Royal Society. All rights reserved.
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