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. 2014 Mar 20;2:e321.
doi: 10.7717/peerj.321. eCollection 2014.

Sampling Locality Is More Detectable Than Taxonomy or Ecology in the Gut Microbiota of the Brood-Parasitic Brown-headed Cowbird (Molothrus Ater)

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Sampling Locality Is More Detectable Than Taxonomy or Ecology in the Gut Microbiota of the Brood-Parasitic Brown-headed Cowbird (Molothrus Ater)

Sarah M Hird et al. PeerJ. .
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Brown-headed Cowbirds (Molothrus ater) are the most widespread avian brood parasite in North America, laying their eggs in the nests of approximately 250 host species that raise the cowbird nestlings as their own. It is currently unknown how these heterospecific hosts influence the cowbird gut microbiota relative to other factors, such as the local environment and genetics. We test a Nature Hypothesis (positing the importance of cowbird genetics) and a Nurture Hypothesis (where the host parents are most influential to cowbird gut microbiota) using the V6 region of 16S rRNA as a microbial fingerprint of the gut from 32 cowbird samples and 16 potential hosts from nine species. We test additional hypotheses regarding the influence of the local environment and age of the birds. We found no evidence for the Nature Hypothesis and little support for the Nurture Hypothesis. Cowbird gut microbiota did not form a clade, but neither did members of the host species. Rather, the physical location, diet and age of the bird, whether cowbird or host, were the most significant categorical variables. Thus, passerine gut microbiota may be most strongly influenced by environmental factors. To put this variation in a broader context, we compared the bird data to a fecal microbiota dataset of 38 mammal species and 22 insect species. Insects were always the most variable; on some axes, we found more variation within cowbirds than across all mammals. Taken together, passerine gut microbiota may be more variable and environmentally determined than other taxonomic groups examined to date.

Keywords: Brood parasite; Gut microbiota; Nature vs. nurture.


Figure 1
Figure 1. Diagrams of how the data could support the major hypotheses.
Diagrams of how the data could support the major hypotheses through dendrograms (top row) and principle coordinates analyses (bottom row), using four (fictional) cowbird microbiota samples (C01–C04) and four host species (H01–H04). (A) Cowbird microbiota may be most closely related to other cowbirds, despite their host species, the “Nature Hypothesis”. (B) Cowbird microbiota may most closely resemble their host microbiota, the “Nurture Hypothesis”. (C) Local factors may determine the gut microbiota, causing birds from different localities (LA vs. CA) to be most similar. (D) Cowbird microbiota may shift between being host-like when they are juveniles (JV) and cowbird-like when they are mature (AD), the “Convergence Hypothesis”.
Figure 2
Figure 2. Relative abundance of the top three bacterial phyla in each sample for (A) birds, (B) insects and (C) mammals with greater than 200 reads.
Locality and adult/juvenile status are shown for each bird. Insect and mammal orders are depicted by bars across the top of their graphs. Insect orders: COLeoptera, HYMenoptera, ISOptera, Lepidoptera. Mammal orders: ARTiodactyla, CARnivora, CHiroptera, Diprotodontia, Insectivora, Monotremata, PERissodactyla, PRImates, PROboscidea, RODentia, Xenarthra.
Figure 3
Figure 3. Relatedness of gut microbiota communities.
Sampling locality is more detectable than taxonomy or ecology in the gut microbiota of the brood-parasitic Brown-Headed Cowbird (Molothrus ater) (A) Dendrogram of gut microbiota relatedness based on weighted UniFrac distances; all samples rarefied to 5 018 reads; jackknifed support values are shown for nodes where support >0.70. (B) NMDS ordination of Bray–Curtis dissimilarities of microbiota composition (see Methods).
Figure 4
Figure 4. Histogram of how many times each of the categorical variables was significant.
Histogram of how many times each of the categorical variables was significant at the p < 0.05 level (out of 12 total tests, see Methods), for (A) All Birds, (B) All Louisiana Birds, (C) Cowbirds Only and (D) Hosts Only. Note some categorical variables were not applicable to some datasets (due to one or fewer individuals belonging to one or more categories). (E) The twelve test contained all permutations of two statistical tests, two distance matrices and three rarefaction levels.
Figure 5
Figure 5. Relationship between mammal, insect and bird microbiota.
(A) Principal coordinates analysis of unweighted UniFrac distances. (B) Nonmetric multidimensional scaling, using relative abundance of bacterial phyla as input (see Methods). Birds are denoted by circles (cowbirds are brown, brood hosts are blue), mammals are squares and insects are triangles. Dashed lines encapsulate all birds, all insects and all mammals.

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Grant support

The National Science Foundation (DEB-0956069 to BCC and RTB) and Sigma Xi Grants-in-Aid of Research (to SMH) funded this research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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