Assessing age, breeding stage, and mating activity as drivers of variation in the reproductive microbiome of female tree swallows

Hernandez, Jessica; Hucul, Catherine; Reasor, Emily; Smith, Taryn J; McGlothlin, Joel W.; Haak, David C.; Belden, Lisa K.; Moore, Ignacio T.

doi:10.1002/ece3.7929

Cited by 13 publications

(14 citation statements)

References 113 publications

(154 reference statements)

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“…We did not find consistent differences between the microbiomes of S. occidentalis males and females, which differs from other research on S. virgatus that found consistent differences between the sexes [21]. A larger sample size, or samples from time points during the reproductive season should be examined for S. occidentalis before a lack of sex difference is generalized for the species [48,49]. Surely reproductive behaviors and physiology could also be drivers of microbial diversity [50,51], but we would not capture that relationship here given our study was conducted at the conclusion of the annual reproductive season.…”

Section: Plos Onecontrasting

confidence: 99%

“…A larger sample size, or samples from time points during the reproductive season should be examined for S . occidentalis before a lack of sex difference is generalized for the species [ 48 , 49 ]. Surely reproductive behaviors and physiology could also be drivers of microbial diversity [ 50 , 51 ], but we would not capture that relationship here given our study was conducted at the conclusion of the annual reproductive season.…”

Section: Discussionmentioning

confidence: 99%

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Cloacal microbiomes of sympatric and allopatric Sceloporus lizards vary with environment and host relatedness

Bunker

Weiss

2022

PLoS ONE

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Animals and their microbiomes exert reciprocal influence; the host’s environment, physiology, and phylogeny can impact the composition of the microbiome, while the microbes present can affect host behavior, health, and fitness. While some microbiomes are highly malleable, specialized microbiomes that provide important functions can be more robust to environmental perturbations. Recent evidence suggests Sceloporus virgatus has one such specialized microbiome, which functions to protect eggs from fungal pathogens during incubation. Here, we examine the cloacal microbiome of three different Sceloporus species (spiny lizards; Family Phrynosomatidae)–Sceloporus virgatus, Sceloporus jarrovii, and Sceloporus occidentalis. We compare two species with different reproductive modes (oviparous vs. viviparous) living in sympatry: S. virgatus and S. jarrovii. We compare sister species living in similar habitats (riparian oak-pine woodlands) but different latitudes: S. virgatus and S. occidentalis. And, we compare three populations of one species (S. occidentalis) living in different habitat types: beach, low elevation forest, and the riparian woodland. We found differences in beta diversity metrics between all three comparisons, although those differences were more extreme between animals in different environments, even though those populations were more closely related. Similarly, alpha diversity varied among the S. occidentalis populations and between S. occidentalis and S. virgatus, but not between sympatric S. virgatus and S. jarrovii. Despite these differences, all three species and all three populations of S. occcidentalis had the same dominant taxon, Enterobacteriaceae. The majority of the variation between groups was in low abundance taxa and at the ASV level; these taxa are responsive to habitat differences, geographic distance, and host relatedness. Uncovering what factors influence the composition of wild microbiomes is important to understanding the ecology and evolution of the host animals, and can lead to more detailed exploration of the function of particular microbes and the community as a whole.

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Section: Plos Onecontrasting

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Cloacal microbiomes of sympatric and allopatric Sceloporus lizards vary with environment and host relatedness

Bunker

Weiss

2022

PLoS ONE

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“…Perhaps not surprisingly, meaningful trends in microbiome structure across species and ecosystems have proved difficult to codify in many cases 6 . Studies on microbiomes of animals under wild conditions have found that they may vary as a function of factors such as host sex 7 , 8 , age 3 , 4 , 9 , reproductive state 10 , 11 , season 2 , 7 , 12 , diet 9 , 13 , 14 , and habitat 2 , 15 , 16 . These factors often are studied separately, but they can interact with one another in complex ways that make identification of causal drivers in microbiome shifts difficult to discern.…”

Section: Introductionmentioning

confidence: 99%

Wild microbiomes of striped plateau lizards vary with reproductive season, sex, and body size

Bunker

Arnold

Weiss

2022

Sci Rep

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Long-term studies of animal microbiomes under natural conditions are valuable for understanding the effects of host demographics and environmental factors on host-associated microbial communities, and how those effects interact and shift over time. We examined how the cloacal microbiome of wild Sceloporus virgatus (the striped plateau lizard) varies under natural conditions in a multi-year study. Cloacal swabs were collected from wild-caught lizards across their entire active season and over three years in southeastern Arizona, USA. Analyses of 16S rRNA data generated on the Illumina platform revealed that cloacal microbiomes of S. virgatus vary as a function of season, sex, body size, and reproductive state, and do so independently of one another. Briefly, microbial diversity was lowest in both sexes during the reproductive season, was higher in females than in males, and was lowest in females when they were vitellogenic, and microbiome composition varied across seasons, sexes, and sizes. The pattern of decreased diversity during reproductive periods with increased sociality is surprising, as studies in other systems often suggest that microbial diversity generally increases with sociality. The cloacal microbiome was not affected significantly by hibernation and was relatively stable from year to year. This study highlights the importance of long term, wide-scale microbiome studies for capturing accurate perspectives on microbiome diversity and composition in animals. It also serves as a warning for comparisons of microbiomes across species, as each may be under a different suite of selective pressures or exhibit short-term variation from external or innate factors, which may differ in a species-specific manner.

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“…In contrast, comparisons between age classes of adult wild birds are relatively few. In one previous study of Tree Swallows ( Tachycineta bicolor ), the microbiota of females of this species was assessed during the breeding season revealing that older birds had significantly higher diversity than birds in their first breeding season, possibly due to increased opportunities for mating and therefore increased contact with other birds (Hernandez et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

Intestinal microbiota of Nearctic‐Neotropical migratory birds vary more over seasons and years than between host species

et al. 2023

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Seasonal migration of Nearctic‐Neotropical passerine birds may have profound effects on the diversity and abundance of their host‐associated microbiota. Migratory birds experience seasonal change in environments and diets throughout the course of the annual cycle that, along with recurrent biological events such as reproduction, may significantly impact their microbiota. In this study, we characterize the intestinal microbiota of four closely related species of migratory Catharus thrushes at three time points of their migratory cycle: during spring migration, on the summer breeding territories and during fall migration. Using observations replicated over 3 years, we determined that microbial community diversity of Catharus thrushes was significantly different across distinct time periods of the annual cycle, whereas community composition was more similar within than across years. Elevated alpha diversity in the summer birds compared to either migratory period indicated that birds may harbour a reduced microbiota during active migration. We also found that community composition of the microbiota did not substantially differ between host species. Finally, we recovered two phyla, Cyanobacteria and Planctomycetota, which are not commonly described from birds, that were in relatively high abundance in specific years. This study contributes to our growing understanding of how microbiota in wild birds vary throughout disparate ecological conditions and reveals potential axes across which an animal's microbial flexibility adapts to variable environments and recurrent biological conditions throughout the annual cycle.

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Assessing age, breeding stage, and mating activity as drivers of variation in the reproductive microbiome of female tree swallows

Abstract: This is an open access article under the terms of the Creat ive Commo ns Attri bution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 13 publications

References 113 publications

Cloacal microbiomes of sympatric and allopatric Sceloporus lizards vary with environment and host relatedness

Cloacal microbiomes of sympatric and allopatric Sceloporus lizards vary with environment and host relatedness

Wild microbiomes of striped plateau lizards vary with reproductive season, sex, and body size

Intestinal microbiota of Nearctic‐Neotropical migratory birds vary more over seasons and years than between host species

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