INTRODUCTION: Decreasing biotic diversity with increasing latitude is an almost universal macroecological pattern documented for a broad range of taxa, however, there have been few studies focused on changes in gut microbiota (GM) across climatic zones. METHODS: Using 16S rRNA amplicon profiling, we analyzed GM variation between temperate (Czechia) and tropical (Cameroon) populations of 99 passerine bird species and assessed GM similarity of temperate species migrating to tropical regions with that of residents/short-distance migrants and tropical residents. Our study also considered the possible influence of diet on GM. RESULTS: We observed no consistent GM diversity differences between tropical and temperate species. In the tropics, GM composition varied substantially between dry and rainy seasons and only a few taxa exhibited consistent differential abundance between tropical and temperate zones, irrespective of migration behavior and seasonal GM changes. During the breeding season, trans-Saharan migrant GM diverged little from species not overwintering in the tropics and did not show higher similarity to tropical passerines than temperate residents/short-distance migrants. Interestingly, GM of two temperate-breeding trans-Saharan migrants sampled in the tropical zone matched that of tropical residents and converged with other temperate species during the breeding season. Diet had a slight effect on GM composition of tropical species, but no effect on GM of temperate hosts. DISCUSSION: Consequently, our results demonstrate extensive passerine GM plasticity, the dominant role of environmental factors in its composition and limited effect of diet.

Department of Ecology Faculty of Science Charles University Prague Czechia

Department of Zoology Faculty of Science Charles University Prague Czechia

Institute of Vertebrate Biology Czech Academy of Sciences Brno Czechia

Montpellier SupAgro Montferrier sur Lez France

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Abdad M. Y., Abou Abdallah R., Fournier P.-E., Stenos J., Vasoo S. (2018). A concise review of the epidemiology and diagnostics of rickettsioses: Rickettsia and PubMed DOI PMC

Abe F., Ishibashi N., Shimamura S. (1995). Effect of administration of bifidobacteria and lactic acid bacteria to newborn calves and piglets. PubMed DOI

Albrecht T., Kleven O., Kreisinger J., Laskemoen T., Omotoriogun T. C., Ottosson U., et al. (2013). Sperm competition in tropical versus temperate zone birds. PubMed DOI PMC

Andreani M. L., Freitas L., Ramos E. K. S., Nery M. F. (2020). Latitudinal diversity gradient and cetaceans from the perspective of MHC genes. PubMed DOI

Bäckhed F., Ley R. E., Sonnenburg J. L., Peterson D. A., Gordon J. I. (2005). Host-bacterial mutualism in the human intestine. PubMed DOI

Benjamini Y., Hochberg Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. DOI

Berlow M., Kohl K. D., Derryberry E. P. (2020). Evaluation of non-lethal gut microbiome sampling methods in a passerine bird. DOI

Bodawatta K. H., Koane B., Maiah G., Sam K., Poulsen M., Jønsson K. A. (2021). Species-specific but not phylosymbiotic gut microbiomes of New Guinean passerine birds are shaped by diet and flight-associated gut modifications. PubMed DOI PMC

Bodawatta K. H., Sam K., Jønsson K. A., Poulsen M. (2018). Comparative analyses of the digestive tract microbiota of New Guinean passerine birds. PubMed DOI PMC

Callahan B. J., McMurdie P. J., Rosen M. J., Han A. W., Johnson A. J. A., Holmes S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. PubMed DOI PMC

Capunitan D. C., Johnson O., Terrill R. S., Hird S. M. (2020). Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea. PubMed DOI

Carter W. A., Pearson S. F., Smith A. D., McWilliams S. R., Levey D. J. (2021). Seasonal and interspecific variation in frugivory by a mixed resident-migrant overwintering songbird community. DOI

Cepák J., Klvaňa P., Škopek J., Schröpfer J., Jelínek M., Hořák D., et al. (2008).

Cox D. T. C., Brandt M. J., McGregor R., Ottosson U., Stevens M. C., Cresswell W. (2013). The seasonality of breeding in savannah birds of West Africa assessed from brood patch and juvenile occurrence. DOI

Davis N. M., Proctor D. M., Holmes S. P., Relman D. A., Callahan B. J. (2018). Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. PubMed DOI PMC

De Filippo C., Cavalieri D., Di Paola M., Ramazzotti M., Poullet J. B., Massart S., et al. (2010). Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. PubMed DOI PMC

Edgar R. C., Haas B. J., Clemente J. C., Quince C., Knight R. (2011). UCHIME improves sensitivity and speed of chimera detection. PubMed DOI PMC

Escallón C., Becker M. H., Walker J. B., Jensen R. V., Cormier G., Belden L. K., et al. (2017). Testosterone levels are positively correlated with cloacal bacterial diversity and the relative abundance of Chlamydiae in breeding male rufous-collared sparrows.

Faith D. P. (1992). Conservation evaluation and phylogenetic diversity. DOI

Fotso R. C. (1996). Seasonal breeding in birds and its implications for the conservation of biodiversity in the Oku region, Cameroon. DOI

Fry C. H., Keith S., Urban E. K. (1982).

Gillingham M. A. F., Béchet A., Cézilly F., Wilhelm K., Rendón-Martos M., Borghesi F., et al. (2019). Offspring microbiomes differ across breeding sites in a panmictic species. PubMed DOI PMC

Gomez A., Rothman J. M., Petrzelkova K., Yeoman C. J., Vlckova K., Umaña J. D., et al. (2016). Temporal variation selects for diet-microbe co-metabolic traits in the gut of PubMed DOI PMC

Green P. N., Ardley J. K. (2018). Review of the genus PubMed DOI

Grond K., Santo Domingo J. W., Lanctot R. B., Jumpponen A., Bentzen R. L., Boldenow M. L., et al. (2019). Composition and drivers of gut microbial communities in Arctic-breeding shorebirds. PubMed DOI PMC

Guarner F., Malagelada J.-R. (2003). Gut flora in health and disease. PubMed DOI

Guernier V., Hochberg M. E., Guégan J.-F. (2004). Ecology drives the worldwide distribution of human diseases. PubMed DOI PMC

Hird S. M., Sánchez C., Carstens B. C., Brumfield R. T. (2015). Comparative gut microbiota of 59 neotropical bird species. PubMed DOI PMC

Jetz W., Freckleton R. P., McKechnie A. E. (2008). Environment, migratory tendency, phylogeny and basal metabolic rate in birds. PubMed DOI PMC

Jetz W., Thomas G. H., Joy J. B., Hartmann K., Mooers A. O. (2012). The global diversity of birds in space and time. PubMed DOI

Jiang H., Lei R., Ding S.-W., Zhu S. (2014). Skewer: A fast and accurate adapter trimmer for next-generation sequencing paired-end reads. PubMed DOI PMC

Jumpertz R., Le D. S., Turnbaugh P. J., Trinidad C., Bogardus C., Gordon J. I., et al. (2011). Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. PubMed DOI PMC

Jurat-Fuentes J. L., Jackson T. A. (2012). “Chapter 8 - Bacterial entomopathogens,” in DOI

Kandler O. (1983). Carbohydrate metabolism in lactic acid bacteria. PubMed DOI

Klindworth A., Pruesse E., Schweer T., Peplies J., Quast C., Horn M., et al. (2013). Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. PubMed DOI PMC

Koch H., Schmid-Hempel P. (2011). Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. PubMed DOI PMC

Kreisinger J., Bastien G., Hauffe H. C., Marchesi J., Perkins S. E. (2015a). Interactions between multiple helminths and the gut microbiota in wild rodents. PubMed DOI PMC

Kreisinger J., Čížková D., Kropáčková L., Albrecht T. (2015b). Cloacal microbiome structure in a long-distance migratory bird assessed using deep 16sRNA pyrosequencing. PubMed DOI PMC

Kreisinger J., Kropáčková L., Petrželková A., Adámková M., Tomášek O., Martin J.-F., et al. (2017). Temporal stability and the effect of transgenerational transfer on fecal microbiota structure in a long distance migratory bird. PubMed DOI PMC

Kropáčková L., Těšický M., Albrecht T., Kubov čiak J., Čížková D., Tomášek O., et al. (2017). Co-diversification of gastrointestinal microbiota and phylogeny in passerines is not explained by ecological divergence. PubMed DOI

Lee S. C., Tang M. S., Lim Y. A. L., Choy S. H., Kurtz Z. D., Cox L. M., et al. (2014). Helminth colonization is associated with increased diversity of the gut microbiota. PubMed DOI PMC

Lewis W. B., Moore F. R., Wang S. (2016a). Changes in gut microbiota of migratory passerines during stopover after crossing an ecological barrier. DOI

Lewis W. B., Moore F. R., Wang S. (2016b). Characterization of the gut microbiota of migratory passerines during stopover along the northern coast of the Gulf of Mexico. DOI

Li M., Bolker B. (2019). DOI

Ljungh A., Wadström T. (2006). Lactic acid bacteria as probiotics. PubMed

Love M. I., Huber W., Anders S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. PubMed DOI PMC

Macpherson A. J., Harris N. L. (2004). Interactions between commensal intestinal bacteria and the immune system. PubMed DOI

Martin T. E., Martin P. R., Olson C. R., Heidinger B. J., Fontaine J. J. (2000). Parental care and clutch sizes in North and South American birds. PubMed DOI

McCoy E. D., Connor E. F. (1980). Latitudinal gradients in the species diversity of North American mammals. PubMed DOI

McWilliams S. R., Karasov W. H. (2001). Phenotypic flexibility in digestive system structure and function in migratory birds and its ecological significance. PubMed DOI

Moreno J., Briones V., Merino S., Ballesteros C., Sanz J. J., Tomás G. (2003). Beneficial effects of cloacal bacteria on growth and fledging size in nestling pied flycatchers ( DOI

Norris D. R., Marra P. P., Kyser T. K., Sherry T. W., Ratcliffe L. M. (2004). Tropical winter habitat limits reproductive success on the temperate breeding grounds in a migratory bird. PubMed DOI PMC

Nunn C. L., Altizer S. M., Sechrest W., Cunningham A. A. (2005). Latitudinal gradients of parasite species richness in primates. DOI

Nwaogu C. J., Tieleman B. I., Cresswell W. (2019). Weak breeding seasonality of a songbird in a seasonally arid tropical environment arises from individual flexibility and strongly seasonal moult. DOI

Ormeño-Orrillo E., Martínez-Romero E. (2019). A genomotaxonomy view of the Bradyrhizobium genus. PubMed DOI PMC

Owen D. F., Owen J. (1974). Species diversity in temperate and tropical Ichneumonidae. DOI

Owen J. C., Moore F. R. (2008). Swainson’s thrushes in migratory disposition exhibit reduced immune function. DOI

Peach W. J., Hanmer D. B., Oatley T. B. (2001). Do southern African songbirds live longer than their European counterparts? DOI

Peng R. D. (2019).

Pérez-Cobas A. E., Gosalbes M. J., Friedrichs A., Knecht H., Artacho A., Eismann K., et al. (2013). Gut microbiota disturbance during antibiotic therapy: A multi-omic approach. PubMed DOI PMC

Piersma T., Gudmundsson G. A., Lilliendahl K. (1999). Rapid changes in the size of different functional organ and muscle groups during refueling in a long-distance migrating shorebird. PubMed DOI

Price M. N., Dehal P. S., Arkin A. P. (2009). FastTree: Computing large minimum evolution trees with profiles instead of a distance matrix. PubMed DOI PMC

Qin J., Li R., Raes J., Arumugam M., Burgdorf K. S., Manichanh C., et al. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. PubMed DOI PMC

Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., et al. (2013). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. PubMed DOI PMC

R Core Team (2020).

Reikvam D. H., Erofeev A., Sandvik A., Grcic V., Jahnsen F. L., Gaustad P., et al. (2011). Depletion of murine intestinal microbiota: Effects on gut mucosa and epithelial gene expression. PubMed DOI PMC

Risely A., Waite D. W., Ujvari B., Hoye B. J., Klaassen M. (2018). Active migration is associated with specific and consistent changes to gut microbiota in PubMed DOI

Risely A., Waite D., Ujvari B., Klaassen M., Hoye B. (2017). Gut microbiota of a long-distance migrant demonstrates resistance against environmental microbe incursions. PubMed DOI

Rockwell S. M., Bocetti C. I., Marra P. P. (2012). Carry-over effects of winter climate on spring arrival date and reproductive success in an endangered migratory bird. Kirtland’s Warbler (Setophaga kirtlandii. DOI

Rognes T., Flouri T., Nichols B., Quince C., Mahé F. (2016). VSEARCH: A versatile open source tool for metagenomics. PubMed DOI PMC

Saino N., Szép T., Ambrosini R., Romano M., Møller A. P. (2004). Ecological conditions during winter affect sexual selection and breeding in a migratory bird. PubMed DOI PMC

Schemske D. W., Mittelbach G. G., Cornell H. V., Sobel J. M., Roy K. (2009). Is there a latitudinal gradient in the importance of biotic interactions? DOI

Schliep K. P. (2011). phangorn: Phylogenetic analysis in R. PubMed DOI PMC

Schwilch R., Grattarola A., Spina F., Jenni L. (2002). Protein loss during long-distance migratory flight in passerine birds: Adaptation and constraint. PubMed DOI

Sender R., Fuchs S., Milo R. (2016). Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. PubMed DOI

Serle W. (1981). The breeding season of birds in the lowland rainforest and in the montane forest of West Cameroon. DOI

Sommer F., Bäckhed F. (2013). The gut microbiota-masters of host development and physiology. PubMed DOI

Stutchbury B. J. M., Morton E. S. (2001).

Suzuki T. A., Worobey M. (2014). Geographical variation of human gut microbial composition. PubMed DOI PMC

Suzuki T. A., Martins F. M., Phifer-Rixey M., Nachman M. W. (2020). The gut microbiota and Bergmann’s rule in wild house mice. PubMed DOI PMC

Turjeman S., Corl A., Wolfenden A., Tsalyuk M., Lublin A., Choi O., et al. (2020). Migration, pathogens and the avian microbiome: A comparative study in sympatric migrants and residents. PubMed DOI

Tye H. (1992). Reversal of breeding season by lowland birds at higher altitudes in western Cameroon. DOI

van Dongen W. F., White J., Brandl H. B., Moodley Y., Merkling T., Leclaire S., et al. (2013). Age-related differences in the cloacal microbiota of a wild bird species. PubMed DOI PMC

Videvall E., Strandh M., Engelbrecht A., Cloete S., Cornwallis C. K. (2018). Measuring the gut microbiome in birds: Comparison of faecal and cloacal sampling. PubMed DOI

Wang Q., Garrity G. M., Tiedje J. M., Cole J. R. (2007). Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. PubMed DOI PMC

Wiersma P., Chappell M. A., Williams J. B. (2007a). Cold- and exercise-induced peak metabolic rates in tropical birds. PubMed DOI PMC

Wiersma P., Muñoz-Garcia A., Walker A., Williams J. B. (2007b). Tropical birds have a slow pace of life. PubMed DOI PMC

Wilman H., Belmaker J., Simpson J., de la Rosa C., Rivadeneira M. M., Jetz W. (2014). EltonTraits 1.0: Species-level foraging attributes of the world’s birds and mammals. DOI

Wright E. S. (2020). RNAconTest: Comparing tools for noncoding RNA multiple sequence alignment based on structural consistency. PubMed DOI PMC

Wu H.-J., Wu E. (2012). The role of gut microbiota in immune homeostasis and autoimmunity. PubMed DOI PMC

Wu Y., Yang Y., Cao L., Yin H., Xu M., Wang Z., et al. (2018). Habitat environments impacted the gut microbiome of long-distance migratory swan geese but central species conserved. PubMed DOI PMC

Yatsunenko T., Rey F. E., Manary M. J., Trehan I., Dominguez-Bello M. G., Contreras M., et al. (2012). Human gut microbiome viewed across age and geography. PubMed DOI PMC

Youngblut N. D., Reischer G. H., Walters W., Schuster N., Walzer C., Stalder G., et al. (2019). Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. PubMed DOI PMC

Zhang F., Xiang X., Dong Y., Yan S., Song Y., Zhou L. (2020). Significant differences in the gut bacterial communities of Hooded Crane ( PubMed DOI PMC

Host Diet Preference Drives Diversity and Composition of Gut Microbiota in Captive Birds