Animal microbiomes play an important role in dietary adaptation, yet the extent to which microbiome changes exhibit parallel evolution is unclear. Of particular interest is an adaptation to extreme diets, such as blood, which poses special challenges in its content of proteins and lack of essential nutrients. In this study, we assessed taxonomic signatures (by 16S rRNA amplicon profiling) and potential functional signatures (inferred by Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt)) of haematophagy in birds and bats. Our goal was to test three alternative hypotheses: no convergence of microbiomes, convergence in taxonomy and convergence in function. We find a statistically significant effect of haematophagy in terms of microbial taxonomic convergence across the blood-feeding bats and birds, although this effect is small compared to the differences found between haematophagous and non-haematophagous species within the two host clades. We also find some evidence of convergence at the predicted functional level, although it is possible that the lack of metagenomic data and the poor representation of microbial lineages adapted to haematophagy in genome databases limit the power of this approach. The results provide a paradigm for exploring convergent microbiome evolution replicated with independent contrasts in different host lineages. This article is part of the theme issue 'Convergent evolution in the genomics era: new insights and directions'.

Biology Centre of ASCR Institute of Parasitology České Budějovice Czech Republic

Center for Microbiome Research University of California San Diego San Diego CA 92093 USA

Colegio de Ciencias Biológicas y Ambientales Universidad San Francisco de Quito Quito Ecuador

Cornell Institute for Host Microbe Interactions and Disease Cornell University Ithaca NY 14853 USA

Department of Animal Sciences Colorado State University Fort Collins CO 80523 USA

Department of Biology University of Miami Coral Gables FL 33146 USA

Department of Computer Science and Engineering University of California San Diego San Diego CA 92093 USA

Department of Ecology and Evolutionary Biology University of Colorado Boulder Boulder CO 80309 USA

Department of Pediatrics University of California San Diego La Jolla CA 92093 USA

Department of Population Health and Reproduction School of Veterinary Medicine University of California Davis Davis CA 95616 USA

Faculty of Science University of South Bohemia České Budějovice Czech Republic

Galápagos Science Center Puerto Baquerizo Moreno Galápagos Ecuador

National Wildlife Research Center U S Department of Agriculture Fort Collins CO 80521 USA

Unidad de Investigación Médica en Inmunología Coordinación de Investigación Instituto Mexicano del Seguro Social Centro Médico Nacional Siglo XXI Hospital de Pediatría 3er piso Mexico City Mexico

United States Geological Survey Great Lakes Science Center Hammond Bay Biological Station Millersburg MI 49759 USA

See more in PubMed

Ley RE, et al. 2008. Evolution of mammals and their gut microbes. Science 320, 1647–1651. (10.1126/science.1155725) PubMed DOI PMC

Muegge BD, Kuczynski J, Knights D, Clemente JC, González A, Fontana L, Henrissat B, Knight R, Gordon JI. 2011. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332, 970–974. (10.1126/science.1198719) PubMed DOI PMC

McFall-Ngai M, et al. 2013. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl Acad. Sci. USA 110, 3229–3236. (10.1073/pnas.1218525110) PubMed DOI PMC

Kohl KD, Weiss RB, Cox J, Dale C, Dearing MD. 2014. Gut microbes of mammalian herbivores facilitate intake of plant toxins. Ecol. Lett. 17, 1238–1246. (10.1111/ele.12329) PubMed DOI

Zhu L, Wu Q, Dai J, Zhang S, Wei F. 2011. Evidence of cellulose metabolism by the giant panda gut microbiome. Proc. Natl Acad. Sci. USA 108, 17 714–17 719. (10.1073/pnas.1017956108) PubMed DOI PMC

Brune A. 2014. Symbiotic digestion of lignocellulose in termite guts. Nat. Rev. Microbiol. 12, 168–180. (10.1038/nrmicro3182) PubMed DOI

McGhee GR. 2011. Convergent evolution: limited forms most beautiful. Cambridge, MA: MIT Press.

Delsuc F, Metcalf JL, Wegener Parfrey L, Song SJ, González A, Knight R. 2014. Convergence of gut microbiomes in myrmecophagous mammals. Mol. Ecol. 23, 1301–1317. (10.1111/mec.12501) PubMed DOI

Rio RVM, Attardo GM, Weiss BL. 2016. Grandeur alliances: symbiont metabolic integration and obligate arthropod haematophagy. Trends Parasitol. 32, 739–749. (10.1016/j.pt.2016.05.002) PubMed DOI PMC

Manzano-Marín A, Oceguera-Figueroa A, Latorre A, Jiménez-García LF, Moya A. 2015. Solving a bloody mess: B-vitamin independent metabolic convergence among gammaproteobacterial obligate endosymbionts from blood-feeding arthropods and the leech Haementeria officinalis. Genome Biol. Evol. 7, 2871–2884. (10.1093/gbe/evv188) PubMed DOI PMC

Baker RJ, Bininda-Emonds ORP, Mantilla-Meluk H, Porter CA, Van Den Bussche RA.. 2012. Molecular time scale of diversification of feeding strategy and morphology in New World Leaf-Nosed Bats (Phyllostomidae): a phylogenetic perspective. In Evolutionary history of bats: fossils, molecules and morphology, Cambridge studies in morphology and molecules: new paradigms in evolutionary biology series, number 2 (eds G Gunnell, N Simmons), pp. 385–409. Cambridge, UK: Cambridge University Press (10.1017/CBO9781139045599.012) DOI

Schmidt U, Greenhall A.. 1988. Natural history of vampire bats. Boca Raton, FL: CRC Press (10.1201/9781351074919) DOI

Koster F, Koster H. 1983. Twelve days among the ‘vampire finches’ of Wolf Island. Noticias de Galápagos 38, 4–10.

Bowman RI, Billeb SL. 1965. Blood-eating in a Galapagos finch. Living Bird 4, 29–44.

Schluter D, Grant PR. 1984. Ecological correlates of morphological evolution in a Darwin's finch, Geospiza difficilis. Evolution 38, 856–869. (10.1111/j.1558-5646.1984.tb00357.x) PubMed DOI

Schluter D, Grant PR. 1982. The distribution of Geospiza difficilis in relation to G. fuliginosa in the Galápagos Islands: tests of three hypotheses. Evolution 36, 1213–1226. (10.1111/j.1558-5646.1982.tb05490.x) PubMed DOI

Lamichhaney S, et al. 2015. Evolution of Darwin's finches and their beaks revealed by genome sequencing. Nature 518, 371–375. (10.1038/nature14181) PubMed DOI

Stuckey MJ, Chomel BB, Galvez-Romero G, Olave-Leyva JI, Obregón-Morales C, Moreno-Sandoval H, Aréchiga-Ceballos N, Salas-Rojas M, Aguilar-Setién A. 2017. Bartonella infection in haematophagous, insectivorous, and phytophagous bat populations of Central Mexico and the Yucatan Peninsula. Am. J. Trop. Med. Hyg. 97, 413–422. (10.4269/ajtmh.16-0680) PubMed DOI PMC

Knutie SA, Gotanda KM. 2018. A non-invasive method to collect fecal samples from wild birds for microbiome studies. Microb. Ecol. 76, 851–855. (10.1007/s00248-018-1182-4) PubMed DOI

Song SJ, Amir A, Metcalf JL, Amato KR, Xu ZZ, Humphrey G, Knight R. 2016. Preservation methods differ in fecal microbiome stability, affecting suitability for field studies. mSystems 1, e00021-16 (10.1128/mSystems.00021-16) PubMed DOI PMC

Vogtmann E, Chen J, Amir A, Shi J, Abnet CC, Nelson H, Knight R, Chia N, Sinha R. 2017. Comparison of collection methods for fecal samples in microbiome studies. Am. J. Epidemiol. 185, 115–123. (10.1093/aje/kww177) PubMed DOI PMC

Thompson LR, et al. 2017. A communal catalogue reveals Earth's multiscale microbial diversity Nature 551, 457–463. (10.1038/nature24621) PubMed DOI PMC

Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R. 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl Acad. Sci. USA 108, 4516–4522. (10.1073/pnas.1000080107) PubMed DOI PMC

Caporaso JG, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336. (10.1038/nmeth.f.303) PubMed DOI PMC

Amir A, et al. 2017. Deblur rapidly resolves single-nucleotide community sequence patterns. mSystems 2, e00191-16 (10.1128/mSystems.00191-16) PubMed DOI PMC

Pedregosa F, et al. 2011. Scikit-learn: machine learning in python. J. Mach. Learn. Res. 12, 2825–2830.

Janssen S, et al. 2018. Phylogenetic placement of exact amplicon sequences improves associations with clinical information. mSystems 3, e00021-18 (10.1128/mSystems.00021-18) PubMed DOI PMC

Mirarab S, Nguyen N, Warnow T. 2012. SEPP: SATé-enabled phylogenetic placement. Pac. Symp. Biocomput. 2012, 247–258. (10.1142/9789814366496_0024) PubMed DOI

Lozupone C, Knight R. 2005. UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228–8235. (10.1128/AEM.71.12.8228-8235.2005) PubMed DOI PMC

Vázquez-Baeza Y, Pirrung M, Gonzalez A, Knight R. 2013. EMPeror: a tool for visualizing high-throughput microbial community data. Gigascience 2, 16 (10.1186/2047-217x-2-16) PubMed DOI PMC

Oksanen J, et al. 2013. vegan: Community Ecology Package. R package version 2. See https://CRAN.Rproject.org/package=vegan.

Langille MGI, et al. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31, 814–821. (10.1038/nbt.2676) PubMed DOI PMC

Kanehisa M, et al. 2008. KEGG for linking genomes to life and the environment. Nucleic Acids Res. 36, D480–D484. (10.1093/nar/gkm882) PubMed DOI PMC

Mandal S, Van Treuren W, White RA, Eggesbø M, Knight R, Peddada SD.. 2015. Analysis of composition of microbiomes: a novel method for studying microbial composition. Microb. Ecol. Health Dis. 26, 27663 (10.3402/mehd.v26.27663) PubMed DOI PMC

Wickham H. 2016. Ggplot2: elegant graphics for data analysis. Berlin, Germany: Springer.

Ingala MR, Simmons NB, Wultsch C, Krampis K, Speer KA, Perkins SL. 2018. Comparing microbiome sampling methods in a wild mammal: fecal and intestinal samples record different signals of host ecology, evolution. Front. Microbiol. 9, 803 (10.3389/fmicb.2018.00803) PubMed DOI PMC

On SLW, Miller WG, Houf K, Fox JG, Vandamme P. 2017. Minimal standards for describing new species belonging to the families Campylobacteraceae and Helicobacteraceae: Campylobacter, Arcobacter, Helicobacter and Wolinella spp. Int. J. Syst. Evol. Microbiol. 67, 5296–5311. (10.1099/ijsem.0.002255) PubMed DOI PMC

McFarland WN, Wimsatt WA. 1969. Renal function and its relation to the ecology of the vampire bat, Desmodus rotundus. Comp. Biochem. Physiol. 28, 985–1006. (10.1016/0010-406X(69)90543-X) DOI

Michel AJ, et al. 2018. The gut of the finch: uniqueness of the gut microbiome of the Galápagos vampire finch. Microbiome 6, 167 (10.1186/s40168-018-0555-8) PubMed DOI PMC

Romine MF, et al. 2017. Elucidation of roles for vitamin B12 in regulation of folate, ubiquinone, and methionine metabolism. Proc. Natl Acad. Sci. USA 114, E1205–E1214. (10.1073/pnas.1612360114) PubMed DOI PMC

Sugita H, Takahashi J, Miyajima C, Deguchi Y. 1991. Vitamin B12-producing ability of the intestinal microflora of rainbow trout (Oncorhynchus mykiss). Agric. Biol. Chem. 55, 893–894. (10.1080/00021369.1991.10870683) DOI

Tsuchiya C, Sakata T, Sugita H. 2008. Novel ecological niche of Cetobacterium somerae, an anaerobic bacterium in the intestinal tracts of freshwater fish. Lett. Appl. Microbiol. 46, 43–48. (10.1111/j.1472-765x.2007.02258.x) PubMed DOI

Hughes MR. 2003. Regulation of salt gland, gut and kidney interactions. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 136, 507–524. (10.1016/j.cbpb.2003.09.005) PubMed DOI

Zepeda Mendoza ML, et al. 2018. Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat. Nat. Ecol. Evol. 2, 659–668. (10.1038/s41559-018-0476-8) PubMed DOI PMC

Amato KR, et al. 2018. Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. ISME J. 13, 576–587. (10.1038/s41396-018-0175-0) PubMed DOI PMC

Microbiomes of Blood-Feeding Triatomines in the Context of Their Predatory Relatives and the Environment

Ontogeny, species identity, and environment dominate microbiome dynamics in wild populations of kissing bugs (Triatominae)

See more in PubMed

figshare
10.6084/m9.figshare.c.4467776