Effect of population size and selection on Toll-like receptor diversity in populations of Galápagos mockingbirds

. 2023 Jan ; 36 (1) : 109-120. [epub] 20221118

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid36398499

The interactions of evolutionary forces are difficult to analyse in free-living populations. However, when properly understood, they provide valuable insights into evolutionary biology and conservation genetics. This is particularly important for the interplay of genetic drift and natural selection in immune genes that confer resistance to disease. The Galápagos Islands are inhabited by four closely related species of mockingbirds (Mimus spp.). We used 12 different-sized populations of Galápagos mockingbirds and one population of their continental relative northern mockingbird (Mimus polyglottos) to study the effects of genetic drift on the molecular evolution of immune genes, the Toll-like receptors (TLRs: TLR1B, TLR4 and TLR15). We found that neutral genetic diversity was positively correlated with island size, indicating an important effect of genetic drift. However, for TLR1B and TLR4, there was little correlation between functional (e.g., protein) diversity and island size, and protein structural properties were largely conserved, indicating only a limited effect of genetic drift on molecular phenotype. By contrast, TLR15 was less conserved and even its putative functional polymorphism correlated with island size. The patterns observed for the three genes suggest that genetic drift does not necessarily dominate selection even in relatively small populations, but that the final outcome depends on the degree of selection constraint that is specific for each TLR locus.

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Alcaide, M., & Edwards, S. V. (2011). Molecular evolution of the Toll-like receptor multigene family in birds. Molecular Biology and Evolution, 28, 1703-1715.

Arbogast, B. S., Drovetski, S. V., & Curry, R. L. (2006). The origin and diversification of Galápagos mockingbirds. Evolution, 60, 370-382.

Areal, H., Abrantes, J., & Esteves, P. J. (2011). Signatures of positive selection in Toll-like receptor (TLR) genes in mammals. BMC Evolutionary Biology, 11, 368.

Azad, A. K., Sadee, W., & Schlesinger, L. S. (2012). Innate immune gene polymorphisms in tuberculosis. Infection and Immunity, 80, 3343-3359.

Bates, D., Maechler, M., Bolker, B., Walker, S., Christensen, R. H. B., Singmann, H., Dai, B., Grothendieck, G., & Green, P. (2015). Fitting linear mixed-effects models using {lme4}. Journal of Statistical Software, 67, 1-48.

Bateson, Z. W., Hammerly, S. C., Johnson, J. A., Morrow, M. E., Whittingham, L. A., & Dunn, P. O. (2016). Specific alleles at immune genes, rather than genome-wide heterozygosity, are related to immunity and survival in the critically endangered Attwater's prairie-chicken. Molecular Ecology, 25, 4730-4744.

Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114-2120.

Clark, N. J., & Clegg, S. M. (2017). Integrating phylogenetic and ecological distances reveals new insights into parasite host specificity. Molecular Ecology, 26(11), 3074-3086. Portico. https://doi.org/10.1111/mec.14101

Charlesworth, B. (2009). Effective population size and patterns of molecular evolution and variation. Nature Reviews Genetics, 10, 195-205.

Darfour-Oduro, K. A., Megens, H.-J., Roca, A. L., Groenen, M. A. M., & Schook, L. B. (2015). Adaptive evolution of Toll-like receptors (TLRs) in the family Suidae. PLoS One, 10, e0124069.

Davies, C. S., Taylor, M. I., Hammers, M., Burke, T., Komdeur, J., Dugdale, H. L., & Richardson, D. S. (2021). Contemporary evolution of the innate immune receptor gene TLR3 in an isolated vertebrate population. Molecular Ecology, 30, 2528-2542.

de Zoete, M. R., Bouwman, L. I., Keestra, A. M., & van Putten, J. P. M. (2011). Cleavage and activation of a Toll-like receptor by microbial proteases. Proceedings of the National Academy of Sciences, 108, 4968-4973.

DeCandia, A. L., Dobson, A. P., & VonHoldt, B. M. (2018). Toward an integrative molecular approach to wildlife disease. Conservation Biology, 32, 798-807.

Deem, S. L., Parker, P. G., Cruz, M. B., Merkel, J., & Hoeck, P. E. A. (2011). Comparison of blood values and health status of Floreana mockingbirds (Mimus trifasciatus) on the islands of champion and Gardner-by-Floreana, Galápagos Islands. Journal of Wildlife Diseases, 47, 94-106.

Egea, R., Casillas, S., & Barbadilla, A. (2008). Standard and generalized McDonald-Kreitman test: A website to detect selection by comparing different classes of DNA sites. Nucleic Acids Research, 36, 157-162.

Eichler, W. (1948). Annals and Magazine of Natural History. Annals and Magazine of Natural History, 1, 588-598.

Ferwerda, B., McCall, M. B. B., Alonso, S., Giamarellos-Bourboulis, E. J., Mouktaroudi, M., Izagirre, N., Syafruddin, D., Kibiki, G., Cristea, T., Hijmans, A., Hamann, L., Israel, S., ElGhazali, G., Troye-Blomberg, M., Kumpf, O., Maiga, B., Dolo, A., Doumbo, O., Hermsen, C. C., … Netea, M. G. (2007). TLR4 polymorphisms, infectious diseases, and evolutionary pressure during migration of modern humans. Proceedings of the National Academy of Sciences, 104(42), 16645-16650. https://doi.org/10.1073/pnas.0704828104

Fiddaman, S. R., Vinkler, M., Spiro, S. G., Levy, H., Emerling, C. A., Boyd, A. C., Dimopoulos, E. A., Vianna, J. A., Cole, T. L., Pan, H., Fang, M., Zhang, G., Hart, T., Frantz, L. A. F., & Smith, A. L. (2022). Adaptation and cryptic pseudogenization in penguin Toll-like receptors. Molecular Biology and Evolution, 39, msab354.

Frankham, R. (2005). Genetics and extinction. Biological Conservation, 126, 131-140.

Galtier, N. (2016). Adaptive protein evolution in animals and the effective population size hypothesis. PLoS Genetics, 12, 1-23.

Gavan, M. K., Oliver, M. K., Douglas, A., & Piertney, S. B. (2015). Gene dynamics of Toll-like receptor 4 through a population bottleneck in an insular population of water voles (Arvicola amphibius). Conservation Genetics, 16, 1181-1193.

Gilroy, D. L., van Oosterhout, C., Komdeur, J., & Richardson, D. S. (2017). Toll-like receptor variation in the bottlenecked population of the endangered Seychelles warbler. Animal Conservation, 20, 235-250.

Gonzalez-Quevedo, C., Spurgin, L. G., Illera, J. C., & Richardson, D. S. (2015). Drift, not selection, shapes Toll-like receptor variation among oceanic Island populations. Molecular Ecology, 24, 5852-5863.

Grantham, R. (1974). Amino acid difference formula to help explain protein evolution. Science, 185, 862-864.

Grueber, C. E., Wallis, G. P., & Jamieson, I. G. (2013). Genetic drift outweighs natural selection at Toll-like receptor (TLR) immunity loci in a re-introduced population of a threatened species. Molecular Ecology, 22, 4470-4482.

Grueber, C. E., Wallis, G. P., & Jamieson, I. G. (2014). Episodic positive selection in the evolution of avian Toll-like receptor innate immunity genes. PLoS One, 9, e89632.

Hartmann, S. A., Schaefer, H. M., & Segelbacher, G. (2014). Genetic depletion at adaptive but not neutral loci in an endangered bird species. Molecular Ecology, 23, 5712-5725.

Hoeck, P. E. A., Bollmer, J. L., Parker, P. G., & Keller, L. F. (2010). Differentiation with drift: A spatio-temporal genetic analysis of Galápagos mockingbird populations (Mimus spp.). Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 1127-1138.

Iwasaki, A., & Medzhitov, R. (2010). Regulation of adaptive immunity by the innate immune system. Science, 327, 291-295.

Jiménez-Uzcátegui, G., Llerena, W., Bryan Milstead, W., Lomas, E. E., & Wiedenfield, D. A. (2011). Is the population of Floreana mockingbird Mimus trifasciatus declining? Cotinga, 33, 34-40.

Jin, M. S., Kim, S. E., Heo, J. Y., Lee, M. E., Kim, H. M., Paik, S. G., Lee, H., & Lee, J. O. (2007). Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell, 130, 1071-1082.

Khan, I., Maldonado, E., Silva, L., Almeida, D., Johnson, W. E., O'Brien, S. J., Zhang, G., Jarvis, E. D., Gilbert, M. T. P., & Antunes, A. (2019). The vertebrate TLR supergene family evolved dynamically by gene gain/loss and positive selection revealing a host-pathogen arms race in birds. Diversity, 11, 131.

Kimura, M. (1983). The neutral theory of molecular evolution. Cambridge University Press.

Kloch, A., Wenzel, M. A., Laetsch, D. R., Michalski, O., Bajer, A., Behnke, J. M., Welc-Falęciak, R., & Piertney, S. B. (2018). Signatures of balancing selection in Toll-like receptor (TLRs) genes-novel insights from a free-living rodent. Scientific Reports, 8, 1-10.

Kosakovsky Pond, S. L., & Frost, S. D. W. (2005). Not so different after all: A comparison of methods for detecting amino acid sites under selection. Molecular Biology and Evolution, 22, 1208-1222.

Králová, T., Albrecht, T., Bryja, J., Hořák, D., Johnsen, A., Lifjeld, J. T., Novotný, M., Sedláček, O., Velová, H., & Vinkler, M. (2018). Signatures of diversifying selection and convergence acting on passerine Toll-like receptor 4 in an evolutionary context. Molecular Ecology, 27, 2871-2883.

Kryazhimskiy, S., & Plotkin, J. B. (2008). The population genetics of dN/dS. PLoS Genetics, 4, e1000304.

Kumar, H., Kawai, T., & Akira, S. (2011). Pathogen recognition by the innate immune system. International Reviews of Immunology, 30, 16-34.

Leigh, J. W., & Bryant, D. (2015). Popart: full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6(9), 1110-1116. Portico. https://doi.org/10.1111/2041-210x.12410

Leveque, G., Forgetta, V., Morroll, S., Smith, A. L., Bumstead, N., Barrow, P., Loredo-Osti, J. C., Morgan, K., & Malo, D. (2003). Allelic variation in TLR4 is linked to susceptibility to salmonella enterica serovar typhimurium infection in chickens. Infection and Immunity, 71, 1116-1124.

Levy, H., Fiddaman, S. R., Vianna, J. A., Noll, D., Clucas, G. V., Sidhu, J. K. H., Polito, M. J., Bost, C. A., Phillips, R. A., Crofts, S., Miller, G. D., Pistorius, P., Bonnadonna, F., le Bohec, C., Barbosa, A., Trathan, P., Raya Rey, A., Frantz, L. A. F., Hart, T., & Smith, A. L. (2020). Evidence of pathogen-induced immunogenetic selection across the large geographic range of a wild seabird. Molecular Biology and Evolution, 37, 1708-1726.

Li, Y., Oosting, M., Smeekens, S. P., Jaeger, M., Aguirre-Gamboa, R., Le, K. T. T., Deelen, P., Ricaño-Ponce, I., Schoffelen, T., Jansen, A. F., & Swertz, M. A. (2016). A functional genomics approach to understand variation in cytokine production in humans. Cell, 167, 1099-1110.e14.

Lovette, I. J., Arbogast, B. S., Curry, R. L., Zink, R. M., Botero, C. A., Sullivan, J. P., Talaba, A. L., Harris, R. B., Rubenstein, D. R., Ricklefs, R. E., & Bermingham, E. (2012). Phylogenetic relationships of the mockingbirds and thrashers (Aves: Mimidae). Molecular Phylogenetics and Evolution, 63, 219-229.

Lynch, M. (2007). The origins of genome architecture. Sinauer Associates.

Miller, H. C., & Lambert, D. M. (2004). Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Molecular Ecology, 13, 3709-3721.

Minias, P., & Vinkler, M. (2022). Selection balancing at innate immune genes: Adaptive polymorphism maintenance in Toll-like receptors. Molecular Biology and Evolution, 39, msac102.

Mugal, C. F., Wolf, J. B. W., & Kaj, I. (2014). Why time matters: Codon evolution and the temporal dynamics of dN/dS. Molecular Biology and Evolution, 31, 212-231.

Mukherjee, S., Sarkar-Roy, N., Wagener, D. K., & Majumder, P. P. (2009). Signatures of natural selection are not uniform across genes of innate immune system, but purifying selection is the dominant signature. Proceedings of the National Academy of Sciences of the United States of America, 106, 7073-7078.

Murrell, B., Moola, S., Mabona, A., Weighill, T., Sheward, D., Kosakovsky Pond, S. L., & Scheffler, K. (2013). FUBAR: A fast, unconstrained Bayesian approximation for inferring selection. Molecular Biology and Evolution, 30, 1196-1205.

Nagai, Y., Akashi, S., Nagafuku, M., Ogata, M., Iwakura, Y., Akira, S., Kitamura, T., Kosugi, A., Kimoto, M., & Miyake, K. (2002). Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nature Immunology, 3, 667-672.

Nelson-Flower, M. J., Germain, R. R., MacDougall-Shackleton, E. A., Taylor, S. S., & Arcese, P. (2018). Purifying selection in the Toll-like receptors of song sparrows Melospiza melodia. Journal of Heredity, 109, 501-509.

Ohta, T. (1992). The nearly neutral theory of molecular evolution. Annual Review of Ecology and Systematics, 23, 263-286.

Park, B. S., Song, D. H., Kim, H. M., Choi, B.-S., Lee, H., & Lee, J.-O. (2009). The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature, 458, 1191-1195.

Quéméré, E., Galan, M., Cosson, J.-F., Klein, F., Aulagnier, S., Gilot-Fromont, E., Merlet, J., Bonhomme, M., Hewison, A. J. M., & Charbonnel, N. (2015). Immunogenetic heterogeneity in a widespread ungulate: The European roe deer (Capreolu s capreolus). Molecular Ecology, 24, 3873-3887.

Quéméré, E., Hessenauer, P., Galan, M., Fernandez, M., Merlet, J., Chaval, Y., Morellet, N., Verheyden, H., Gilot-Fromont, E., Charbonnel, N., & Charbonnel, N. (2021). Pathogen-mediated selection favours the maintenance of innate immunity gene polymorphism in a widespread wild ungulate. Journal of Evolutionary Biology, 34, 1156-1166.

R Core Team. (2016). R: A language and environment for statistical computing. R Foundation for Statistical Computing.

Raven, N., Lisovski, S., Klaassen, M., Lo, N., Madsen, T., Ho, S. Y. W., & Ujvari, B. (2017). Purifying selection and concerted evolution of RNA-sensing Toll-like receptors in migratory waders. Infection, Genetics and Evolution, 53, 135-145.

Richter, S., Wenzel, A., Stein, M., Gabdoulline, R. R., & Wade, R. C. (2008). webPIPSA: A web server for the comparison of protein interaction properties. Nucleic Acids Research, 36, 276-280.

Robinson, J. A., Brown, C., Kim, B. Y., Lohmueller, K. E., & Wayne, R. K. (2018). Purging of strongly deleterious mutations explains long-term persistence and absence of inbreeding depression in Island foxes. Current Biology, 28, 3487-3494.e4.

Rousett, F. (2008). genepop'007: A complete re-implementation of the genepop software for windows and Linux. Molecular Ecology Resources, 8, 103-106.

Ruan, W. K., Wu, Y. H., An, J., & Zheng, S. J. (2012). Polymorphisms of chicken Toll-like receptors 4, 15, and 21 in different breeds. Poultry Science, 91, 2512-2516.

Rudd, M. F., Williams, R. D., Webb, E. L., Schmidt, S., Sellick, G. S., & Houlston, R. S. (2005). The predicted impact of coding single nucleotide polymorphisms database. Cancer Epidemiology Biomarkers and Prevention, 14, 2598-2604.

Snell, H. M., Stone, P. A., & Snell, H. L. (1996). A summary of geographical characteristics of the Galápagos Islands. Journal of Biogeography, 23, 619-624.

Spielman, D., Brook, B. W., & Frankham, R. (2004). Most species are not driven to extinction before genetic factors impact them. Proceedings of the National Academy of Sciences of the United States of America, 101, 15261-15264.

Stephens, M., Smith, N. J., & Donnelly, P. (2001). A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics, 68, 978-989.

Sukumaran, J., & Holder, M. T. (2010). DendroPy: A python library for phylogenetic computing. Bioinformatics, 26, 1569-1571.

Suzuki, R., & Shimodaira, H. (2006). Pvclust: An R package for assessing the uncertainty in hierarchical clustering. Bioinformatics, 22, 1540-1542.

Tschirren, B. (2015). Borrelia burgdorferi sensu lato infection pressure shapes innate immune gene evolution in natural rodent populations across Europe. Biology Letters, 11, 20150263.

Tschirren, B., Andersson, M., Scherman, K., Westerdahl, H., & Råberg, L. (2012). Contrasting patterns of diversity and population differentiation at the innate immunity gene Toll-like receptor 2 (tlr2) in two sympatric rodent species. Evolution, 66, 720-731.

Velová, H., Gutowska-Ding, M. W., Burt, D. W., & Vinkler, M. (2018). Toll-like receptor evolution in birds: Gene duplication, pseudogenization, and diversifying selection. Molecular Biology and Evolution, 35, 2170-2184.

Vinkler, M., Bainová, H., & Bryja, J. (2014). Protein evolution of Toll-like receptors 4, 5 and 7 within Galloanserae birds. Genetics Selection Evolution, 46, 72.

Vinkler, M., Bainová, H., Bryjová, A., Tomášek, O., Albrecht, T., & Bryja, J. (2015). Characterisation of Toll-like receptors 4, 5 and 7 and their genetic variation in the grey partridge. Genetica, 143, 101-112.

Vlček, J. (2022). Vlkofly/TLR-amplicon: Scripts for a publication on Toll-like receptors in Galápagos mockingbirds. Zenodo. Vienna, Austria: R Foundation for Statistical Computing. https://doi.org/10.5281/zenodo.7248527

Vlček, J., Hoeck, P. E. A., Keller, L. F., Wayhart, J., Dolinová, I., & Štefka, J. (2016). Balancing selection and genetic drift create unusual patterns of MHCIIβ variation in Galápagos mockingbirds. Molecular Ecology, 25, 4757-4772.

Vlček, J., Miláček, M., Vinkler, M., & Štefka, J. (2020). Supplementary tables for: Effect of population size and selection on cirds. Figshare. https://doi.org/10.6084/m9.figshare.12180027.v4

Walsh, C., Gangloff, M., Monie, T., Smyth, T., Wei, B., McKinley, T. J., Maskell, D., Gay, N., & Bryant, C. (2008). Elucidation of the MD-2/TLR4 Interface required for signaling by lipid IVa. The Journal of Immunology, 181, 1245-1254.

Wang, J., Zhang, Z., Liu, J., Zhao, J., & Yin, D. (2016). Ectodomain architecture affects sequence and functional evolution of vertebrate Toll-like receptors. Scientific Reports, 6, 1-10.

Wertheim, J. O., Murrell, B., Smith, M. D., Pond, S. L. K., & Scheffler, K. (2015). RELAX: Detecting relaxed selection in a phylogenetic framework. Molecular Biology and Evolution, 32, 820-832.

Wickham, H. (2009). ggplot2: Elegant graphics for data analysis. Springer.

Wikelski, M., Foufopoulos, J., Vargas, H., & Snell, H. (2004). Galápagos birds and diseases: Invasive pathogens as threats for Island species. Ecology and Society, 9, 5.

Willi, Y., Van Buskirk, J., & Hoffmann, A. A. (2006). Limits to the adaptive potential of small populations. Annual Review of Ecology, Evolution, and Systematics, 37, 433-458.

Wlasiuk, G., Khan, S., Switzer, W. M., & Nachman, M. W. (2009). A history of recurrent positive selection at the Toll-like receptor 5 in primates. Molecular Biology and Evolution, 26, 937-949.

Yang, J., & Zhang, Y. (2015). I-TASSER server: New development for protein structure and function predictions. Nucleic Acids Research, 43, W174-W181.

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