Genotype-environment associations reveal genes potentially linked to avian malaria infection in populations of an endemic island bird.
adaptation
avian malaria
birds
genotype–environment association
immune defence
pathogen‐mediated selection
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
27 Mar 2024
27 Mar 2024
Historique:
revised:
29
01
2024
received:
07
03
2023
accepted:
01
03
2024
medline:
27
3
2024
pubmed:
27
3
2024
entrez:
27
3
2024
Statut:
aheadofprint
Résumé
Patterns of pathogen prevalence are, at least partially, the result of coevolutionary host-pathogen interactions. Thus, exploring the distribution of host genetic variation in relation to infection by a pathogen within and across populations can provide important insights into mechanisms of host defence and adaptation. Here, we use a landscape genomics approach (Bayenv) in conjunction with genome-wide data (ddRADseq) to test for associations between avian malaria (Plasmodium) prevalence and host genetic variation across 13 populations of the island endemic Berthelot's pipit (Anthus berthelotii). Considerable and consistent spatial heterogeneity in malaria prevalence was observed among populations over a period of 15 years. The prevalence of malaria infection was also strongly positively correlated with pox (Avipoxvirus) prevalence. Multiple host loci showed significant associations with malaria prevalence after controlling for genome-wide neutral genetic structure. These sites were located near to or within genes linked to metabolism, stress response, transcriptional regulation, complement activity and the inflammatory response, many previously implicated in vertebrate responses to malarial infection. Our findings identify diverse genes - not just limited to the immune system - that may be involved in host protection against malaria and suggest that spatially variable pathogen pressure may be an important evolutionary driver of genetic divergence among wild animal populations, such as Berthelot's pipit. Furthermore, our data indicate that spatio-temporal variation in multiple different pathogens (e.g. malaria and pox in this case) may have to be studied together to develop a more holistic understanding of host pathogen-mediated evolution.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e17329Subventions
Organisme : Natural Environment Research Council
ID : NE/L002582/1
Organisme : Natural Environment Research Council
ID : NE/S007334/1
Organisme : Regional Government of Asturias
ID : AYUD/2021/51261
Organisme : European Regional Development Fund
ID : PGC2018-097575-B-I00
Informations de copyright
© 2024 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.
Références
Aguilar, A., Roemer, G., Debenham, S., Binns, M., Garcelon, D., & Wayne, R. K. (2004). High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proceedings of the National Academy of Sciences of the United States of America, 101, 3490–3494.
Akey, B. L., Nayar, J. K., & Forrester, D. J. (1981). Avian pox in Florida wild Turkeys: Culex nigripalpus and Wyeomyia vanduzeei as experimental vectors. Journal of Wildlife Diseases, 17, 597–599.
Alley, M. R., Ha, H. J., Howe, L., Hale, K. A., & Cash, W. (2010). Concurrent avian malaria and avipox virus infection in translocated South Island saddlebacks (Philesturnus carunculatus carunculatus). New Zealand Veterinary Journal, 58, 218–223.
Anderson, R. M., & May, R. M. (1979). Population biology of infectious diseases: Part I. Nature, 280, 361–367.
Andrade, B. B., Reis‐Filho, A., Souza‐Neto, S. M., Raffaele‐Netto, I., Camargo, L. M. A., Barral, A., & Barral‐Netto, M. (2010). Plasma superoxide dismutase‐1 as a surrogate marker of vivax malaria severity. PLoS Neglected Tropical Diseases, 4, e650.
Armstrong, C., Davies, R. G., González‐Quevedo, C., Dunne, M., Spurgin, L. G., & Richardson, D. S. (2019). Adaptive landscape genetics and malaria across divergent Island bird populations. Ecology and Evolution, 9, 12482–12502.
Armstrong, C., Richardson, D. S., Hipperson, H., Horsburgh, G. J., Küpper, C., Percival‐Alwyn, L., Clark, M., Burke, T., & Spurgin, L. G. (2018). Genomic associations with bill length and disease reveal drift and selection across Island bird populations. Evolution Letters, 2, 22–36.
Asghar, M., Hasselquist, D., & Bensch, S. (2011). Are chronic avian haemosporidian infections costly in wild birds? Journal of Avian Biology, 42, 530–537.
Asghar, M., Hasselquist, D., Hansson, B., Zehtindjiev, P., Westerdahl, H., & Bensch, S. (2015). Hidden costs of infection: Chronic malaria accelerates telomere degradation and senescence in wild birds. Science, 347, 436–438.
Atkinson, C. T., Lease, J. K., Dusek, R. J., & Samuel, M. D. (2005). Prevalence of pox‐like lesions and malaria in forest bird communities on leeward Mauna Loa Volcano, Hawaii. The Condor, 107, 537–546.
Atkinson, C. T., Saili, K. S., Utzurrum, R. B., & Jarvi, S. I. (2013). Experimental evidence for evolved tolerance to avian malaria in a wild population of low elevation Hawai'i 'Amakihi (Hemignathus virens). EcoHealth, 10, 366–375.
Atkinson, C. T., Woods, K. L., Dusek, R. J., Sileo, L. S., & Iko, W. M. (1995). Wildlife disease and conservation in Hawaii: Pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected Iiwi (Vestiaria coccinea). Parasitology, 111, 59–69.
Bayly‐Jones, C., Bubeck, D., & Dunstone, M. A. (2017). The mystery behind membrane insertion: A review of the complement membrane attack complex. Philosophical Transactions of the Royal Society, B: Biological Sciences, 372, 20160221.
Beaumont, M. A. (2005). Adaptation and speciation: What can Fst tell us? Trends in Ecology & Evolution, 20, 435–440.
Bilgin, R., Yalcin, M. S., Yucebilgic, G., Koltas, I. S., & Yazar, S. (2012). Oxidative stress in vivax malaria. Korean Journal of Parasitology, 50, 375–377.
Blair, L. M., Granka, J. M., & Feldman, M. W. (2014). On the stability of the Bayenv method in assessing human SNP‐environment associations. Human Genomics, 8, 1–13.
Bonneaud, C., Federici, P., Sorci, G., Pérez‐Tris, J., & Chastel, O. (2006). Major histocompatibility alleles associated with local resistance to malaria in a passerine. Evolution, 60, 383–389.
Boštjančić, L. L., Francesconi, C., Rutz, C., Hoffbeck, L., Poidevin, L., Kress, A., Jussila, J., Makkonen, J., Feldmeyer, B., Bálint, M., Schwenk, K., Lecompte, O., & Theissinger, K. (2022). Host‐pathogen coevolution drives innate immune response to Aphanomyces astaci infection in freshwater crayfish: Transcriptomic evidence. BMC Genomics, 23, 600.
Brooks, M. E., Kristensen, K., Van Benthem, K. J., Magnusson, A., Berg, C. W., Nielsen, A., Skaug, H. J., Machler, M., & Bolker, B. M. (2017). glmmTMB balances speed and flexibility among packages for zero‐inflated generalized linear mixed modeling. The R Journal, 9, 378–400.
Brouwer, L., Barr, I., Van De Pol, M., Burke, T., Komdeur, J., & Richardson, D. S. (2010). MHC‐dependent survival in a wild population: Evidence for hidden genetic benefits gained through extra‐pair fertilizations. Molecular Ecology, 19, 3444–3455.
Brum, L. M., Lopez, M. C., Varela, J. C., Baker, H. V., & Moyer, R. W. (2003). Microarray analysis of A549 cells infected with rabbitpox virus (RPV): A comparison of wild‐type RPV and RPV deleted for the host range gene, SPI‐1. Virology, 315, 322–334.
Busetto, V., Barbosa, I., Basquin, J., Marquenet, E., Hocq, R., Hennion, M., Paternina, J. A., Namane, A., Conti, E., Bensaude, O., & Le Hir, H. (2020). Structural and functional insights into CWC27/CWC22 heterodimer linking the exon junction complex to spliceosomes. Nucleic Acids Research, 48, 5670–5683.
Cao, J., Teoh, M., Moon, M., & McFadden, G. (2022). Leporipoxvirus Cu‐Zn superoxide dismutase homologs inhibit cellular superoxide dismutase, but are not essential for virus replication or virulence. Virology, 296, 125–135.
Carrete, M., Serrano, D., Illera, J. C., López, G., Vögeli, M., Delgado, A., & Tella, J. L. (2009). Goats, birds, and emergent diseases: Apparent and hidden effects of exotic species in an Island environment. Ecological Applications, 19, 840–853.
Cassandri, M., Smirnov, A., Novelli, F., Pitolli, C., Agostini, M., Malewicz, M., Melino, G., & Raschellà, G. (2017). Zinc‐finger proteins in health and disease. Cell Death Discovery, 3, 17071.
Cassin‐Sackett, L., Callicrate, T. E., & Fleischer, R. C. (2019). Parallel evolution of gene classes, but not genes: Evidence from Hawai'ian honeycreeper populations exposed to avian malaria. Molecular Ecology, 28, 568–583.
Castro, A. P. V., Carvalho, T. M. U., Moussatché, N., & Damaso, C. R. A. (2003). Redistribution of cyclophilin a to viral factories during vaccinia virus infection and its incorporation into mature particles. Journal of Virology, 77, 9052–9068.
Chang, C. C., Chow, C. C., Tellier, L. C. A. M., Vattikuti, S., Purcell, S. M., & Lee, J. J. (2015). Second‐generation PLINK: Rising to the challenge of larger and richer datasets. GigaScience, 4, 7.
Charlesworth, D. (2006). Balancing selection and its effects on sequences in nearby genome regions. PLoS Genetics, 2, 379–384.
Chen, G. B., Lee, S. H., Zhu, Z. X., Benyamin, B., & Robinson, M. R. (2016). EigenGWAS: Finding loci under selection through genome‐wide association studies of eigenvectors in structured populations. Heredity, 117, 51–61.
Cheng, W., Jia, H., Wang, X., He, X., Jin, Q., Cao, J., & Jing, Z. (2018). Ectromelia virus upregulates the expression of heat shock protein 70 to promote viral replication. International Journal of Molecular Medicine, 42, 1044–1053.
Chu, Z. J., Wang, Y. J., Ying, S. H., Wang, X. W., & Feng, M. G. (2016). Genome‐wide host‐pathogen interaction unveiled by transcriptomic response of diamondback moth to fungal infection. PLoS One, 11, e0152908.
Ciloglu, A., Ellis, V. A., Bernotienė, R., Valkiūnas, G., & Bensch, S. (2019). A new one‐step multiplex PCR assay for simultaneous detection and identification of avian haemosporidian parasites. Parasitology Research, 118, 191–201.
Clark, N. J., Wells, K., Dimitrov, D., & Clegg, S. M. (2016). Co‐infections and environmental conditions drive the distributions of blood parasites in wild birds. Journal of Animal Ecology, 85, 1461–1470.
Coop, G., Witonsky, D., Di Rienzo, A., & Pritchard, J. K. (2010). Using environmental correlations to identify loci underlying local adaptation. Genetics, 185, 1411–1423.
Cox, F. E. G. (2001). Concomitant infections, parasites and immune responses. Parasitology, 122, S23–S28.
DaCosta, J. M., & Sorenson, M. D. (2014). Amplification biases and consistent recovery of loci in a double‐digest RAD‐seq protocol. PLoS One, 9, e106713.
Daszak, P., Cunningham, A. A., & Hyatt, A. D. (2000). Emerging infectious diseases of wildlife – Threats to biodiversity and human health. Science, 287, 443–449.
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.
Dawkins, R., & Krebs, J. R. (1979). Arms races between and within species. Proceedings of the Royal Society B: Biological Sciences, 205, 489–511.
Delhaye, J., Jenkins, T., & Christe, P. (2016). Plasmodium infection and oxidative status in breeding great tits, Parus major. Malaria Journal, 15, 531.
DiGiuseppe, S., Rollins, M. G., Bartom, E. T., & Walsh, D. (2018). ZNF598 plays distinct roles in interferon‐stimulated gene expression and poxvirus protein synthesis. Cell Reports, 23, 1249–1258.
Doherty, P. C., & Zinkernagel, R. M. (1975). Enhanced immunological surveillance in mice heterozygous at the H‐2 gene complex. Nature, 256, 50–52.
Douma, J. C., & Weedon, J. T. (2019). Analysing continuous proportions in ecology and evolution: A practical introduction to beta and Dirichlet regression. Methods in Ecology and Evolution, 10, 1412–1430.
Ellis, V. A., Cornet, S., Merrill, L., Kunkel, M. R., Tsunekage, T., & Ricklefs, R. E. (2015). Host immune responses to experimental infection of Plasmodium relictum (lineage SGS1) in domestic canaries (Serinus canaria). Parasitology Research, 114, 3627–3636.
Fernandes, R. C., Hasan, M., Gupta, H., Geetha, K., Rai, P. S., Hande, M. H., D'Souza, S. C., Adhikari, P., Brand, A., & Satyamoorthy, K. (2015). Host genetic variations in glutathione‐S‐transferases, superoxide dismutases and catalase genes influence susceptibility to malaria infection in an Indian population. Molecular Genetics and Genomics, 290, 1155–1168.
Ferrer‐Admetlla, A., Bosch, E., Sikora, M., Marquès‐Bonet, T., Ramírez‐Soriano, A., & Muntasell, A. (2008). Balancing selection is the main force shaping the evolution of innate immunity genes. Journal of Immunology, 181, 1315–1322.
Fischer, U., & Meese, E. (2007). Glioblastoma multiforme: The role of DSB repair between genotype and phenotype. Oncogene, 26, 7809–7815.
Forrester, D. J. (1991). The ecology and epizootiology of avian pox and malaria in wild turkeys. Bulletin of the Society for Vector Ecology, 16, 127–148.
Foster, J. T., Woodworth, B. L., Eggert, L. E., Hart, P. J., Palmer, D., Duffy, D. C., & Fleischer, R. C. (2007). Genetic structure and evolved malaria resistance in Hawaiian honeycreepers. Molecular Ecology, 16, 4738–4746.
Frichot, E., Schoville, S. D., Bouchard, G., & François, O. (2013). Testing for associations between loci and environmental gradients using latent factor mixed models. Molecular Biology and Evolution, 30, 1687–1699.
Fridavich, I. (1995). Superoxide radical and superoxide dismutases. Annual Review of Biochemistry, 64, 97–112.
Fumagalli, M., Sironi, M., Pozzoli, U., Ferrer‐Admettla, A., Pattini, L., & Nielsen, R. (2011). Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution. PLoS Genetics, 7, e1002355.
Garroway, C. J., Radersma, R., Sepil, I., Santure, A. W., De Cauwer, I., Slate, J., & Sheldon, B. C. (2013). Fine‐scale genetic structure in a wild bird population: The role of limited dispersal and environmentally based selection as causal factors. Evolution, 67, 3488–3500.
Gautier, M. (2015). Genome‐wide scan for adaptive divergence and association with population‐specific covariates. Genetics, 201, 1555–1579.
González‐Quevedo, C., Davies, R. G., Phillips, K. P., Spurgin, L. G., & Richardson, D. S. (2016). Landscape‐scale variation in an anthropogenic factor shapes immune gene variation within a wild population. Molecular Ecology, 25, 4234–4246.
González‐Quevedo, C., Davies, R. G., & Richardson, D. S. (2014). Predictors of malaria infection in a wild bird population: Landscape‐level analyses reveal climatic and anthropogenic factors. Journal of Animal Ecology, 83, 1091–1102.
González‐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.
Günther, T., & Coop, G. (2013). Robust identification of local adaptation from allele frequencies. Genetics, 195, 205–220.
Gunther, T., & Coop, G. (2018). A short manual for Bayenv2.0.
Ha, H. J., Banda, M., Alley, M. R., Howe, L., & Gartrell, B. D. (2012). The seroprevalence of avipoxvirus and its association with avian malaria (Plasmodium spp.) infection in introduced passerine birds in the southern regions of the North Island of New Zealand. Avian Diseases, 57, 109–115.
Hancock, A. M., Witonsky, D. B., Ehler, E., Alkorta‐Aranburu, G., Beall, C., Gebremedhin, A., Sukernik, R., Utermann, G., Pritchard, J., Coop, G., & di Rienzo, A. (2010). Human adaptations to diet, subsistence, and ecoregion are due to subtle shifts in allele frequency. Proceedings of the National Academy of Sciences of the United States of America, 107, 8924–8930.
Hawley, D. M., & Fleischer, R. C. (2012). Contrasting epidemic histories reveal pathogen‐mediated balancing selection on class II MHC diversity in a wild songbird. PLoS One, 7, e30222.
Hellard, E., Fouchet, D., Vavre, F., & Pontier, D. (2015). Parasite‐parasite interactions in the wild: How to detect them? Trends in Parasitology, 31, 640–652.
Hellgren, O., Atkinson, C. T., Bensch, S., Albayrak, T., Dimitrov, D., Ewen, J. G., Kim, K. S., Lima, M. R., Martin, L., Palinauskas, V., Ricklefs, R., Sehgal, R. N. M., Valkiūnas, G., Tsuda, Y., & Marzal, A. (2015). Global phylogeography of the avian malaria pathogen Plasmodium relictum based on MSP1 allelic diversity. Ecography, 38, 842–850.
Hill, A. V. S., Allsopp, C. E. M., Kwiatkowski, D., Anstey, N. M., Twumasi, P., Rowe, P. A., Bennett, S., Brewster, D., McMichael, A. J., & Greenwood, B. M. (1991). Common West African HLA antigens are associated with protection from severe malaria. Nature, 352, 595–600.
Hoban, S., Kelley, J. L., Lotterhos, K. E., Antolin, M. F., Bradburd, G., Lowry, D. B., Poss, M. L., Reed, L. K., Storfer, A., & Whitlock, M. C. (2016). Finding the genomic basis of local adaptation: Pitfalls, practical solutions, and future directions. American Naturalist, 188, 379–397.
Huang, X., Rapševičius, P., Chapa‐Vargas, L., Hellgren, O., & Bensch, S. (2019). Within‐lineage divergence of avian haemosporidians: A case study to reveal the origin of a widespread Haemoproteus parasite. Journal of Parasitology, 105, 414–422.
Huang, Y., Li, Y., Burt, D. W., Chen, H., Zhang, Y., Qian, W., Kim, H., Gan, S., Zhao, Y., Li, J., Yi, K., Feng, H., Zhu, P., Li, B., Liu, Q., Fairley, S., Magor, K. E., du, Z., Hu, X., … Li, N. (2013). The duck genome and transcriptome provide insight into an avian influenza virus reservoir species. Nature Genetics, 45, 776–783.
Illera, J. C., Emerson, B. C., & Richardson, D. S. (2007). Population history of Berthelot's pipit: Colonization, gene flow and morphological divergence in Macaronesia. Molecular Ecology, 16, 4599–4612.
Illera, J. C., Emerson, B. C., & Richardson, D. S. (2008). Genetic characterization, distribution and prevalence of avian pox and avian malaria in the Berthelot's pipit (Anthus berthelotii) in Macaronesia. Parasitology Research, 103, 1435–1443.
Illera, J. C., López, G., García‐Padilla, L., & Moreno, Á. (2017). Factors governing the prevalence and richness of avian haemosporidian communities within and between temperate mountains. PLoS One, 12, e0184587.
Jiménez‐Peñuela, J., Ferraguti, M., Martínez‐De La Puente, J., Soriguer, R. C., & Figuerola, J. (2023). Oxidative status in relation to blood parasite infections in house sparrows living along an urbanization gradient. Environmental Pollution, 316, 120712.
Jindal, S., & Young, R. A. (1992). Vaccinia virus infection induces a stress response that leads to association of Hsp70 with viral proteins. Journal of Virology, 66, 5357–5362.
Johnson, P. T. J., & Buller, I. D. (2011). Parasite competition hidden by correlated coinfection: Using surveys and experiments to understand parasite interactions. Ecology, 92, 535–541.
Kloch, A., Babik, W., Bajer, A., Siński, E., & Radwan, J. (2010). Effects of an MHC‐DRB genotype and allele number on the load of gut parasites in the bank vole Myodes glareolus. Molecular Ecology, 19, 255–265.
Kowalczyk, A., Guzik, K., Slezak, K., Dziedzic, J., & Rokita, H. (2005). Heat shock protein and heat shock factor 1 expression and localization in vaccinia virus infected human monocyte derived macrophages. Journal of Inflammation, 2, 1–10.
Kurtovic, L., Boyle, M. J., Opi, D. H., Kennedy, A. T., Tham, W. H., Reiling, L., Chan, J. A., & Beeson, J. G. (2020). Complement in malaria immunity and vaccines. Immunological Reviews, 293, 38–56.
Lachish, S., Knowles, S. C. L., Alves, R., Wood, M. J., & Sheldon, B. C. (2011). Fitness effects of endemic malaria infections in a wild bird population: The importance of ecological structure. Journal of Animal Ecology, 80, 1196–1206.
Lapointe, D. A., Atkinson, C. T., & Samuel, M. D. (2012). Ecology and conservation biology of avian malaria. Annals of the New York Academy of Sciences, 1249, 211–226.
Lauron, E. J., Oakgrove, K. S., Tell, L. A., Biskar, K., Roy, S. W., & Sehgal, R. N. M. (2014). Transcriptome sequencing and analysis of Plasmodium gallinaceum reveals polymorphisms and selection on the apical membrane antigen‐1. Malaria Journal, 13, 382.
Lewontin, R. C., & Krakauer, J. (1973). Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics, 74, 175–195.
Lochmiller, R. L., & Deerenberg, C. (2000). Trade‐offs in evolutionary immunology: Just what is the cost of immunity? Oikos, 88, 87–98.
Loiseau, C., Richard, M., Garnier, S., Chastel, O., Julliard, R., Zoorob, R., & Sorci, G. (2009). Diversifying selection on MHC class I in the house sparrow (Passer domesticus). Molecular Ecology, 18, 1331–1340.
Longley, R., Smith, C., Fortin, A., Berghout, J., McMorran, B., Burgio, G., Foote, S., & Gros, P. (2011). Host resistance to malaria: Using mouse models to explore the host response. Mammalian Genome, 22, 32–42.
Lotterhos, K. E., & Whitlock, M. C. (2015). The relative power of genome scans to detect local adaptation depends on sampling design and statistical method. Molecular Ecology, 24, 1031–1046.
Mabbott, N. A. (2018). The influence of parasite infections on host immunity to co‐infection with other pathogens. Frontiers in Immunology, 9, 2579.
Mackinnon, M. J., Ndila, C., Uyoga, S., Macharia, A., Snow, R. W., Band, G., Rautanen, A., Rockett, K. A., Kwiatkowski, D. P., & Williams, T. N. (2016). Environmental correlation analysis for genes associated with protection against malaria. Molecular Biology and Evolution, 33, 1188–1204.
MalariaGEN. (2019). Insights into malaria susceptibility using genome‐wide data on 17,000 individuals from Africa, Asia and Oceania. Nature Communications, 10, 1–19.
Martin, C. A., Armstrong, C., Illera, J. C., Emerson, B. C., Richardson, D. S., & Spurgin, L. G. (2021). Genomic variation, population history and within‐archipelago adaptation between Island bird populations. Royal Society Open Science, 8, 201146.
Martin, C. A., Sheppard, E. C., Illera, J. C., Suh, A., Nadachowska‐Brzyska, K., Spurgin, L. G., & Richardson, D. S. (2023). Runs of homozygosity reveal past bottlenecks and contemporary inbreeding across diverging Island populations of a bird. Molecular Ecology, 32, 1972–1989.
Martin, L. B., Scheuerlein, A., & Wikelski, M. (2003). Immune activity elevates energy expenditure of house sparrows: A link between direct and indirect costs? Proceedings of the Royal Society of London B, 270, 153–158.
Marzal, A., Bensch, S., Reviriego, M., Balbontin, J., & De Lope, F. (2008). Effects of malaria double infection in birds: One plus one is not two. Journal of Evolutionary Biology, 21, 979–987.
McNew, S. M., Loyola, D. C., Yepez, J., Andreadis, C., Gotanda, K., Saulsberry, A., & Fessl, B. (2022). Transcriptomic responses of Galápagos finches to avian poxvirus infection. Molecular Ecology, 31, 5552–5567.
McNew, S. M., Yepez, J., Loyola, C. D., Andreadis, C., & Fessl, B. (2021). Transcriptomic responses of Galápagos finches to avian pox virus infection. BioRxiv, https://doi.org/10.1101/2021.10.15.46458
Miller, C. G., Justus, D. E., Jayaraman, S., & Kotwal, G. J. (1995). Severe and prolonged inflammatory response to localized cowpox virus infection in footpads of C5‐deficient mice: Investigation of the role of host complement in poxvirus pathogenesis. Cellular Immunology, 162, 326–332.
Mukhin, A., Palinauskas, V., Platonova, E., Kobylkov, D., Vakoliuk, I., & Valkiunas, G. (2016). The strategy to survive primary malaria infection: An experimental study on behavioural changes in parasitized birds. PLoS One, 11, e0159216.
Musa, S., Mackenstedt, U., Woog, F., & Dinkel, A. (2022). Untangling the actual infection status: Detection of avian haemosporidian parasites of three Malagasy bird species using microscopy, multiplex PCR, and nested PCR methods. Parasitology Research, 121, 2817–2829.
Names, G. R., Schultz, E. M., Hahn, T. P., Hunt, K. E., Angelier, F., Ribout, C., & Klasing, K. C. (2021). Variation in immunity and health in response to introduced avian malaria in an endemic Hawaiian songbird. Animal Conservation, 25, 455–466.
Names, G. R., Schultz, E. M., Krause, J. S., Hahn, T. P., Wingfield, J. C., Heal, M., Cornelius, J. M., Klasing, K. C., & Hunt, K. E. (2021). Stress in paradise: Effects of elevated corticosterone on immunity and avian malaria resilience in a Hawaiian passerine. The Journal of Experimental Biology, 224, 1–9. https://doi.org/10.1242/jeb.242951
Narsaria, N., Mohanty, C., Das, B. K., Mishra, S. P., & Prasad, R. (2012). Oxidative stress in children with severe malaria. Journal of Tropical Pediatrics, 58, 147–150.
Nneji, C. M., Adaramoye, O. A., Falade, C. O., & Ademowo, O. G. (2013). Effect of chloroquine, methylene blue and artemether on red cell and hepatic antioxidant defence system in mice infected with Plasmodium yoelii nigeriensis. Parasitology Research, 112, 2619–2625.
Ots, I., Kerimov, A. B., Ivankina, E. V., Ilyina, T. A., & Hõrak, P. (2001). Immune challenge affects basal metabolic activity in wintering great tits. Proceedings of the Royal Society of London B, 268, 1175–1181.
Padilla, D. P., Illera, J. C., Gonzalez‐Quevedo, C., Villalba, M., & Richardson, D. S. (2017). Factors affecting the distribution of haemosporidian parasites within an oceanic Island. International Journal for Parasitology, 47, 225–235.
Palinauskas, V., Valkiunas, G., Bolshakov, C. V., & Bensch, S. (2008). Plasmodium relictum (lineage P‐SGS1): Effects on experimentally infected passerine birds. Experimental Parasitology, 120, 372–380.
Pamplona, R., & Costantini, D. (2011). Molecular and structural antioxidant defenses against oxidative stress in animals. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 301, 843–863.
Pardo‐Diaz, C., Salazar, C., & Jiggins, C. D. (2015). Towards the identification of the loci of adaptive evolution. Methods in Ecology and Evolution, 6, 445–464.
Paterson, S., Vogwill, T., Buckling, A., Benmayor, R., Spiers, A. J., Thomson, N. R., Quail, M., Smith, F., Walker, D., Libberton, B., Fenton, A., Hall, N., & Brockhurst, M. A. (2010). Antagonistic coevolution accelerates molecular evolution. Nature, 464, 275–278.
Pigeault, R., Cozzarolo, C., Glaizot, O., & Christe, P. (2020). Effect of age, haemosporidian infection and body condition on pair composition and reproductive success in great tits Parus major. Ibis, 162, 613–626.
Popa, G. L., & Popa, M. I. (2021). Recent advances in understanding the inflammatory response in malaria: A review of the dual role of cytokines. Journal of Immunology Research, 2021, 1–9.
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 (Capreolus capreolus). Molecular Ecology, 24, 3873–3887.
Quin, J. E., Bujila, I., Chérif, M., Sanou, G. S., Qu, Y., Vafa Homann, M., Rolicka, A., Sirima, S. B., O'Connell, M. A., Lennartsson, A., Troye‐Blomberg, M., Nebie, I., & Östlund Farrants, A. K. (2017). Major transcriptional changes observed in the Fulani, an ethnic group less susceptible to malaria. eLife, 6, 1–19.
R Core Team. (2023). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R‐project.org/
Råberg, L., Graham, A. L., & Read, A. F. (2009). Decomposing health: Tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society, B: Biological Sciences, 364, 37–49.
Råberg, L., Sim, D., & Read, A. F. (2007). Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science, 318, 812–814.
Ravenhall, M., Campino, S., Sepúlveda, N., Manjurano, A., Nadjm, B., Mtove, G., Wangai, H., Maxwell, C., Olomi, R., Reyburn, H., Drakeley, C. J., Riley, E. M., Clark, T. G., & in collaboration with MalariaGEN. (2018). Novel genetic polymorphisms associated with severe malaria and under selective pressure in North‐eastern Tanzania. PLoS Genetics, 14, e1007172.
Rellstab, C., Gugerli, F., Eckert, A. J., Hancock, A. M., & Holderegger, R. (2015). A practical guide to environmental association analysis in landscape genomics. Molecular Ecology, 24, 4348–4370.
Reuling, I. J., de Jong, G. M., Yap, X. Z., Asghar, M., Walk, J., van de Schans, L. A., Koelewijn, R., Färnert, A., de Mast, Q., van der Ven, A. J., Bousema, T., van Hellemond, J. J., van Genderen, P. J. J., & Sauerwein, R. W. (2018). Liver injury in uncomplicated malaria is an overlooked phenomenon: An observational study. eBioMedicine, 36, 131–139.
Richardson, D. S., Jury, F. L., Blaakmeer, K., Komdeur, J., & Burke, T. (2001). Parentage assignment and extra‐group paternity in a cooperative breeder: The Seychelles warbler (Acrocephalus sechellensis). Molecular Ecology, 10, 2263–2273.
Rockett, K. A., Clarke, G. M., Fitzpatrick, K., Hubbart, C., Jeffreys, A. E., Rowlands, K., Craik, R., Jallow, M., Conway, D. J., Bojang, K. A., Pinder, M., Usen, S., Sisay‐Joof, F., Sirugo, G., Toure, O., Thera, M. A., Konate, S., Sissoko, S., Niangaly, A., … Kwiatkowski, D. P. (2014). Reappraisal of known malaria resistance loci in a large multicenter study. Nature Genetics, 46, 1197–1204.
Roestenberg, M., McCall, M., Mollnes, T. E., van Deuren, M., Sprong, T., Klasen, I., Hermsen, C. C., Sauerwein, R. W., & van der Ven, A. (2007). Complement activation in experimental human malaria infection. Transactions of the Royal Society of Tropical Medicine and Hygiene, 101, 643–649.
Rosenblum, E. B., Poorten, T. J., Settles, M., & Murdoch, G. K. (2012). Only skin deep: Shared genetic response to the deadly chytrid fungus in susceptible frog species. Molecular Ecology, 21, 3110–3120.
Samuel, M. D., Woodworth, B. L., Atkinson, C. T., Hart, P. J., & LaPointe, D. A. (2018). The epidemiology of avian pox and interaction with avian malaria in Hawaiian forest birds. Ecological Monographs, 88, 621–637.
Scaccabarozzi, D., Deroost, K., Corbett, Y., Lays, N., Corsetto, P., Salè, F. O., Van den Steen, P. E., & Taramelli, D. (2018). Differential induction of malaria liver pathology in mice infected with Plasmodium chabaudi AS or Plasmodium berghei NK65. Malaria Journal, 17, 18.
Schat, K. A., & Skinner, M. A. (2013). Avian immunosuppressive diseases and immune evasion. In Avian immunology (2nd ed., pp. 275–297). Academic Press.
Schoville, S. D., Bonin, A., François, O., Lobreaux, S., Melodelima, C., & Manel, S. (2012). Adaptive genetic variation on the landscape: Methods and cases. Annual Review of Ecology, Evolution, and Systematics, 43, 23–43.
Sedger, L., & Ruby, J. (1994). Heat shock response to vaccinia virus infection. Journal of Virology, 68, 4685–4689.
Sehgal, R. N. M. (2015). Manifold habitat effects on the prevalence and diversity of avian blood parasites. International Journal for Parasitology: Parasites and Wildlife, 4, 421–430.
Sepil, I., Lachish, S., Hinks, A. E., & Sheldon, B. C. (2013). MHC supertypes confer both qualitative and quantitative resistance to avian malaria infections in a wild bird population. Proceedings of the Royal Society B: Biological Sciences, 280, 20130134.
Sheppard, E. C., Martin, C. A., Illera, J. C., Suh, A., Spurgin, L. G., & Richardson, D. S. (2022). Genomic associations with pox virus across divergent populations in Berthelot's pipit. Molecular Ecology, 31, 3154–3173.
Silver, K. L., Higgins, S. J., Mcdonald, C. R., & Kain, K. C. (2010). Complement driven innate immune response to malaria: Fuelling severe malarial diseases. Wiley Online Library, 12, 1036–1045.
Slade, R. W., & McCallum, H. I. (1992). Overdominant vs. frequency‐dependent selection at MHC loci. Genetics, 132, 861–862.
Sommer, S. (2005). The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Frontiers in Zoology, 2, 16–34.
Sottile, M. L., & Nadin, S. B. (2018). Heat shock proteins and DNA repair mechanisms: An updated overview. Cell Stress and Chaperones, 23, 303–315.
Spurgin, L. G., Illera, J. C., Jorgensen, T. H., Dawson, D. A., & Richardson, D. S. (2014). Genetic and phenotypic divergence in an Island bird: Isolation by distance, by colonization or by adaptation? Molecular Ecology, 23, 1028–1039.
Spurgin, L. G., Illera, J. C., Padilla, D. P., & Richardson, D. S. (2012). Biogeographical patterns and co‐occurrence of pathogenic infection across Island populations of Berthelot's pipit (Anthus berthelotii). Oecologia, 168, 691–701.
Spurgin, L. G., & Richardson, D. S. (2010). How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proceedings of the Royal Society B: Biological Sciences, 277, 979–988.
Srivastava, P., Puri, S. K., Dutta, G. P., & Pandey, V. C. (1992). Status of oxidative stress and antioxidant defences during Plasmodivm knowlesi infection and chloroquine treatment in Macaca mulatta. International Journal for Parasitology, 22, 243–245.
Stewart, M. D., Ritterhoff, T., Klevit, R. E., & Brzovic, P. S. (2016). E2 enzymes: More than just middle men. Cell Research, 26, 423–440.
Sundaramoorthy, E., Ryan, A. P., Fulzele, A., Leonard, M., Daugherty, M. D., & Bennett, E. J. (2021). Ribosome quality control activity potentiates vaccinia virus protein synthesis during infection. Journal of Cell Science, 134, 1–12.
Szabó, C. (2003). Multiple pathways of peroxynitrite cytotoxicity. Toxicology Letters, 140–141, 105–112.
Teoh, M. L. T., Turner, P. V., & Evans, D. H. (2005). Tumorigenic poxviruses up‐regulate intracellular superoxide to inhibit apoptosis and promote cell proliferation. Journal of Virology, 79, 5799–5811.
Teoh, M. L. T., Walasek, P. J., & Evans, D. H. (2003). Leporipoxvirus Cu,Zn‐superoxide dismutase (SOD) homologs are catalytically inert decoy proteins that bind copper chaperone for SOD. The Journal of Biological Chemistry, 278, 33175–33184.
Tschirren, B., Råberg, L., & Westerdahl, H. (2011). Signatures of selection acting on the innate immunity gene toll‐like receptor 2 (TLR2) during the evolutionary history of rodents. Journal of Evolutionary Biology, 24, 1232–1240.
Valkiunas, G. (2005). Avian malaria parasites and other Haemosporidia. CRC Press.
van de Crommenacker, J., Richardson, D. S., Koltz, A. M., Hutchings, K., & Komdeur, J. (2012). Parasitic infection and oxidative status are associated and vary with breeding activity in the Seychelles warbler. Proceedings of the Royal Society B: Biological Sciences, 279, 1466–1476.
Vasquez, M., Zuniga, M., & Rodriguez, A. (2021). Oxidative stress and pathogenesis in malaria. Frontiers in Cellular and Infection Microbiology, 11, 768182.
Videvall, E., Cornwallis, C. K., Palinauskas, V., Valkiunas, G., & Hellgren, O. (2015). The avian transcriptome response to malaria infection. Molecular Biology and Evolution, 32, 1255–1267.
Videvall, E., Palinauskas, V., Valkiūnas, G., & Hellgren, O. (2020). Host transcriptional responses to high‐ and low‐virulent avian malaria parasites. American Naturalist, 195, 1079–1084.
Voelker, G. (1999). Dispersal, vicariance, and clocks: Historical biogeography and speciation in a cosmopolitan passerine genus (Anthus: Motacillidae). Evolution, 53, 1536–1552.
Waldenström, J., Bensch, S., Hasselquist, D., & Östman, Ö. (2004). A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology, 90, 191–194.
Warren, W. C., Clayton, D. F., Ellegren, H., Arnold, A. P., Hillier, L. W., Künstner, A., Searle, S., White, S., Vilella, A. J., Fairley, S., Heger, A., Kong, L., Ponting, C. P., Jarvis, E. D., Mello, C. V., Minx, P., Lovell, P., Velho, T. A. F., Ferris, M., … Wilson, R. K. (2010). The genome of a songbird. Nature, 464, 757–762.
Yorinks, N., Atkinson, T., & Carter, T. (2000). Effects of malaria on activity budgets of experimentally infected juvenile apapane (Himatione sanguinea). The Auk, 117, 731–738.
Zhou, Y., Gao, F., Lv, L., Wang, S., He, W., Lan, Y., Li, Z., Lu, H., Song, D., Guan, J., & Zhao, K. (2021). Host factor cyclophilin B affects Orf virus replication by interacting with viral ORF058 protein. Veterinary Microbiology, 258, 109099.
Zueva, K. J., Lumme, J., Veselov, A. E., Kent, M. P., Lien, S., & Primmer, C. R. (2014). Footprints of directional selection in wild Atlantic salmon populations: Evidence for parasite‐driven evolution? PLoS One, 9, 91672.
Zueva, K. J., Lumme, J., Veselov, A. E., Kent, M. P., & Primmer, C. R. (2018). Genomic signatures of parasite‐driven natural selection in north European Atlantic salmon (Salmo salar). Marine Genomics, 39, 26–38.