Ecology

1.Sala, O. E. et al. Global biodiversity scenarios for the year 2100. Science 287, 1770–1774 (2000).CAS 
Article 

Google Scholar 
2.Sakai, A. K. et al. The population biology of invasive species. Annu. Rev. Ecol. Evol. Syst. 32, 305–312 (2001).Article 

Google Scholar 
3.Buckingham, G. R. Biological control of alligator weed, Alternanthera philoxeroides, the world’s first aquatic weed success story. Castanea 61, 232–243 (1996).
Google Scholar 
4.Bassett, I., Paynter, Q., Hankin, R. & Beggs, J. R. Characterising alligator weed (Alternanthera philoxeroides; Amaranthaceae) invasion at a northern New Zealand lake. New Zeal. J. Ecol. 36, 216–222 (2012).
Google Scholar 
5.Chatterjee, A. & Dewanji, A. Effect of varying Alternanthera philoxeroides (alligator weed) cover on the macrophyte species diversity of pond ecosystems: A quadrat-based study. Aquat. Invasions 9, 343–355 (2014).Article 

Google Scholar 
6.Xu, C. Y., Zhang, W. J., Fu, C. Z. & Lu, B. R. Genetic diversity of alligator weed in China by RAPD analysis. Biodivers. Conserv. 12, 637–645 (2003).Article 

Google Scholar 
7.Wang, B. R., Li, W. G. & Wang, J. B. Genetic diversity of Alternanthera philoxeroides in China. Aquat. Bot. 81, 277–283 (2005).Article 

Google Scholar 
8.Geng, Y. P. et al. Phenotypic plasticity of invasive Alternanthera philoxeroides in relation to different water availability, compared to its native congener. Acta. Oecol. 30, 380–385 (2006).ADS 
Article 

Google Scholar 
9.Pan, X. Y., Geng, Y. P., Zhang, W. J., Li, B. & Chen, J. K. The influence of abiotic stress and phenotypic plasticity on the distribution of invasive Alternanthera philoxeroides along a riparian zone. Acta. Oecol. 30, 333–341 (2006).ADS 
Article 

Google Scholar 
10.Peng, X. M. et al. Vegetative propagation capacity of invasive alligator weed through small stolon fragments under different treatments. Sci. Rep. 7, 43826. https://doi.org/10.1038/srep43826 (2017).ADS 
Article 
PubMed 
PubMed Central 

Google Scholar 
11.Dugdale, T., Clements, D., Hunt, T. & Butler, K. Alligator weed produces viable stem fragments in response to herbicide treatment. J. Aquat. Plant Manag. 48, 84–91 (2010).
Google Scholar 
12.Chen, Y., Zhou, Y., Yin, T. F., Liu, C. X. & Lou, F. L. The invasive wetland plant Alternanthera philoxeroides shows a higher tolerance to waterlogging than its native congener Alternanthera sessilis. PloS One 8, e81456. https://doi.org/10.1371/journal.pone.0081456 (2013).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
13.Tao, Y., Chen, F., Wan, K. Y., Li, X. W. & Li, J. Q. The structural adaptation of aerial parts of invasive Alternanthera philoxeroides to water regime. J. Plant Biol. 52, 403–410 (2009).Article 

Google Scholar 
14.Wang, N. et al. Clonal integration supports the expansion from terrestrial to aquatic environments of the amphibious stoloniferous herb Alternanthera philoxeroides. Plant Biol. 11, 483–489 (2009).CAS 
PubMed 
Article 

Google Scholar 
15.Fan, S. F. et al. The effects of complete submergence on the morphological and biomass allocation response of the invasive plant Alternanthera philoxeroides. Hydrobiologia 746, 159–169 (2015).CAS 
Article 

Google Scholar 
16.Wang, H. F. et al. Effects of submergence on growth, survival and recovery growth of Alternanthera philoxeroides. J. Wuhan Bot. Res. 26, 147–152 (2008).
Google Scholar 
17.Zhang, H. J. et al. Effects of submergence and eutrophication on the morphological traits and biomass allocation of the invasive plant Alternanthera philoxeroides. J. Freshw. Ecol. 31, 341–349 (2016).CAS 
Article 

Google Scholar 
18.Sun, J. F. et al. Addition of Phosphorus and nitrogen support the invasiveness of Alternanthera philoxeroides under water stress. Clean Soil Air Water 48, 2000059. https://doi.org/10.1002/clen.202000059 (2020).CAS 
Article 

Google Scholar 
19.Zhou, J., Li, H. L., Alpert, P., Zhang, M. X. & Yu, F. H. Fragmentation of the invasive, clonal plant Alternanthera philoxeroides decreases its growth but not its competitive effect. Flora 228, 17–23 (2017).Article 

Google Scholar 
20.Danckwerts, J. E. & Gordon, A. J. Long-term partitioning, storage and remobilization of 14C assimilated by Trifolium repens (cv. Blanc). Ann. Bot. 64, 533–544 (1989).Article 

Google Scholar 
21.Corre, N., Bouchart, V., Ourry, A. & Boucaud, J. Mobilization of nitrogen reserves during regrowth of defoliated Trifolium repens L. and identification of potential vegetative storage proteins. J. Exp. Bot. 47, 1111–1118 (1996).CAS 
Article 

Google Scholar 
22.Granstedt, R. C. & Huffaker, R. C. Identification of the leaf vacuole as a major nitrate storage pool. Plant Physiol. 70, 410–413 (1982).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
23.Dong, B. C. et al. How internode length, position and presence of leaves affect survival and growth of Alternanthera philoxeroides after fragmentation?. Evol. Ecol. 24, 1447–1461 (2010).Article 

Google Scholar 
24.Wu, Y. J., Du, T. S. & Wang, L. X. Isotope signature of maize stem and leaf and investigation of transpiration and water transport. Agric. Water Manag. 247, 106727. https://doi.org/10.1016/j.agwat.2020.106727 (2021).Article 

Google Scholar 
25.Khaitov, B. et al. Licorice (Glycyrrhiza glabra)—Growth and phytochemical compound secretion in degraded lands under drought stress. Sustainability 13, 2923. https://doi.org/10.3390/su13052923 (2021).Article 

Google Scholar 
26.Poorter, H., Remkes, C. & Lambers, H. Carbon and nitrogen economy of 24 wild species differing in relative growth rate. Plant Physiol. 94, 621–627 (1990).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
27.Mommer, L. & Visser, E. J. W. Underwater photosynthesis in flooded terrestrial plants: A matter of leaf plasticity. Ann. Bot. Lond. 96, 581–589 (2005).CAS 
Article 

Google Scholar 
28.Gibbs, J. & Greenway, H. Review: Mechanisms of anoxia tolerance in plants I. Growth, survival and anaerobic catabolism. Funct. Plant Biol. 30, 353 (2003).PubMed 
Article 

Google Scholar 
29.Wang, H. F. et al. Survival and growth response of Vetiveria zizanioides, Acorus calamus and Alternanthera philoxeroides to long-term submergence. Acta Ecol. Sinica 28, 2571–2580 (2008).Article 

Google Scholar 
30.Singh, H. B., Singh, B. B. & Ram, P. C. Submergence tolerance of rain fed lowland rice: Search for physiological marker traits. J. Plant Physiol. 158, 883–889 (2001).CAS 
Article 

Google Scholar 
31.Das, K. K., Sarkar, R. K. & Ismail, A. M. Elongation ability and nonstructural carbohydrate levels in relation to submergence tolerance in rice. Plant Sci. 168, 131–136 (2005).CAS 
Article 

Google Scholar 
32.Laan, P. & Blom, C. W. P. M. Growth and survival responses of Rumex species to flooded and submerged conditions: The importance of shoot elongation, underwater photosynthesis and reserve carbohydrates. J. Exp. Bot. 228, 775–783 (1990).Article 

Google Scholar 
33.Lynn, D. E. & Waldren, S. Survival of Ranunculus repens L. (Creeping Buttercup) in an amphibious habitat. Ann. Bot. Lond. 91, 75–84 (2003).CAS 
Article 

Google Scholar 
34.Kende, H., van deer Knaap, E. & Cho, H. T. Deep water rice: A model plant to study stem elongation. Plant Physiol. 118, 1105–1110 (1998).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
35.Voesenek, L. A. C. J. et al. Plant hormones regulate fast shoot elongation under water: From genes to communities. Ecology 85, 16–27 (2003).Article 

Google Scholar 
36.Voesenek, L. A. C. J. et al. How plants cope with complete submergence. New Phytol. 170, 213–226 (2006).CAS 
PubMed 
Article 

Google Scholar 
37.Groeneveld, H. W. & Voesenek, L. A. C. J. Submergence-induced petiole elongation in Rumex palustris is controlled by developmental stage and storage compounds. Plant Soil. 253, 115–123 (2003).CAS 
Article 

Google Scholar 
38.Jackson, M. B. & Colmer, T. D. Response and adaptation by plants to flooding stress. Ann. Bot. Lond. 96, 501–505 (2005).CAS 
Article 

Google Scholar 
39.Banach, K. et al. Differences in flooding tolerance between species from two wetland habitats with contrasting hydrology: Implications for vegetation development in future floodwater retention areas. Ann. Bot Lond. 103, 341–351 (2009).Article 

Google Scholar 
40.Bailey-Serres, J. & Voesenek, L. A. C. J. Flooding stress: Acclimations and genetic diversity. Annu. Rev. Plant Biol. 59, 313–339 (2008).CAS 
PubMed 
Article 

Google Scholar 
41.Kawano, N., Ito, O. & Sakagami, J. I. Morphological and physiological responses of rice seedlings to complete submergence (flash flooding). Ann. Bot. Lond. 103, 161–169 (2009).Article 

Google Scholar 
42.Luo, F. L. et al. Recovery dynamics of growth, photosynthesis and carbohydrate accumulation after de-submergence: A comparison between two wetland plants showing escape and quiescence strategies. Ann. Bot. Lond. 107, 49–63 (2011).CAS 
Article 

Google Scholar 
43.Akman, M. et al. Wait or escape? Contrasting submergence tolerance strategies of Rorippa amphibia, Rorippa sylvestris and their hybrid. Ann. Bot. Lond. 109, 1263–1275 (2012).CAS 
Article 

Google Scholar 
44.He, J. B. et al. Survival tactics of Ranunculus species in river floodplains. Oecologia 118, 1–8 (1999).ADS 
CAS 
PubMed 
Article 

Google Scholar 
45.Julien, M. H., Bourne, A. S. & Low, V. H. K. Growth of the weed Alternanthera philoxeroides (Martius) Grisebach, (alligator weed) in aquatic and terrestrial habitats in Australia. Plant Prot. Q. 7, 102–108 (1992).
Google Scholar 
46.Mauchamp, A., Blanch, S. & Grillas, P. Effects of submergence on the growth of Phragmites australis seedlings. Aquat. Bot. 69, 147–164 (2001).Article 

Google Scholar 
47.Chen, H. J., Qualls, R. G. & Miller, G. C. Adaptive responses of Lepidium latifolium to soil flooding: Biomass allocation, adventitious rooting, aerenchyma formation and ethylene production. Environ. Exp. Bot. 48, 119–128 (2002).Article 

Google Scholar 
48.Shen, J. Y., Shen, M. Q., Wang, X. H. & Lu, Y. T. Effect of environmental factors on shoot emergence and vegetative growth of alligatrorweed (Alternanthera philoxeroides). Weed Sci. 53, 471–478 (2005).CAS 
Article 

Google Scholar 
49.Schooler, S. S. Alternanthera philoxeroides (Martius) Grisebach. A Handbook of Global Freshwater Invasive Species (ed. Francis, R. A.) 25–35 (Earthscan, 2012).50.Blom, C. W. P. M. & Voesenek, L. A. C. J. Flooding: The survival strategies of plants. Trends Ecol. Evol. 11, 290–295 (1996).CAS 
PubMed 
Article 

Google Scholar 
51.Vartapetian, B. B. & Jackson, M. B. Plant adaptations to anaerobic stress. Ann. Bot-London 79, 3–20 (1997).CAS 
Article 

Google Scholar 
52.Visser, E. J. W., Bögemann, G. M., Van De Steeg, H. M., Pierik, R. & Blom, C. W. P. M. Flooding tolerance of Carex species in relation to field distribution and aerenchyma formation. New Phytol. 148, 93–103 (2000).CAS 
PubMed 
Article 

Google Scholar 
53.Ruprecht, E., Fenesi, A. & Nijs, I. Are plasticity in functional traits and constancy in performance traits linked with invasiveness? An experimental test comparing invasive and naturalized plant species. Biol. Invasions 16, 1359–1372 (2014).Article 

Google Scholar 
54.Poorter, H. et al. Biomass allocation to leaves, stems and roots: Meta-analyses of interspecific variation and environmental control. New Phytol. 193, 30–50 (2012).CAS 
PubMed 
Article 

Google Scholar 
55.Fu, H. et al. An alternative mechanism for shade adaptation: Implication of allometric responses of three submersed macrophytes to water depth. Ecol. Res. 27, 1087–1094 (2012).Article 

Google Scholar 
56.The weather network. https://www.tianqi.com/ More

1.Honey: market value worldwide 2007–2016. https://www.statista.com/statistics/933928/global-market-value-of-honey/. Accessed Nov 2020.2.Highfield AC, El Nagar A, Mackinder LCM, Noël LM-LJ, Hall MJ, Martin SJ, et al. Deformed wing virus implicated in overwintering honeybee colony losses. Appl Environ Microbiol. 2009;75:7212–20.CAS 
PubMed 
PubMed Central 

Google Scholar 
3.Ongus JR, Peters D, Bonmatin JM, Bengsch E, Vlak JM, van Oers MM. Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. J Gen Virol. 2004;85:3747–55.CAS 
PubMed 

Google Scholar 
4.Lanzi G, Miranda JRD, Boniotti MB, Cameron CE, Lavazza A, Capucci L, et al. Molecular and biological characterization of Deformed wing virus of honeybees (Apis mellifera L.). J Virol. 2006;80:4998–5009.CAS 
PubMed 
PubMed Central 

Google Scholar 
5.Fujiyuki T, Takeuchi H, Ono M, Ohka S, Sasaki T, Nomoto A, et al. Kakugo virus from brains of aggressive worker honeybees. Adv Virus Res. 2005;65:1–27.CAS 
PubMed 

Google Scholar 
6.Dalmon A, Desbiez C, Coulon M, Thomasson M, Le Conte Y, Alaux C, et al. Evidence for positive selection and recombination hotspots in Deformed wing virus (DWV). Sci Rep. 2017;7:41045.CAS 
PubMed 
PubMed Central 

Google Scholar 
7.Zioni N, Soroker V, Chejanovsky N. Replication of Varroa destructor virus 1 (VDV-1) and a Varroa destructor virus 1–deformed wing virus recombinant (VDV-1–DWV) in the head of the honey bee. Virology. 2011;417:106–12.CAS 
PubMed 

Google Scholar 
8.Ryabov EV, Childers AK, Chen Y, Madella S, Nessa A, Vanengelsdorp D, et al. Recent spread of Varroa destructor virus – 1, a honey bee pathogen, in the United States. Sci Rep. 2017;7:17447.PubMed 
PubMed Central 

Google Scholar 
9.Moore J, Jironkin A, Chandler D, Burroughs N, Evans DJ, Ryabov EV. Recombinants between Deformed wing virus and Varroa destructor virus-1 may prevail in Varroa destructor-infested honeybee colonies. J Gen Virol. 2011;92:156–61.CAS 
PubMed 

Google Scholar 
10.Mordecai GJ, Brettell LE, Martin SJ, Dixon D, Jones IM, Schroeder DC. Superinfection exclusion and the long-term survival of honey bees in Varroa-infested colonies. ISME J. 2015;10:1182–91.PubMed 
PubMed Central 

Google Scholar 
11.Woodford L, Evans DJ. Deformed wing virus: using reverse genetics to tackle unanswered questions about the most important viral pathogen of honey bees. FEMS Microbiol Rev. 2020; fuaa070, https://doi.org/10.1093/femsre/fuaa070.12.Mordecai GJ, Wilfert L, Martin SJ, Jones IM, Schroeder DC. Diversity in a honey bee pathogen: first report of a third master variant of the Deformed Wing Virus quasispecies. ISME J. 2016;10:1264–73.CAS 
PubMed 

Google Scholar 
13.McMahon DP, Natsopoulou ME, Doublet V, Fürst M, Weging S, Brown MJF, et al. Elevated virulence of an emerging viral genotype as a driver of honeybee loss. Proc Biol Sci. 2016;283:443–9.
Google Scholar 
14.Wilfert L, Long G, Leggett HC, Schmid-Hempel P, Butlin R, Martin SJM, et al. Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science. 2016;351:594–7.CAS 
PubMed 

Google Scholar 
15.de Miranda JR, Genersch E. Deformed wing virus. J Invertebr Pathol. 2010;103:S48–S61.PubMed 

Google Scholar 
16.Roberts JMK, Anderson DL, Durr PA. Absence of deformed wing virus and Varroa destructor in Australia provides unique perspectives on honeybee viral landscapes and colony losses. Sci Rep. 2017;7:6925.PubMed 
PubMed Central 

Google Scholar 
17.Yue C, Schröder M, Gisder S, Genersch E. Vertical-transmission routes for deformed wing virus of honeybees (Apis mellifera). J Gen Virol. 2007;88:2329–36.CAS 
PubMed 

Google Scholar 
18.Ryabov EV, Childers AK, Lopez D, Grubbs K, Posada-Florez F, Weaver D, et al. Dynamic evolution in the key honey bee pathogen deformed wing virus: novel insights into virulence and competition using reverse genetics. PLoS Biol. 2019; 17; https://doi.org/10.1371/journal.pbio.3000502.19.Martin SJ, Highfield AC, Brettell L, Villalobos EM, Budge GE, Powell M, et al. Global honey bee viral landscape altered by a parasitic mite. Science. 2012;336:1304–6.CAS 
PubMed 

Google Scholar 
20.Loope KJ, Baty JW, Lester PJ, Wilson Rankin EE. Pathogen shifts in a honeybee predator following the arrival of the Varroa mite. Proc Biol Sci. 2019;286:20182499.CAS 
PubMed 
PubMed Central 

Google Scholar 
21.Ryabov EV, Wood GR, Fannon JM, Moore JD, Bull JC, Chandler D, et al. A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission. PLoS Pathog. 2014;10:e1004230.PubMed 
PubMed Central 

Google Scholar 
22.Kevill JL, de Souza FS, Sharples C, Oliver R, Schroeder DC, Martin SJ. DWV-A lethal to honey bees (Apis mellifera): a colony level survey of DWV variants (A, B, and C) in England, Wales, and 32 States across the US. Viruses. 2019;11:426.PubMed Central 

Google Scholar 
23.Tehel A, Vu Q, Bigot D, Gogol-Döring A, Koch P, Jenkins C, et al. The two prevalent genotypes of an emerging infectious disease, Deformed wing virus, cause equally low pupal mortality and equally high wing deformities in host honey bees. Viruses. 2019;11:114.CAS 
PubMed Central 

Google Scholar 
24.Norton AM, Remnant EJ, Buchmann G, Beekman M. Accumulation and competition amongst Deformed wing virus genotypes in naïve Australian honeybees provides insight Into the increasing global prevalence of genotype B. Front Microbiol. 2020;11:620.PubMed 
PubMed Central 

Google Scholar 
25.Gusachenko ON, Woodford L, Balbirnie-Cumming K, Campbell EM, Christie CR, Bowman AS, et al. Green bees: reverse genetic analysis of Deformed wing virus transmission, replication, and tropism. Viruses. 2020;12:532.CAS 
PubMed Central 

Google Scholar 
26.Steck FT, Rubin H. The mechanism of interference between an avian leukosis virus and Rous sarcoma virus. II. Early steps of infection by RSV of cells under conditions of interference. Virology. 1966;29:642–53.CAS 
PubMed 

Google Scholar 
27.Adams RH, Brown DT. BHK cells expressing Sindbis virus-induced homologous interference allow the translation of nonstructural genes of superinfecting virus. J Virol. 1985;54:351–7.CAS 
PubMed 
PubMed Central 

Google Scholar 
28.Strauss JH, Strauss EG. The alphaviruses: gene expression, replication, and evolution. Microbiol Rev. 1994;58:491–562.CAS 
PubMed 
PubMed Central 

Google Scholar 
29.Karpf AR, Lenches E, Strauss EG, Strauss JH, Brown DT. Superinfection exclusion of alphaviruses in three mosquito cell lines persistently infected with Sindbis virus. J Virol. 1997;71:7119–23.CAS 
PubMed 
PubMed Central 

Google Scholar 
30.Singh IR, Suomalainen M, Varadarajan S, Garoff H, Helenius A. Multiple mechanisms for the inhibition of entry and uncoating of superinfecting Semliki Forest virus. Virology. 1997;231:59–71.CAS 
PubMed 

Google Scholar 
31.Geib T, Sauder C, Venturelli S, Hässler C, Staeheli P, Schwemmle M. Selective virus resistance conferred by expression of Borna disease virus nucleocapsid components. J Virol. 2003;77:4283–90.CAS 
PubMed 
PubMed Central 

Google Scholar 
32.Edwards MC, Bragg J, Jackson AO. Natural resistance mechanisms to viruses in barley. In: Loebenstein G and Carr JP, editors. Natural Resistance Mechanisms of Plants to Viruses. Dordrecht, The Netherlands: Springer; 2006. p. 465–501.33.Bergua M, Zwart MP, El-Mohtar C, Shilts T, Elena SF, Folimonova SY. A viral protein mediates superinfection exclusion at the whole-organism level but Is not required for exclusion at the cellular Level. J Virol. 2014;88:11327–38.PubMed 
PubMed Central 

Google Scholar 
34.Michel N, Allespach I, Venzke S, Fackler OT, Keppler OT. The Nef protein of human immunodeficiency virus establishes superinfection immunity by a dual strategy to downregulate cell-surface CCR5 and CD4. Curr Biol. 2005;15:714–23.CAS 
PubMed 

Google Scholar 
35.Tscherne DM, Evans MJ, von Hahn T, Jones CT, Stamataki Z, McKeating JA, et al. Superinfection exclusion in cells infected with hepatitis C virus. J Virol. 2007;81:3693–703.CAS 
PubMed 
PubMed Central 

Google Scholar 
36.Leonard SP, Powell JE, Perutka J, Geng P, Heckmann LC, Horak RD, et al. Engineered symbionts activate honey bee immunity and limit pathogens. Science. 2020;367:573–6.CAS 
PubMed 
PubMed Central 

Google Scholar 
37.Lamp B, Url A, Seitz K, Rgen Eichhorn J, Riedel C, Sinn LJ, et al. Construction and rescue of a molecular clone of Deformed wing virus (DWV). PLoS ONE. 2016;11:e0164639.38.Gusachenko ON, Woodford L, Balbirnie-Cumming K, Ryabov EV, Evans DJ. Evidence for and against deformed wing virus spillover from honey bees to bumble bees: a reverse genetic analysis. Sci Rep. 2020;10:16847.CAS 
PubMed 
PubMed Central 

Google Scholar 
39.Routh A, Johnson JE. Discovery of functional genomic motifs in viruses with ViReMa – a Virus Recombination Mapper – for analysis of next-generation sequencing data. Nucleic Acids Res. 2014;42:e11.CAS 
PubMed 

Google Scholar 
40.Ryabov EV, Christmon K, Heerman MC, Posada-Florez F, Harrison RL, Chen Y, et al. Development of a honey bee RNA virus vector based on the genome of a Deformed wing virus. Viruses. 2020;12:374.CAS 
PubMed Central 

Google Scholar 
41.Mueller S, Wimmer E. Expression of foreign proteins by poliovirus polyprotein fusion: analysis of genetic stability reveals rapid deletions and formation of cardioviruslike open reading frames. J Virol. 1998;72:20–31.CAS 
PubMed 
PubMed Central 

Google Scholar 
42.Kirkegaard K, Baltimore D. The mechanism of RNA recombination in poliovirus. Cell. 1986;47:433–43.CAS 
PubMed 
PubMed Central 

Google Scholar 
43.Egger D, Bienz K. Recombination of poliovirus RNA proceeds in mixed replication complexes originating from distinct replication start sites. J Virol. 2002;76:10960–71.CAS 
PubMed 
PubMed Central 

Google Scholar 
44.Lowry K, Woodman A, Cook J, Evans DJ. Recombination in enteroviruses is a biphasic replicative process involving the generation of greater-than genome length ‘imprecise’ Intermediates. PLoS Pathog. 2014;10; https://doi.org/10.1371/journal.ppat.1004191.45.de Miranda JR, Fries I. Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). J Invertebr Pathol. 2008;98:184–9.PubMed 

Google Scholar 
46.Yañez O, Jaffé R, Jarosch A, Fries I, Robin FAM, Robert JP, et al. Deformed wing virus and drone mating flights in the honey bee (Apis mellifera): Implications for sexual transmission of a major honey bee virus. Apidologie. 2012;43:17–30.
Google Scholar 
47.Simon KO, Cardamone JJ Jr, Whitaker-Dowling PA, Youngner JS, Widnell CC. Cellular mechanisms in the superinfection exclusion of vesicular stomatitis virus. Virology. 1990;177:375–9.CAS 
PubMed 

Google Scholar 
48.Stevenson M, Meier C, Mann AM, Chapman N, Wasiak A. Envelope glycoprotein of HIV induces interference and cytolysis resistance in CD4+ cells: mechanism for persistence in AIDS. Cell. 1988;53:483–96.CAS 
PubMed 

Google Scholar 
49.Bratt MA, Rubin H.Specific interference among strains of Newcastle disease virus. II. Comparison of interference by active and inactive virus.Virology. 1968;35:381–94.CAS 
PubMed 

Google Scholar 
50.Zou G, Zhang B, Lim P-Y, Yuan Z, Bernard KA, Shi P-Y. Exclusion of West Nile virus superinfection through RNA replication. J Virol. 2009;83:11765–76.CAS 
PubMed 
PubMed Central 

Google Scholar 
51.Ziebell H, Carr JP. Cross-protection: a century of mystery. Adv Virus Res. 2010;76:211–64.CAS 
PubMed 

Google Scholar 
52.Folimonova SY. Developing an understanding of cross-protection by Citrus tristeza virus. Front Microbiol. 2013;4; https://doi.org/10.3389/fmicb.2013.00076.53.Gisder S, Genersch E. Direct evidence for infection of mites with the bee-pathogenic Deformed wing virus variant B – but not variant A – via fluorescence-hybridization analysis. J Virol. 2021;95:e01786–20.CAS 

Google Scholar 
54.Posada-Florez F, Childers AK, Heerman MC, Egekwu NI, Cook SC, Chen Y, et al. Deformed wing virus type A, a major honey bee pathogen, is vectored by the mite Varroa destructor in a non-propagative manner. Sci Rep. 2019;9:12445.PubMed 
PubMed Central 

Google Scholar 
55.Barr JN, Fearns R. How RNA viruses maintain their genome integrity. J Gen Virol. 2010;91:1373–87.CAS 
PubMed 

Google Scholar 
56.Bentley K, Evans DJ. Mechanisms and consequences of positive-strand RNA virus recombination. J Gen Virol. 2018;99:1345–56.CAS 
PubMed 

Google Scholar 
57.Muslin C, Mac Kain A, Bessaud M, Blondel B, Delpeyroux F. Recombination in enteroviruses, a multi-step modular evolutionary process. Viruses. 2019;11:859.CAS 
PubMed Central 

Google Scholar 
58.Alnaji FG, Bentley K, Pearson A, Woodman A, Moore JD, Fox H, et al. Recombination in enteroviruses is a ubiquitous event independent of sequence homology and RNA structure. 2020; preprint at bioRxiv; https://doi.org/10.1101/2020.09.29.319285.59.Brutscher LM, Flenniken ML. RNAi and antiviral defense in the honey bee. J Immunol Res. 2015;2015:941897.PubMed 
PubMed Central 

Google Scholar 
60.Chejanovsky N, Ophir R, Schwager MS, Slabezki Y, Grossman S, Cox-Foster D. Characterization of viral siRNA populations in honey bee colony collapse disorder. Virology. 2014;454-5:176–83.
Google Scholar 
61.Desai SD, Eu YJ, Whyard S, Currie RW. Reduction in deformed wing virus infection in larval and adult honey bees (Apis mellifera L.) by double-stranded RNA ingestion. Insect Mol Biol. 2012;21:446–55.CAS 
PubMed 

Google Scholar 
62.Hunter W, Ellis J, Vanengelsdorp D, Hayes J, Westervelt D, Glick E, et al. Large-scale field application of RNAi technology reducing Israeli acute paralysis virus disease in honey bees (Apis mellifera, hymenoptera: Apidae). PLoS Pathog. 2010;6:e1001160.PubMed 
PubMed Central 

Google Scholar 
63.Maori E, Paldi N, Shafir S, Kalev H, Tsur E, Glick E, et al. IAPV, a bee-affecting virus associated with colony collapse disorder can be silenced by dsRNA ingestion. Insect Mol Biol. 2009;18:55–60.CAS 
PubMed 

Google Scholar  More

1.Evans, D. L. & Schmidt, J. O. Insect Defenses: Adaptive Mechanisms and Strategies of Prey and Predators (State University of New York Press, Albany, 1990).
Google Scholar 
2.Callow, L. L. Sawfly poisoning in cattle. Queensl. Agric. J. 81, 155–161 (1955).
Google Scholar 
3.Oelrichs, P. B., MacLeod, J. K. & Williams, D. H. Lophyrotomin a new hepatotoxic octapeptide from sawfly larvae Lophyrotoma interrupta. Toxicon 21(Suppl.3), 321–323 (1983).Article 

Google Scholar 
4.Oelrichs, P. B. et al. Unique toxic peptides isolated from sawfly larvae in three continents. Toxicon 37, 537–544 (1999).CAS 
PubMed 
Article 

Google Scholar 
5.Dutra, F., Riet-Correa, F., Mendez, M. C. & Paiva, N. Poisoning of cattle and sheep in Uruguay by sawfly (Perreyia flavipes) larvae. Vet. Hum. Toxicol. 39, 281–286 (1997).CAS 
PubMed 

Google Scholar 
6.Kannan, R., Oelrichs, P. B., Thamsborg, S. M. & Williams, D. H. Identification of the octapeptide lophyrotomin in the European birch sawfly (Arge pullata). Toxicon 26, 224–226 (1988).CAS 
PubMed 
Article 

Google Scholar 
7.Tessele, B., Brum, J. S., Schild, A. L., Soares, M. P. & Barros, C. S. L. Sawfly larval poisoning in cattle: Report on new outbreaks and brief review of the literature. Pesqui. Vet. Bras. 32, 1095–1102 (2012).Article 

Google Scholar 
8.Wouters, A. T. B. et al. Brain lesions associated with acute toxic hepatopathy in cattle. J. Vet. Diagn. Investig. 29, 287–292 (2017).Article 

Google Scholar 
9.Boevé, J.-L., Rozenberg, R., Shinohara, A. & Schmidt, S. Toxic peptides occur frequently in pergid and argid sawfly larvae. PLoS One 9(8), e105301 (2014).PubMed 
PubMed Central 
Article 
ADS 
CAS 

Google Scholar 
10.Boevé, J.-L., Nyman, T., Shinohara, A. & Schmidt, S. Endogenous toxins and the coupling of gregariousness to conspicuousness in Argidae and Pergidae sawflies. Sci. Rep. 8, 17636 (2018).PubMed 
PubMed Central 
Article 
ADS 
CAS 

Google Scholar 
11.Boevé, J.-L. & Rozenberg, R. Body distribution of toxic peptides in larvae of a pergid and an argid sawfly species. Sci. Nat. 107, 1 (2020).Article 
CAS 

Google Scholar 
12.Maxwell, D. E. The comparative internal larval anatomy of sawflies (Hymenoptera: Symphyta). Can. Entomol. 87, 1–132 (1955).Article 

Google Scholar 
13.Morrow, P. A., Bellas, T. E. & Eisner, T. Eucalyptus oils in the defensive oral discharge of Australian sawfly larvae (Hymenoptera: Pergidae). Oecologia 24, 193–206 (1976).CAS 
PubMed 
Article 
ADS 

Google Scholar 
14.Schmidt, S., McKinnon, A. E., Moore, C. J. & Walter, G. H. Chemical detoxification vs mechanical removal of host plant toxins in Eucalyptus feeding sawfly larvae (Hymenoptera: Pergidae). J. Insect Physiol. 56, 1770–1776 (2010).CAS 
PubMed 
Article 

Google Scholar 
15.Lorenz, H. & Kraus, M. Die Larvalsystematik der Blattwespen (Tenthredinoidea und Megalodontoidea) (Akademie-Verlag, Berlin, 1957).
Google Scholar 
16.Schmidt, S., Walter, G. H., Grigg, J. & Moore, C. J. Sexual communication and host plant associations of Australian pergid sawflies (Hymenoptera: Symphyta: Pergidae). In Recent Sawfly Research: Synthesis and Prospects (eds Blank, S. M. et al.) 173–193 (Goecke & Evers, Krefeld, 2006).
Google Scholar 
17.Petre, C.-A., Detrain, C. & Boevé, J.-L. Anti-predator defence mechanisms in sawfly larvae of Arge (Hymenoptera, Argidae). J. Insect Physiol. 53, 668–675 (2007).CAS 
PubMed 
Article 

Google Scholar 
18.Boevé, J.-L., Marín-Armijos, D. S., Domínguez, D. F. & Smith, D. R. Sawflies (Hymenoptera: Argidae, Pergidae, Tenthredinidae) from southern Ecuador, with a new record for the country and some ecological data. J. Hymenopt. Res. 51, 55–89 (2016).Article 

Google Scholar 
19.Shinohara, A., Hara, H. & Kim, J. The species-group of Arge captiva (Insecta, Hymenoptera, Argidae). Bull. Natl. Museum Nat. Sci. Ser. A (Zoology) Tokyo 35, 249–278 (2009).
Google Scholar 
20.Hara, H. & Shinohara, A. Arge enkianthus n. sp. (Hymenoptera, Argidae) feeding on Enkianthus campanulatus in Japan. Bull. Natl. Museum Nat. Sci. Ser. A (Zoology) Tokyo 38, 21–32 (2012).
Google Scholar 
21.Shinohara, A., Kojima, H. & Hara, H. New host plant records and life history notes on Spinarge flavicostalis (Hymenoptera: Argidae) in Japan. Bull. Natl. Museum Nat. Sci. Ser. A (Zoology) Tokyo 39, 185–191 (2013).
Google Scholar 
22.Ruxton, G. D., Sherratt, T. N. & Speed, M. P. Avoiding Attack. The Evolutionary Ecology of Crypsis, Warning Signals, and Mimicry (Oxford University Press, Oxford, 2004).Book 

Google Scholar 
23.Boevé, J.-L., Blank, S. M., Meijer, G. & Nyman, T. Invertebrate and avian predators as drivers of chemical defensive strategies in tenthredinid sawflies. BMC Evol. Biol. 13, 198 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
24.Benson, R. B. An introduction to the natural history of British sawflies. Trans. Soc. Br. Entomol. 10, 45–142 (1950).
Google Scholar 
25.Codella, S. G. & Raffa, K. F. Defense strategies of folivorous sawflies. In Sawfly Life History Adaptations to Woody Plants (eds Wagner, M. & Raffa, K. F.) 261–294 (Academic Press, Cambridge, 1993).
Google Scholar 
26.Schwerdtfeger, F. Untersuchungen über die Wirkung von Ameisen-Ansiedlungen auf die Dichte der Kleinen Fichtenblattwespe. Z. Angew. Entomol. 66, 187–206 (1970).
Google Scholar 
27.Woodman, R. L. & Price, P. W. Differential larval predation by ants can influence willow sawfly community structure. Ecology 73, 1028–1037 (1992).Article 

Google Scholar 
28.Boevé, J.-L. & Schaffner, U. Why does the larval integument of some sawfly species disrupt so easily? The harmful hemolymph hypothesis. Oecologia 134, 104–111 (2003).PubMed 
Article 
ADS 

Google Scholar 
29.Dettner, K. Toxins, defensive compounds and drugs from insects. In Insect Molecular Biology and Ecology (ed. Hoffmann, K. H.) 39–93 (Taylor & Francis, Boca Raton, 2015).
Google Scholar 
30.Taeger, A., Blank, S. M. & Liston, A. D. World Catalog of Symphyta (Hymenoptera). Zootaxa 2580, 1–1064 (2010).Article 

Google Scholar 
31.Boevé, J.-L. & Rozenberg, R. Berberis sawfly contains toxic peptides not only at larval stage. Sci. Nat. 106, 14 (2019).Article 
CAS 

Google Scholar 
32.Schoenly, K. The predators of insects. Ecol. Entomol. 15, 333–345 (1990).Article 

Google Scholar 
33.Way, M. J. & Khoo, K. C. Role of ants in pest managment. Annu. Rev. Entomol. 37, 479–503 (1992).Article 

Google Scholar 
34.Dyer, L. A. A quantification of predation rates, indirect positive effects on plants, and foraging variation of the giant tropical ant, Paraponera clavata. J. Insect Sci. 2, 18 (2002).PubMed 
PubMed Central 
Article 

Google Scholar 
35.Jervis, M. & Kidd, N. Insect Natural Enemies. Practical Approaches to their Study and Evaluation (Chapman & Hall, London, 1996).Book 

Google Scholar 
36.Philpott, S. M., Greenberg, R., Bichier, P. & Perfecto, I. Impacts of major predators on tropical agroforest arthropods: Comparisons within and across taxa. Oecologia 140, 140–149 (2004).PubMed 
Article 
ADS 

Google Scholar 
37.Rosumek, F. B. et al. Ants on plants: A meta-analysis of the role of ants as plant biotic defenses. Oecologia 160, 537–549 (2009).PubMed 
Article 
ADS 
PubMed Central 

Google Scholar 
38.Fittkau, E. J. & Klinge, H. On biomass and trophic structure of the Central Amazonian rain forest ecosystem. Biotropica 5, 2–14 (1973).Article 

Google Scholar 
39.Hölldobler, B. & Wilson, E. O. The Ants (Harvard University Press, Harvard, 1990).Book 

Google Scholar 
40.Ryder Wilkie, K. T., Mertl, A. L. & Traniello, J. F. A. Species diversity and distribution patterns of the ants of Amazonian Ecuador. PLoS One 5, e13146 (2010).PubMed 
PubMed Central 
Article 
ADS 
CAS 

Google Scholar 
41.Wills, B. D. & Landis, D. A. The role of ants in north temperate grasslands: A review. Oecologia 186, 323–338 (2018).CAS 
PubMed 
Article 
ADS 

Google Scholar 
42.Pasteels, J. M., Grégoire, J.-C. & Rowell-Rahier, M. The chemical ecology of defense in arthropods. Annu. Rev. Entomol. 28, 263–289 (1983).CAS 
Article 

Google Scholar 
43.Whitman, D. W., Blum, M. R. & Alsop, D. W. Allomones: Chemicals for defense. In Insect Defenses: Adaptive Mechanisms and Strategies of Prey and Predators (eds Evans, D. L. & Schmidt, J. O.) 289–351 (State University of New York Press, Albany, 1990).
Google Scholar 
44.Eisner, T., Eisner, M. & Siegler, M. Secret Weapons: Defenses of Insects, Spiders, Scorpions, and other Many-Legged Creatures (Harvard University Press, Harvard, 2005).
Google Scholar 
45.Morton, T. C. & Vencl, F. V. Larval beetles form a defense from recycled host-plant chemicals discharged as fecal wastes. J. Chem. Ecol. 24, 765–785 (1998).CAS 
Article 

Google Scholar 
46.Zhang, S. et al. A novel property of spider silk: Chemical defence against ants. Proc. R. Soc. B Biol. Sci. 279, 1824–1830 (2011).Article 
CAS 

Google Scholar 
47.Hilker, M. Protective devices of early developmental stages in Pyrrhalta viburni (Coleoptera, Chrysomelidae). Oecologia 92, 71–75 (1992).PubMed 
Article 
ADS 
PubMed Central 

Google Scholar 
48.Gross, J., Eben, A., Müller, I. & Wensing, A. A well protected intruder: The effective antimicrobial defense of the invasive ladybird Harmonia axyridis. J. Chem. Ecol. 36, 1180–1188 (2010).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
49.Gentry, G. L. & Dyer, L. A. On the conditional nature of Neotropical caterpillar defenses against their natural enemies. Ecology 83, 3108–3119 (2009).Article 

Google Scholar 
50.Rojas, B. et al. How to fight multiple enemies: Target-specific chemical defences in an aposematic moth. Proc. R. Soc. B Biol. Sci. 284, 20171424 (2017).Article 

Google Scholar 
51.Boevé, J.-L. & Pasteels, J. M. Modes of defense in nematine sawfly larvae. Efficiency against ants and birds. J. Chem. Ecol. 11, 1019–1036 (1985).PubMed 
Article 

Google Scholar 
52.Schaffner, U., Boevé, J.-L., Gfeller, H. & Schlunegger, U. P. Sequestration of Veratrum alkaloids by specialist Rhadinoceraea nodicornis Konow (Hymenoptera, Tenthredinidae) and its ecoethological implications. J. Chem. Ecol. 20, 3233–3250 (1994).CAS 
PubMed 
Article 

Google Scholar 
53.Boevé, J.-L. Some sawfly larvae survive predator-prey interactions with pentatomid Picromerus bidens. Sci. Nat. 108, 8 (2021).Article 
CAS 

Google Scholar 
54.Remmel, T., Davison, J. & Tammaru, T. Quantifying predation on folivorous insect larvae: The perspective of life-history evolution. Biol. J. Linn. Soc. 104, 1–18 (2011).Article 

Google Scholar 
55.Verhaagh, M. „Parasitierung” einer Ameisen-Pflanzen-Symbiose in neotropischen Regenwald? Carolinea 46, 150 (1988).
Google Scholar 
56.Boevé, J.-L. & Heilporn, S. Secretion of the ventral glands in Craesus sawfly larvae. Biochem. Syst. Ecol. 36, 836–841 (2008).Article 
CAS 

Google Scholar 
57.Aili, S. R. et al. Diversity of peptide toxins from stinging ant venoms. Toxicon 92, 166–178 (2014).CAS 
PubMed 
Article 

Google Scholar 
58.Boevé, J.-L. & Müller, C. Defence effectiveness of easy bleeding sawfly larvae towards invertebrate and avian predators. Chemoecology 15, 51–58 (2005).Article 
CAS 

Google Scholar 
59.Chevin, H. Notes sur les Hyménoptères Tenthredoides. 2. Identification des larves d’Arge pagana (Panz.) et d’Arge ochropa (Gmel.). Bull. Mens. la Société Linnéenne Lyon 1, 2–5 (1972).Article 

Google Scholar 
60.Schmidt, S. & Smith, D. R. Pergidae of the World – An online catalogue of the sawfly family Pergidae (Insecta, Hymenoptera, Symphyta). World Wide Web electronic publication (2018). Available at: http://pergidae.snsb-zsm.de. (Accessed: 25th July 2016)61.Olofsson, E. Predation by Formica polyctena Förster (Hym., Formicidae) on newly emerged larvae of Neodiprion sertifer (Geoffroy) (Hym., Diprionidae). J. Appl. Entomol. 114, 315–319 (1992).Article 

Google Scholar 
62.Hughes, L., Westoby, M. & Jurado, E. Convergence of elaiosomes and insect prey: Evidence from ant foraging behaviour and fatty acid composition. Funct. Ecol. 8, 358–365 (1994).Article 

Google Scholar  More

Andersson M (2006) Condition-dependent indicators in sexual selection: development of theory and tests. In: Lucas JR, Simmons LW (eds) Essays in Animal Behaviour: Celebrating 50 Years of Animal Behaviour. Elsevier Academic Press, p 255–269.Badyaev AV, Hill GE (2000) Evolution of sexual dichromatism: contribution of carotenoid- versus melanin-based colouration. Biol J Linn Soc 69:153–172Article 

Google Scholar 
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48Article 

Google Scholar 
Bednekoff PA, Houston AI (1994) Avian daily foraging patterns: effects of digestive constraints and variability. Evol Ecol 8:36–52Article 

Google Scholar 
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57:289–300.Bonduriansky R, Rowe L (2005) Sexual selection, genetic architecture, and the condition dependence of body shape in the sexually dimorphic fly Prochyliza xanthostoma (Piophilidae). Evolution 59:138–151PubMed 
Article 
PubMed Central 

Google Scholar 
Brooks R, Kemp DJ (2001) Can older males deliver the good genes? TREE 16:308–313CAS 
PubMed 
PubMed Central 

Google Scholar 
Butler D (2009) ASReml R package version 3.0. VSN International Ltd, Hemel Hempstead, UK
Google Scholar 
Cassey P, Ewen J, Blackburn T, Hauber M, Vorobyev M, Marshall N (2008) Eggshell colour does not predict measures of maternal investment in eggs of Turdus thrushes. Naturwissenschaften 95:713–721CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
Charmantier A, Wolak ME, Grégoire A, Fargevieille A, Doutrelant C (2017) Colour ornamentation in the blue tit: quantitative genetic (co) variances across sexes. Heredity 118:125CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
Class B, Kluen E, Brommer JE (2019) Tail colour signals performance in blue tit nestlings. J Evol Biol 32:913–920PubMed 
Article 
PubMed Central 

Google Scholar 
Cotton S, Fowler K, Pomiankowski A (2004) Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc R Soc Lond B Biol Sci 271:771–783Article 

Google Scholar 
Cuthill IC (2006) Color perception. In: Hill GE, McGraw KJ (eds) Bird coloration, Vol. 1. Harvard University Press, p 3–40.D’Alba L, Van Hemert C, Spencer KA, Heidinger BJ, Gill L, Evans NP et al. (2014) Melanin-based color of plumage: role of condition and of feathers’ microstructure. Integr Comp Biol 54:633–644PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
Dale J, Dey CJ, Delhey K, Kempenaers B, Valcu M (2015) The effects of life history and sexual selection on male and female plumage colouration. Nature 527:367–370CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
Darwin C (1871) The Descent of Man and Selection in Relation to Sex. Princeton University Press.Delhey K, Burger C, Fiedler W, Peters A (2010) Seasonal changes in colour: a comparison of structural, melanin-and carotenoid-based plumage colours. PLoS ONE 5:e11582PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Delhey K, Delhey V, Kempenaers B, Peters A (2015) A practical framework to analyze variation in animal colors using visual models. Behav Ecol 26:367–375Article 

Google Scholar 
Delhey K, Hall ML, Kingma SA, Peters A (2013) Increased conspicuousness can explain the match between visual sensitivities and blue plumage colours in fairy-wrens. Proc R Soc Lond B Biol Sci 284:20121771
Google Scholar 
Delhey K, Peters A (2008) Quantifying variability of avian colours: Are signalling traits more variable? PLoS ONE 3:e1689.Delhey K, Szecsenyi B, Nakagawa S, Peters A (2017) Conspicuous plumage colours are highly variable. Proc R Soc Lond B Biol Sci 284:20162593
Google Scholar 
Dobson AE, Schmidt DJ, Hughes JM (2019) Heritability of plumage colour morph variation in a wild population of promiscuous, long-lived Australian magpies. Heredity 123:349–358PubMed 
PubMed Central 
Article 

Google Scholar 
Dunn PO, Whittingham LA, Pitcher TE (2001) Mating systems, sperm competition, and the evolution of sexual dimorphism in birds. Evolution 55:161–175CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
Endler JA, Mielke PW (2005) Comparing entire colour patterns as birds see them. Biol J Linn Soc 86:405–431Article 

Google Scholar 
Endler JA, Westcott DA, Madden JR, Robson T (2005) Animal visual systems and the evolution of color patterns: sensory processing illuminates signal evolution. Evolution 59:1795–1818PubMed 
Article 
PubMed Central 

Google Scholar 
Evans MR, Barnard P (1995) Variable sexual ornaments in scarlet-tufted malachite sunbirds (Nectarinia johnstoni) on Mount Kenya. Biol J Linn Soc 54:371–381Article 

Google Scholar 
Evans SR, Sheldon BC (2012) Quantitative genetics of a carotenoid-based color: heritability and persistent natal environmental effects in the great tit. Am Nat 179:79–94PubMed 
Article 
PubMed Central 

Google Scholar 
Fan M, D’Alba L, Shawkey MD, Peters A, Delhey K (2019) Multiple components of feather microstructure contribute to structural plumage colour diversity in fairy-wrens. Biol J Linn Soc 128:550–568Article 

Google Scholar 
Fan M, Hall ML, Kingma SA, Mandeltort LM, Hidalgo Aranzamendi N, Delhey K et al. (2017) No fitness benefits of early molt in a fairy-wren: relaxed sexual selection under genetic monogamy? Behav Ecol 28:1055–1067Article 

Google Scholar 
Fan M, Teunissen N, Hall ML, Hidalgo Aranzamendi N, Kingma SA, Roast M et al. (2018) From ornament to armament or loss of function? Breeding plumage acquisition in a genetically monogamous bird. J Anim Ecol 87:1274–1285PubMed 
Article 
PubMed Central 

Google Scholar 
Garant D, Sheldon BC, Gustafsson L (2004) Climatic and temporal effects on the expression of secondary sexual characters: genetic and environmental components. Evolution 58:634–644PubMed 
Article 
PubMed Central 

Google Scholar 
Gosden TP, Chenoweth SF (2011) On the evolution of heightened condition dependence of male sexual displays. J Evol Biol 24:685–692CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
Guilford T, Dawkins MS (1991) Receiver psychology and the evolution of animal signals. Anim Behav 42:1–14Article 

Google Scholar 
Guindre‐Parker S, Love OP (2014) Revisiting the condition‐dependence of melanin‐based plumage. J Avian Biol 45:29–33Article 

Google Scholar 
Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22Article 

Google Scholar 
Hadfield JD, Burgess MD, Lord A, Phillimore AB, Clegg SM, Owens IP (2006) Direct versus indirect sexual selection: genetic basis of colour, size and recruitment in a wild bird. Proc R Soc Lond B Biol Sci 273:1347–1353
Google Scholar 
Hadfield JD, Nutall A, Osorio D, Owens IPF (2007) Testing the phenotypic gambit: phenotypic, genetic and environmental correlations of colour. J Evol Biol 20:549–557CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
Hall ML, Kingma SA, Peters A (2013) Male songbird indicates body size with low-pitched advertising songs. PLoS ONE 8:e56717CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Hall ML, Peters A (2009) Do male paternity guards ensure female fidelity in a duetting fairy-wren? Behav Ecol 20:222–228Article 

Google Scholar 
Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
Hart NS (2001) Variations in cone photoreceptor abundance and the visual ecology of birds. J Comp Physiol A 187:685–697CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
Hart NS, Hunt DM (2007) Avian visual pigments: characteristics, spectral tuning, and evolution. Am Nat 169(S1):S7–S26PubMed 
Article 
PubMed Central 

Google Scholar 
Hawkins GL, Hill GE, Mercadante A (2012) Delayed plumage maturation and delayed reproductive investment in birds. Biol Rev 87:257–274PubMed 
Article 
PubMed Central 

Google Scholar 
Hegyi G, Szigeti B, Török J, Eens M (2007) Melanin, carotenoid and structural plumage ornaments: information content and role in great tits Parus major. J Avian Biol 38:698–708Article 

Google Scholar 
Hidalgo Aranzamendi N (2017) Life-history variation in a tropical cooperative bird: ecological and social effects on productivity. PhD Thesis, Monash University.Hidalgo Aranzamendi N, Hall ML, Kingma SA, Sunnucks P, Peters A (2016) Incest avoidance, extrapair paternity, and territory quality drive divorce in a year-round territorial bird. Behav Ecol 27:1808–1819.Hidalgo Aranzamendi N, Hall ML, Kingma SA, van de Pol M, Peters A (2019) Rapid plastic breeding response to rain matches peak prey abundance in a tropical savanna bird. J Anim Ecol 88:1799–1811PubMed 
Article 
PubMed Central 

Google Scholar 
Hill GE (2006) Environmental regulation of ornamental coloration. In: Hill GE, McGraw KJ (eds) Bird coloration, Vol. 1. Harvard University Press. p 507–560.Hill GE, Brawner WR (1998) Melanin-based plumage colouration in the house finch is unaffected by coccidial infection. Proc R Soc Lond B Biol Sci 265:1105–1109Article 

Google Scholar 
Johnstone RA, Rands SA, Evans MR (2009) Sexual selection and condition‐dependence. J Evol Biol 22:2387–2394CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
Kappers EF, de Vries C, Alberda A, Forstmeier W, Both C, Kempenaers B (2018) Inheritance patterns of plumage coloration in common buzzards Buteo buteo do not support a one-locus two-allele model. Biol Lett 14:20180007PubMed 
PubMed Central 
Article 

Google Scholar 
Kemp DJ, Rutowski RL (2007) Condition dependence, quantitative genetics, and the potential signal content of iridescent ultraviolet butterfly coloration. Evolution 61:168–183PubMed 
Article 
PubMed Central 

Google Scholar 
Kendeigh SC, Kontogiannis JE, Mazac A, Roth RR (1969) Environmental regulation of food intake by birds. Comp Biochem Physiol 31:941–957Article 

Google Scholar 
Keyser AJ, Hill GE (2000) Structurally based plumage coloration is an honest signal of quality in male blue grosbeaks. Behav Ecol 11:202–209Article 

Google Scholar 
Kingma SA, Hall ML, Arriero E, Peters A (2010) Multiple benefits of cooperative breeding in purple-crowned fairy-wrens: a consequence of fidelity? J Anim Ecol 79:757–768PubMed 
PubMed Central 

Google Scholar 
Kingma SA, Hall ML, Peters A (2011) No evidence for offspring sex-ratio adjustment to social or environmental conditions in cooperatively breeding purple-crowned fairy-wrens. Behav Ecol Sociobiol 65:1203–1213Article 

Google Scholar 
Kingma SA, Hall ML, Segelbacher G, Peters A (2009) Radical loss of an extreme extra-pair mating system. BMC Ecol 9:15PubMed 
PubMed Central 
Article 

Google Scholar 
Kokko H (1997) Evolutionarily stable strategies of age-dependent sexual advertisement. Behav Ecol Sociobiol 41:99–107Article 

Google Scholar 
Kuznetsova A, Brockhoff PB, Christensen RHB (2015) Package ‘lmerTest’ R version 20–33.Lantz SM, Karubian J (2016) Male Red-backed Fairywrens appear to enhance a plumage-based signal via adventitious molt. The Auk 133:338–346Article 

Google Scholar 
Lind O, Chavez J, Kelber A (2014) The contribution of single and double cones to spectral sensitivity in budgerigars during changing light conditions. J Comp Physiol A 200:197–207Article 

Google Scholar 
Lind O, Henze MJ, Kelber A, Osorio D (2017) Coevolution of coloration and colour vision? Philos Trans R Soc Lond B Biol Sci 372:20160338PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Lindström Å, Visser GH, Daan S (1993) The energetic cost of feather synthesis is proportional to basal metabolic rate. Physiol Zool 66:490–510Article 

Google Scholar 
Manning JT (1985) Choosy females and correlates of male age. J Theor Biol 116:349–354Article 

Google Scholar 
Masello JF, Lubjuhn T, Quillfeldt P (2008) Is the structural and psittacofulvin-based coloration of wild burrowing parrots Cyanoliseus patagonus condition dependent? J Avian Biol 39:653–662Article 

Google Scholar 
McGraw KJ (2006) Mechanics of melanin coloration in birds. In: Hill GE, McGraw KJ (eds) Bird coloration, Vol. 1. Harvard University Press. p 243–294.McGraw KJ, Mackillop EA, Dale J, Hauber ME (2002) Different colors reveal different information: how nutritional stress affects the expression of melanin- and structurally based ornamental plumage. J Exp Biol 205:3747–3755PubMed 
Article 
PubMed Central 

Google Scholar 
McGraw KJ, Safran RJ, Wakamatsu K (2005) How feather colour reflects its melanin content. Funct Ecol 19:816–821Article 

Google Scholar 
McQueen A, Delhey K, Barzan FR, Naimo AC, Peters A (2021) Male fairy-wrens produce and maintain vibrant breeding colors irrespective of individual quality. Behav Ecol 32:178–187Article 

Google Scholar 
Merilä J, Sheldon BC (1999) Genetic architecture of fitness and nonfitness traits: empirical patterns and development of ideas. Heredity 83:103–109PubMed 
Article 
PubMed Central 

Google Scholar 
Meunier J, Pinto SF, Burri R, Roulin A (2011) Eumelanin-based coloration and fitness parameters in birds: a meta-analysis. Behav Ecol Sociobiol 65:559–567Article 

Google Scholar 
Ödeen A, Pruett-Jones S, Driskell AC, Armenta JK, Håstad O (2012) Multiple shifts between violet and ultraviolet vision in a family of passerine birds with associated changes in plumage coloration. Proc R Soc Lond B Biol Sci 279:1269–1276
Google Scholar 
Olsson P, Lind O, Kelber A (2017) Chromatic and achromatic vision: parameter choice and limitations for reliable model predictions. Behav Ecol 29:273–282Article 

Google Scholar 
Owens IPF, Hartley IR (1998) Sexual dimorphism in birds: why are there so many different forms of dimorphism? Proc R Soc Lond B Biol Sci 265:397–407Article 

Google Scholar 
Peters A, Delhey K, Andersson S, Van Noordwijk H, Förschler MI (2008) Condition‐dependence of multiple carotenoid‐based plumage traits: an experimental study. Funct Ecol 22:831–839Article 

Google Scholar 
Peters A, Kingma SA, Delhey K (2013) Seasonal male plumage as a multi-component sexual signal: Insights and opportunities. Emu 113:232–247Article 

Google Scholar 
Peters A, Kurvers RHJM, Roberts ML, Delhey K (2011) No evidence for general condition-dependence of structural plumage colour in blue tits: an experiment. J Evol Biol 24:976–987CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
Pomiankowski A, Møller AP (1995) A resolution of the lek paradox. Proc R Soc Lond B Biol Sci 260:21–29Article 

Google Scholar 
Price T, Schluter D (1991) On the low heritability of life‐history traits. Evolution 45:853–861PubMed 
Article 
PubMed Central 

Google Scholar 
Proulx SR, Day T, Rowe L (2002) Older males signal more reliably. Proc R Soc Lond B Biol Sci 269:2291–2299Article 

Google Scholar 
Prum RO (2006) Anatomy, physics, and evolution of structural colours. In: Hill GE, McGraw KJ (eds) Bird coloration, Vol. 1. Harvard University Press. p 295–353.Prum RO (2010) The Lande–Kirkpatrick mechanism is the null model of evolution by intersexual selection: implications for meaning, honesty, and design in intersexual signals. Evolution 64:3085–3100PubMed 
Article 
PubMed Central 

Google Scholar 
R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/.Reinhold K (2011) Variation in acoustic signalling traits exhibits footprints of sexual selection. Evolution 65:738–745PubMed 
Article 
PubMed Central 

Google Scholar 
Renoult JP, Kelber A, Schaefer HM (2017) Colour spaces in ecology and evolutionary biology. Biol Rev 92:292–315PubMed 
Article 
PubMed Central 

Google Scholar 
Roast MJ, Aranzamendi NH, Fan M, Teunissen N, Hall MD, Peters A (2020) Fitness outcomes in relation to individual variation in constitutive innate immune function. Proc R Soc Lond B Biol Sci 287:20201997
Google Scholar 
Roulin A (2016) Condition‐dependence, pleiotropy and the handicap principle of sexual selection in melanin‐based colouration. Biol Rev 91:328–348PubMed 
Article 
PubMed Central 

Google Scholar 
Roulin A, Ducrest AL (2013) Seminars in cell and developmental biology, Vol 24, no 6–7. Academic Press. p 594–608.Rowe L, Houle D (1996) The lek paradox and the capture of genetic variance by condition dependent traits. Proc R Soc Lond B Biol Sci 263:1415–1421Article 

Google Scholar 
Rowley I, Russell E (1997) Fairy-wrens and Grasswrens: Maluridae. Oxford University Press.Taylor PD, Williams GC (1982) The lek paradox is not resolved. Theor Popul Biol 22:392–409Article 

Google Scholar 
Schodde R (1982) The Fairy-wrens: a monograph of the Maluridae. Lansdowne Editions.Shawkey MD, D’Alba L (2017) Interactions between colour-producing mechanisms and their effects on the integumentary colour palette. Philos Trans R Soc Lond B Biol Sci 372:20160536PubMed 
PubMed Central 
Article 

Google Scholar 
Tibbetts EA (2010) The condition dependence and heritability of signaling and nonsignaling color traits in paper wasps. Am Nat 175:495–503PubMed 
Article 
PubMed Central 

Google Scholar 
Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual Selection and the Descent of Man 1871–1971. Heinemann. p 136–179.Vorobyev M, Osorio D, Bennett AT, Marshall NJ, Cuthill IC (1998) Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol A 183:621–633CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
White TE (2020) Structural colours reflect individual quality: a meta-analysis. Biol Lett 16:20200001PubMed 
PubMed Central 
Article 

Google Scholar 
Wilson AJ, Reale D, Clements MN, Morrissey MM, Postma E, Walling CA et al. (2010) An ecologist’s guide to the animal model. J Anim Ecol 79:13–26PubMed 
Article 
PubMed Central 

Google Scholar  More

1.Shewry, P. R. Wheat. J. Exp. Bot. 60, 1537–1553 (2009).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
2.Shewry, P. R. & Hey, S. J. The contribution of wheat to human diet and health. Food Energy Secur. 4, 178–202 (2015).PubMed 
PubMed Central 
Article 

Google Scholar 
3.Shiferaw, B. et al. Crops that feed the world 10: Past successes and future challenges to the role played by wheat in global food security. Food Secur. 5, 291–317 (2013).Article 

Google Scholar 
4.Pickett, J. A. et al. Delivering sustainable crop protection systems via the seed: Exploiting natural constitutive and inducible defence pathways. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 369, 20120281 (2014).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
5.Dinant, S., Bonnemain, J. L., Girousse, C. & Kehr, J. Phloem sap intricacy and interplay with aphid feeding. C. R. Biol. 333, 504–515 (2010).PubMed 
Article 
PubMed Central 

Google Scholar 
6.Rabbinge, R., Drees, E. M., van der Graaf, M., Verberne, F. C. M. & Wesselo, A. Damage effects of cereal aphids in wheat. Netherlands J. Plant Pathol. 87, 217–232 (1981).Article 

Google Scholar 
7.Leather, S. R., Walters, K. F. A. & Dixon, A. F. G. Factors determining the pest status of the bird cherry-oat aphid, Rhopalosiphum padi (L.) (Hemiptera: Aphididae), in Europe: A study and review. Bull. Entomol. Res. 79, 345–360 (1989).Article 

Google Scholar 
8.Halbert, S. E., Connelly, J. B., Bishop, G. W. & Blackmer, J. L. Transmission of barley yellow dwarf virus by field collected aphids (Homoptera: Aphididae) and their relative importance in barley yellow dwarf epidemiology in southwestern Idaho. Ann. Appl. Biol. 121, 105–121 (1992).Article 

Google Scholar 
9.Chapin, J. W., Thomas, J. S., Gray, S. M., Smith, D. M. & Halbert, S. E. Seasonal abundance of aphids (Homoptera: Aphididae) in wheat and their role as barley yellow dwarf virus vectors in the South Carolina coastal plain. J. Econ. Entomol. 94, 410–421 (2001).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
10.Tanguy, S. & Dedryver, C. Reduced BYDV–PAV transmission by the grain aphid in a Triticum monococcum line. Eur. J. Plant Pathol. 123, 281–289 (2009).Article 

Google Scholar 
11.Yu, W. et al. Variation in the transmission of barley yellow dwarf virus-PAV by different Sitobion avenae clones in China. J. Virol. Methods 194, 1–6 (2013).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
12.Voss, T. S., Kieckhefer, R. W., Fuller, B. W., Mcleod, M. J. & Beck, D. A. Yield losses in maturing spring wheat caused by cereal aphids (Homoptera: Aphididae) under laboratory conditions. J. Econ. Entomol. 90, 1346–1350 (1997).Article 

Google Scholar 
13.Aradottir, G. I. & Crespo-Herrera, L. Host plant resistance in wheat to barley yellow dwarf viruses and their aphid vectors: A review. Curr. Opin. Insect Sci. 45, 59–68 (2021).PubMed 
Article 
PubMed Central 

Google Scholar 
14.Foster, S. P. et al. A mutation (L1014F) in the voltage-gated sodium channel of the grain aphid, Sitobion avenae, is associated with resistance to pyrethroid insecticides. Pest Manag. Sci. 70, 1249–1253 (2014).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
15.Carvalho, F. P. Agriculture, pesticides, food security and food safety. Environ. Sci. Policy 9, 685–692 (2006).Article 

Google Scholar 
16.Pickett, J. A. Food security: Intensification of agriculture is essential, for which current tools must be defended and new sustainable technologies invented. Food Energy Secur. 2, 167–173 (2013).Article 

Google Scholar 
17.Bezemer, T. M., Jones, T. H. & Knight, K. J. Long-term effects of elevated CO2 and temperature on populations of the peach potato aphid Myzus persicae and its parasitoid aphidius matricariae. Oecologia 116, 128–135 (1998).ADS 
PubMed 
Article 
PubMed Central 

Google Scholar 
18.Van Der Putten, W. H., Macel, M. & Visser, M. E. Predicting species distribution and abundance responses to climate change: Why it is essential to include biotic interactions across trophic levels. Philos. Trans. R. Soc. B. 365, 2025–2034 (2010).Article 

Google Scholar 
19.Thaler, J. S. Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399, 686–688 (1999).ADS 
CAS 
Article 

Google Scholar 
20.Agrawal, A. A. Macroevolution of plant defense strategies. Trends Ecol. Evol. 22, 103–109 (2007).PubMed 
Article 
PubMed Central 

Google Scholar 
21.Rasmann, S., Chassin, E., Bilat, J., Glauser, G. & Reymond, P. Trade-off between constitutive and inducible resistance against herbivores is only partially explained by gene expression and glucosinolate production. J. Exp. Bot. 66, 2527–2534 (2015).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
22.Turley, N. E. & Johnson, M. T. J. Ecological effects of aphid abundance, genotypic variation, and contemporary evolution on plants. Oecologia 178, 747–759 (2015).ADS 
PubMed 
Article 
PubMed Central 

Google Scholar 
23.Züst, T. & Agrawal, A. A. Mechanisms and evolution of plant resistance to aphids. Nat. Plants 2, 1–9 (2016).Article 
CAS 

Google Scholar 
24.Kogan, M. & Ortman, E. F. Antixenosis: A new term proposed to define painter’s ‘nonpreference’ modality of resistance. Bull. Entomol. Soc. Am. 24, 175–176 (1978).
Google Scholar 
25.Mumm, R. & Dicke, M. Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Can. J. Zool. 88, 628–667 (2010).CAS 
Article 

Google Scholar 
26.Stout, M. J. Reevaluating the conceptual framework for applied research on host-plant resistance. Insect Sci. 20, 263–272 (2013).PubMed 
Article 
PubMed Central 

Google Scholar 
27.Aradottir, G. I., Martin, J. L., Clark, S. J., Pickett, J. A. & Smart, L. E. Searching for wheat resistance to aphids and wheat bulb fly in the historical Watkins and Gediflux wheat collections. Ann. Appl. Biol. 170, 179–188 (2017).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
28.Singh, B. et al. Characterization of bird cherry-oat aphid (Rhopalosiphum padi L.) behaviour and aphid host preference in relation to partially resistant and susceptible wheat landraces. Ann. Appl. Biol. https://doi.org/10.1111/aab.12616 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
29.Radchenko, E. E. Resistance of Triticum species to cereal aphids. Czech J. Genet. Plant Breed. 47, 67–70 (2011).Article 

Google Scholar 
30.Sotherton, N. W. & Lee, G. Field assessments of resistance to the aphids Sitobion avenae and Metopolophium dirhodum in old and modern spring-sown wheats. Ann. Appl. Biol. 112, 239–248 (1988).Article 

Google Scholar 
31.Hu, X. S. et al. Resistance of wheat accessions to the English grain aphid Sitobion avenae. PLoS ONE 11, 1–17 (2016).
Google Scholar 
32.Salamini, F., Ozkan, H., Brandolini, A., Schäfer-Pregl, R. & Martin, W. Genetics and geography of wild cereal domestication in the near east. Nat. Rev. Genet. 3, 429–441 (2002).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
33.Greenslade, A. F. C. et al. Triticum monococcum lines with distinct metabolic phenotypes and phloem-based partial resistance to the bird cherry-oat aphid Rhopalosiphum padi. Ann. Appl. Biol. 168, 435–449 (2016).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
34.Spiller, N. J. & Llewellyn, M. A comparison of the level of resistance in diploid Triticum monococcum and hexaploid Triticum aestivum wheat seedlings to the aphids Metopolophium dirhodum and Rhopalosiphum padi. Ann. Appl. Biol. 109, 173–177 (1986).Article 

Google Scholar 
35.Migui, S. M. & Lamb, R. J. Patterns of resistance to three cereal aphids among wheats in the genus Triticum (Poaceae). Bull. Entomol. Res. 93, 323–333 (2003).PubMed 
Article 
PubMed Central 

Google Scholar 
36.Migui, S. M. & Lamb, R. J. Seedling and adult plant resistance to Sitobion avenae (Hemiptera: Aphididae) in Triticum monococcum (Poaceae), an ancestor of wheat. Bull. Entomol. Res. 94, 35–46 (2004).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
37.di Pietro, J. P., Caillaud, C. M., Chaubet, B., Pierre, J. S. & Trottet, M. Variation in resistance to the grain aphid, Sitobion avenae (Sternorhynca: Aphididae), among diploid wheat genotypes: Multivariate analysis of agronomic data. Plant Breed. 117, 407–413 (1998).Article 

Google Scholar 
38.Simon, A. L., Wellham, P. A. D., Aradottir, G. I. & Gange, A. C. Unravelling mycorrhiza-induced wheat susceptibility to the English grain aphid Sitobion avenae. Sci. Rep. 7, 1–11 (2017).CAS 
Article 

Google Scholar 
39.Rosenheim, J. A. Source-sink dynamics for a generalist insect predator in habitats with strong higher-order predation. Ecol. Monogr. 71, 93–116 (2001).
Google Scholar 
40.Pålsson, J. et al. Recruiting on the spot: A biodegradable formulation for lacewings to trigger biological control of aphids. Insects 10, 1–15 (2019).Article 

Google Scholar 
41.Mohamed, A. H., Lester, P. J. & Holtzer, T. O. Abundance and effects of predators and parasitoids on the Russian wheat aphid (Homoptera: Aphididae) under organic farming conditions in Colorado. Environ. Entomol. 29, 360–368 (2000).Article 

Google Scholar 
42.Schröder, M. L., Glinwood, R., Ingell, R. & Krüger, K. Visual cues and host-plant preference of the bird cherry-oat aphid, Rhopalosiphum padi (Hemiptera: Aphididae). Afr. Entomol. 22, 428–436 (2014).Article 

Google Scholar 
43.Weaver, D. K. et al. Cultivar preferences of ovipositing wheat stem sawflies as influenced by the amount of volatile attractant. J. Econ. Entomol. 102, 1009–1017 (2009).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
44.Dong, L. et al. Characterization of volatile aroma compounds in different brewing barley cultivars. J. Sci. Food Agric. 95, 915–921 (2015).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
45.Mattiolo, E., Licciardello, F., Lombardo, G. M., Muratore, G. & Anastasi, U. Volatile profiling of durum wheat kernels by HS–SPME/GC–MS. Eur. Food Res. Technol. 243, 147–155 (2017).CAS 
Article 

Google Scholar 
46.Schröder, M. L., Glinwood, R., Webster, B., Ignell, R. & Krüger, K. Olfactory responses of Rhopalosiphum padi to three maize, potato, and wheat cultivars and the selection of prospective crop border plants. Entomol. Exp. Appl. 157, 241–253 (2015).Article 
CAS 

Google Scholar 
47.Evans, E. W. & Youssef, N. N. Numerical responses of aphid predators to varying prey density among utah alfalfa fields. J. Kansas Entomol. Soc. 65, 30–38 (1992).
Google Scholar 
48.Garratt, M. P. D., Wright, D. J. & Leather, S. R. The effects of organic and conventional fertilizers on cereal aphids and their natural enemies. Agric. For. Entomol. 12, 307–318 (2010).
Google Scholar 
49.Messina, F. J. & Sorenson, S. M. Effectiveness of lacewing larvae in reducing Russian wheat aphid populations on susceptible and resistant wheat. Biol. Control 21, 19–26 (2001).Article 

Google Scholar 
50.Farid, A., Johnson, J. B., Shafii, B. & Quisenberry, S. S. Tritrophic studies of Russian wheat aphid, a parasitoid, and resistant and susceptible wheat over three parasitoid generations. Biol. Control 12, 1–6 (1998).Article 

Google Scholar 
51.Ponder, K. L., Pritchard, J., Bale, J. S. & Harrington, R. Feeding behaviour of the aphid Rhopalosiphum padi (Hemiptera: Aphididae) on nitrogen and water-stressed barley (Hordeum vulgare) seedlings. Bull. Entomol. Res. 91, 125–130 (2001).CAS 
PubMed 
PubMed Central 

Google Scholar 
52.Cabrera, H. M., Argandoña, V. H., Zúñiga, G. E. & Corcuera, L. J. Effect of infestation by aphids on the water status of barley and insect development. Phytochemistry 40, 1083–1088 (1995).CAS 
Article 

Google Scholar 
53.Pons, X. & Tatchell, G. M. Drought stress and cereal aphid performance. Ann. Appl. Biol. 126, 19–31 (1995).Article 

Google Scholar 
54.Silva, P. S., Albuquerque, G. S., Tauber, C. A. & Tauber, M. J. Life history of a widespread Neotropical predator, Chrysopodes (Chrysopodes) lineafrons (Neuroptera: Chrysopidae). Biol. Control 41, 33–41 (2007).Article 

Google Scholar 
55.Malina, R., Praslička, J. & Schlarmannová, J. Developmental rates of the aphid Aphis pomi (Aphidoidea: Aphididae) and its parasitoid Aphidius ervi (Hymenoptera: Aphidiidae). Biologia 65, 899–902 (2010).Article 

Google Scholar 
56.Bensadia, F., Boudreault, S., Guay, J. F., Michaud, D. & Cloutier, C. Aphid clonal resistance to a parasitoid fails under heat stress. J. Insect Physiol. 52, 146–157 (2006).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
57.Vorburger, C., Ganesanandamoorthy, P. & Kwiatkowski, M. Comparing constitutive and induced costs of symbiont-conferred resistance to parasitoids in aphids. Ecol. Evol. 3, 706–713 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
58.Dai, A. Increasing drought under global warming in observations and models. Nat. Clim. Chang. 3, 52–58 (2013).ADS 
Article 

Google Scholar  More

SPOTLIGHT
29 June 2021

China’s economic approach to protecting its ecology

Ecotourism could provide an alternative income for those who risk losing their livelihoods when areas are given national-park status.

Sarah O’Meara

0

Sarah O’Meara

Sarah O’Meara is a freelance journalist in London.

View author publications

You can also search for this author in PubMed
 Google Scholar

Share on Twitter
Share on Twitter

Share on Facebook
Share on Facebook

Share via E-Mail
Share via E-Mail

Tourists take photos at a bird-observation ecotourism point in Ziyun Village, in southeast China’s Fujian province.Credit: Xinhua/Shutterstock

Later this year, China will announce the first parks to be included in its new protected-areas system. It is aiming to replace the current fragmented network of poorly managed protected areas with a national-park model similar to that in other nations.Since the idea was mooted in 2013, the Chinese government has drawn on expertise from around the world and set up ten pilot national parks to test specific conservation strategies.Yet, millions of people work in and around these areas, doing everything from farming to running hotels. And once the parks receive formal protection, there will be a much smaller window for commercial activities and these people risk losing their livelihoods, says Rose Niu, chief conservation officer at the Paulson Institute in Washington DC. For the plan to succeed, China’s National Forestry and Grassland Administration will need to achieve a balance between protecting the country’s ecological systems and its people, Niu says. Her team has been closely involved in the plan’s development: advising on policy planning, training and the sharing of information between Chinese and international experts.
Spotlight on Ecology in China
Proposed ideas to tackle the loss in earnings that local people could face include compensation schemes and the resettling of households. Jobs will also be created in park management and protection and in ecotourism to encourage residents to be employed as part of conservation efforts.Niu thinks that encouraging local people to embrace this new economy, which also includes jobs in organic farming and wildlife management, is a very ambitious goal. “People’s awareness of these ideas is, sorry to say, still not very high. So you have to develop very strict rules for planning and management, so any ecotourism doesn’t get out of control. This can happen quickly, because it’s such a lucrative area and China has a highly entrepreneurial culture.”People, protected areas and ChinaEconomic development and environmental protection have a complicated history in China, born of the competing needs of boosting rural economies and conserving their natural resources. Short-term, profit-oriented projects have often won out.For example, Jiuzhaigou, a biodiverse and famously scenic valley in Sichuan province, was designated a nature reserve in 1982 because of its endangered plants and animals, including giant pandas. Poorly managed tourism followed and the local economy boomed, but the reserve declined. A sharp rise in air and water pollution led to the removal of private transport and the closure of hotels and restaurants in the reserve at the end of 2004.However, simply suspending tourism projects to regain control over the environment has an immediate knock-on effect for local residents, says Linjing Ren, a public-policy researcher at Northwestern Polytechnical University in Xi’an, China. “Many rely on offering accommodation and catering services for tourists, and can suddenly lose their main source of income,” she says.

Wild yaks navigate the Sanjiangyuan region of northwest China’s Qinghai province. The number of wild animals in the area is on the rise.Credit: CHINE NOUVELLE/SIPA/Shutterstock

And despite government efforts, protected areas continue to be exploited for commercial use. As recently as 2016, officials from five provinces were disciplined for allowing environmental regulations to be flouted. Their misdemeanours included allowing the discharge of untreated waste water into rivers and the mining of coal.Having agricultural areas inside protected regions can also lead to conflict between people and wildlife. In the Qinling Mountains in central China, for example, the establishment of a nature reserve increased the numbers of animals such as bears and wild boar that eat and damage crops. Unfortunately, the government’s financial compensation scheme does not completely cover such losses, according to Yali Wen, a researcher at Beijing Forestry University who specializes in economics and the environment.“One thing that could be improved is more government funding for human and wildlife conflicts. Not only is this fair, but it gives communities an incentive to engage with the idea that natural resources need to be protected in the long term,” Wen says.New parks, new ecotourismThe need for a strategic approach to ensure the economic security of communities affected by the plan is urgent, given that four of the ten pilot parks are in western and central China, which contain the country’s poorest regions. The Giant Panda National Park, for instance — a 27,133-square-kilometre wildlife corridor in central China — encompasses impoverished areas in Sichuan, Shaanxi and Gansu provinces. And most of the 17,000 households who live inside the largest pilot park, 123,100-square-kilometre Sanjiangyuan in the northwest of Qinghai, make their living by yak herding. Many have collective land rights, which allow them to use the land for grazing, says Lu Zhi, a conservation biologist at Peking University in Beijing.

Bee hives, tended by local villagers, adorn cliffs in Guanba. The hives are in a community-conserved conservation area that also includes panda and otter habitats.Credit: Lu Zhi

But instead of paying compensation to local communities to convert swathes of land from grazing to parkland — an expensive exercise — the government decided to recruit one person from each household to retrain as a park ranger. According to Niu, who evaluated the retraining scheme in 2019, each community ranger is paid 20,000 yuan (US$3,100) per year to monitor wildlife and protect the local environment. This alternative livelihood makes them less dependent on the park’s natural resources, she says. “The herders said that although that salary is not a lot of money — it’s roughly the price of three yaks — they were very proud to be doing this work. The project was well designed to give them a sense of ownership.”Government statistics say that 17,211 herders have already been hired to monitor the conservation of grassland and wildlife and raise awareness of environmental laws.New ideas in actionTerry Townshend, a wildlife conservationist and biodiversity adviser to Beijing’s government, has since 2017 been training yak herders in Qinghai in the kinds of skills that ecologists hope could be a model for sustainable development since 2017. In 2016, he met the official responsible for Zaduo, a county in Qinghai Province where snow leopards roam the valleys, at a wildlife-watching festival organized by the Shan Shui Conservation Centre, a Chinese non-profit body. After mentioning that snow-leopard tours had been popular and lucrative in other countries, Townshend was invited to write an ecotourism proposal for Zaduo. Three months later, his ideas were given the green light.“There’s very little literature on doing anything like this,” says Townshend. “I think it’s the first of its kind in China. I made it up from scratch. I remember flying there, thinking, is this really going to work? Are we really going to get Tibetan herders to come to a classroom to do training?”

A-Ta, a Tibetan herder whose income largely comes from raising yaks and collecting caterpillar fungus, places debris in a bag as he leads his team of rubbish collectors in Sanjiangyuan.Credit: Ng Han Guan/AP/Shutterstock

Over 3 days, Townshend and other specialists gave 16 herders the skills they needed to host tourists and take them on tours of local wildlife spots — everything from cooking and basic first aid to animal tracking and identification. What was key to the project’s success, he says, was giving the community autonomy to make decisions. By 2019, the project had generated 1 million yuan in revenue. “They made all major calls, from pricing the tours to deciding the programme’s organizational structure, and all of the income stays with the households,” says Townshend. “The long-term advantage is that the risk of local people killing wildlife is reduced, because they now see these predators as assets. It also means that tourism is carefully managed and profits [are] divided entirely equally.”Townshend says the project was fortunate to have the three key elements he thinks are required for success: abundant wildlife, an effective community structure that can cooperatively deal with issues as they arise and the full support of local government.From working with other snow-leopard-tourism teams in Italy, India, Nepal, Sweden and Afghanistan, he has found that projects missing any one of those ingredients are likely to fail. “Often, if the project is not effectively managed, there can be a breakdown in social cohesion. Families end up competing, with some benefiting more than others, causing jealousy and negative behaviour,” he says.The need for full community buy-inIn 2018, Wen and his team at Beijing Forestry University surveyed 1,270 households inside and adjacent to the mooted pilot Giant Panda National Park. Around one-fifth had chosen to participate in local ecotourism schemes, such as running farm tours, providing catering and accommodation and selling local products to tourists. And Wen’s team found that those that did were already in a better economic and social position than were those who declined1.“The early adopters were those who could afford to take a risk. They were already financially secure, had some form of higher education and were well placed geographically to work with tourists,” says Wen, adding that successful ecotourism depends on the ability of participants to withstand the risks and difficulties common to starting a business.“In China, this means having a combination of financial and social capital: enough money to provide a safety net and strong-enough community connections to ensure that you can get support when you need it,” he says. And ultimately, the tourists need to turn up: local government has to deliver a well-considered and managed plan to encourage tourism into the area, he says.One challenge posed by bringing ecotourism into poor communities is that it has the potential to exacerbate existing social divisions. Wen’s survey participants complained that wealthy people in the area were better equipped to take advantage of the fresh economic opportunities. “They felt it resulted in a widening gap between rich and poor,” he says.Yet, despite income disparities, and complaints about how tourists can be invasive, Wen says that overall attitudes towards ecotourism were extremely positive, with most locals agreeing that the advantages entirely outweighed the disadvantages. Many of the most attractive aspects of ecotourism stem from a shift in people’s daily priorities, his research suggests. As agriculture has become more mechanized and fewer family members are needed to tend small plots, young people head to the cities for work. Creating ecotourism business models gives them an economic incentive to stay, he says. “Generations of families like the idea of being able to stay together, and the projects also increase people’s sense of pride in their home towns.” A chance for the next generationEcologists in China hope that future generations will develop and improve ecotourism projects in protected areas. Niu, who grew up in a remote area of China, says it is key that any change to a person’s way of life brought about by government policy is voluntary. “No one should be forced to move, for example. But if people who live in remote areas are willing to move to places where they can access better public services, like schooling for their children and health care for seniors, the relocation should not be criticized,” she says. “The government should also give people opportunities to take part in sustainable business such as ecotourism, so they don’t have to rely on the overuse of natural resources.”Lu has spent more than a decade developing a community conservation programme in the village of Guanba, in a part of Sichuan province that is also home to pandas. The programme includes a social enterprise that sells local honey. She says it took many years for people in China to come to appreciate these kinds of ecological products and for a market to grow around it. And it’s still in its early stages of profitability.As the programme slowly developed and overcame setbacks, the community began to think more deeply about how to protect its environment. Eventually, in 2015, it declared the forest land around Guanba a community conservation area. Now the village has three separate ventures, all owned by the community. They are run by young people who moved back to the area to be part of this work.Lu is confident that the village will benefit from the involvement of that younger generation.“We are ecologists,” she says. “We are not trained in business management. We need to train people to do both. And ensure they bring these projects to life in far less than a decade.”

doi: https://doi.org/10.1038/d41586-021-01741-1This article is part of Nature Spotlight on Ecology in China, an editorially independent supplement. Advertisers have no influence over the content.

References1.Ma, B. et al. J. Environ. Manage. 250, 109506 (2019).PubMed 
Article 

Google Scholar 
Download references

Competing Interests
The author declares no competing interests.

Related Articles

Biodiversity’s importance is growing in China’s urban agenda

Seeing biodiversity from a Chinese perspective

How to limit the ecological costs of urbanization in China

Spotlight on Ecology in China

Subjects

Ecology

Government

Policy

Latest on:

Ecology

Red light, green light: both signal ‘go’ to deadly algae
Research Highlight 24 JUN 21

Limited potential for bird migration to disperse plants to cooler latitudes
Article 23 JUN 21

Migratory birds aid the redistribution of plants to new climates
News & Views 23 JUN 21

Government

Cameroon: doubt could mean vaccine doses expire
Correspondence 29 JUN 21

It is dangerous to normalize solar geoengineering research
Correspondence 29 JUN 21

Deadly Myanmar mine disaster caused by poor planning, say data sleuths
News 29 JUN 21

Policy

Mental health of graduate students sorely overlooked
Career Feature 28 JUN 21

Impact factor abandoned by Dutch university in hiring and promotion decisions
Career News 25 JUN 21

Killing at Chinese university highlights tensions over tenure system
News 25 JUN 21

Jobs from Nature Careers

All jobs

Research Career Development Fellowships at the Institute of Structural and Molecular Biology, UCL/Birkbeck: Expression of Interest for 2021
University College London (UCL)
London, United Kingdom

JOB POST

Senior Research Associate – Data Scientist
University of Bristol
Bristol, United Kingdom

JOB POST

High Performance Computing (HPC) System Engineer (Linux)
CRUK Manchester Institute
Manchester, United Kingdom

JOB POST

School Lecturer, Senior Lecturer, Associate Professor and Professor roles
University of Bristol
Bristol, United Kingdom

JOB POST

Nature Briefing
An essential round-up of science news, opinion and analysis, delivered to your inbox every weekday.

Email address

Yes! Sign me up to receive the daily Nature Briefing email. I agree my information will be processed in accordance with the Nature and Springer Nature Limited Privacy Policy.

Sign up More

1.Akram, W. & Kumar, R. A study on positive and negative effects of social media on society. Int. J. Comput. Sci. Eng. 5, 351–354 (2017).
Google Scholar 
2.Freeman, B. & Chapman, S. Is, “YouTube” telling or selling you something? Tobacco content on the YouTube video-sharing website. Tob. Control 16, 207–210 (2007).PubMed 
PubMed Central 
Article 

Google Scholar 
3.Lipsman, A., Mudd, G., Rich, M. & Bruich, S. The power of “like”: How brands reach (and influence) fans through social-media marketing. J. Advert. Res. 52, 40–52 (2012).Article 

Google Scholar 
4.Romero, D. M., Galuba, W., Asur, S. & Huberman, B. A. Influence and passivity in social media in Joint European Conference on Machine Learning and Knowledge Discovery in Databases (eds. Gunopulos, D. Hofmann, T., Malerba, D. & Vazirgiannis, M.)  18–33 (Springer, 2011).5.Kucharski, A. Study epidemiology of fake news. Nature 540, 525–525 (2016).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
6.Correia, R. A. et al. Digital data sources and methods for conservation culturomics. Conserv. Biol. 35, 398–411 (2021).PubMed 
Article 
PubMed Central 

Google Scholar 
7.El Bizri, H. R., Morcatty, T. Q., Lima, J. J. & Valsecchi, J. The thrill of the chase: Uncovering illegal sport hunting in Brazil through YouTubeTM posts. Ecol. Soc. 20, 1–30 (2015).
Google Scholar 
8.Sbragaglia, V., Correia, R. A., Coco, S. & Arlinghaus, R. Data mining on YouTube reveals fisher group-specific harvesting patterns and social engagement in recreational anglers and spearfishers. ICES J. Mar. Sci. 77, 2234–2244 (2020).Article 

Google Scholar 
9.Oteros-Rozas, E., Martín-López, B., Fagerholm, N., Bieling, C. & Plieninger, T. Using social media photos to explore the relation between cultural ecosystem services and landscape features across five European sites. Ecol. Ind. 94, 74–86 (2018).Article 

Google Scholar 
10.Richards, D. R. & Tunçer, B. Using image recognition to automate assessment of cultural ecosystem services from social media photographs. Ecosyst. Serv. 31, 318–325 (2018).Article 

Google Scholar 
11.Aguilera-Alcalá, N., Morales-Reyes, Z., Martín-López, B., Moleón, M. & Sánchez-Zapata, J. A. Role of scavengers in providing non-material contributions to people. Ecol. Indic. 117, 106643 (2020).Article 

Google Scholar 
12.Hausmann, A. et al. Social media data can be used to understand tourists’ preferences for nature-based experiences in protected areas. Conserv. Lett. 11, e12343 (2018).Article 

Google Scholar 
13.Do, Y. Valuating aesthetic benefits of cultural ecosystem services using conservation culturomics. Ecosyst. Serv. 36, 100894 (2019).Article 

Google Scholar 
14.Casola, W. R., Rushing, J., Futch, S., Vayer, V., Lawson, D. F., Cavalieri, M. J., Larson, L. R. & Peterson, N. How do YouTube videos impact tolerance of wolves? Human Dimens. Wildl. 1–13 (2020).15.Miranda, E. B., Ribeiro, R. P. Jr. & Strüssmann, C. The ecology of human-anaconda conflict: A study using internet videos. Trop. Conserv. Sci. 9, 43–77 (2016).Article 

Google Scholar 
16.Rust, N. A. Media framing of financial mechanisms for resolving human–predator conflict in Namibia. Hum. Dimens. Wildl. 20, 440–453 (2015).Article 

Google Scholar 
17.Margalida, A. & Donázar, J. A. Fake news and vultures. Nat. Sustain. 3, 492–493 (2020).18.Nekaris, K.A.-I., Campbell, N., Coggins, T. G., Rode, E. J. & Nijman, V. Tickled to death: Analysing public perceptions of ‘cute’videos of threatened species (slow lorises–Nycticebus spp.) on Web 2.0 Sites. PLoS ONE 8, e69215 (2013).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
19.Lambertucci, S. A., Margalida, A., Amar, A. & Ballejo, F. Presumed killers? Vultures, stakeholders, science and misperceptions. Conserv. Sci. Pract. https://doi.org/10.1111/csp2.415 (2021).Article 

Google Scholar 
20.Kusmanoff, A. M., Fidler, F., Gordon, A., Garrard, G. E. & Bekessy, S. A. Five lessons to guide more effective biodiversity conservation message framing. Conserv. Biol. 34, 1131–1141 (2020).PubMed 
Article 

Google Scholar 
21.Jones, C., Hine, D. W. & Marks, A. D. The future is now: Reducing psychological distance to increase public engagement with climate change. Risk Anal. 37, 331–341 (2017).PubMed 
Article 

Google Scholar 
22.McDonald, R. I., Chai, H. Y. & Newell, B. R. Personal experience and the ‘psychological distance’of climate change: An integrative review. J. Environ. Psychol. 44, 109–118 (2015).Article 

Google Scholar 
23.Festinger, L. Cognitive dissonance. Sci. Am. 207, 93–106 (1962).CAS 
PubMed 
Article 

Google Scholar 
24.Harmon-Jones, E. & Mills, J. An introduction to cognitive dissonance theory and an overview of current persepectives on the theory in Cognitive Dissonance: Perspectives on a Pivotal Theory in Social Psychology (eds. Harmon-Jones, E. & Mills, J) 3–21 (American Psychological Association1999).25.Ballejo, F., Plaza, P. I. & Lambertucci, S. A. The conflict between scavenging birds and farmers: Field observations do not support people’s perceptions. Biol. Conserv. 248, 108627 (2020).Article 

Google Scholar 
26.Guerisoli, M. D. L. M. et al. Characterization of puma–livestock conflicts in rangelands of central Argentina. R. Soc. Open Sci. 4, 170852 (2017).PubMed 
PubMed Central 
Article 

Google Scholar 
27.Torres, D. F., Oliveira, E. S. & Alves, R. R. Conflicts between humans and terrestrial vertebrates: A global review. Trop. Conserv. Sci. 11, 1940082918794084 (2018).
Google Scholar 
28.Inskip, C. & Zimmermann, A. Human-felid conflict: A review of patterns and priorities worldwide. Oryx 43, 18–34 (2009).Article 

Google Scholar 
29.Arnulphi, V. B. C., Lambertucci, S. A. & Borghi, C. E. Education can improve the negative perception of a threatened long-lived scavenging bird, the Andean condor. PLoS ONE 12, e0185278 (2017).Article 
CAS 

Google Scholar 
30.Duriez, O. et al. Vultures attacking livestock: A problem of vulture behavioural change or farmers’ perception?. Bird Conserv. Int. 29, 437–453 (2019).Article 

Google Scholar 
31.Margalida, A., Campión, D. & Donázar, J. A. Vultures vs livestock: Conservation relationships in an emerging conflict between humans and wildlife. Oryx 48, 172–176 (2014).Article 

Google Scholar 
32.Reyes-Menendez, A., Saura, J. R. & Filipe, F. Marketing challenges in the# MeToo era: Gaining business insights using an exploratory sentiment analysis. Heliyon 6, e03626 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
33.Ballejo, F., Grilli, M. G. & Lambertucci, S. A. A long and troublesome journey: People’s perceptions and attitudes along the migratory path of a scavenger bird. Ethnobiol. Conserv. 8, 1–13 (2019).
Google Scholar 
34.Zollo, F. et al. Debunking in a world of tribes. PLoS ONE 12, e0181821 (2017).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
35.Bessi, A. et al. Users polarization on Facebook and Youtube. PLoS ONE 11, e0159641 (2016).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
36.Baumeister, R. F., Bratslavsky, E., Finkenauer, C. & Vohs, K. D. Bad is stronger than good. Rev. Gen. Psychol. 5, 323–370 (2001).Article 

Google Scholar 
37.Plaza, P. I., Martínez-López, E. & Lambertucci, S. A. The perfect threat: Pesticides and vultures. Sci. Total Environ. 687, 1207–1218 (2019).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
38.Macdonald, E. A. et al. Conservation inequality and the charismatic cat: Felis felicis. Glob. Ecol. Conserv. 3, 851–866 (2015).Article 

Google Scholar 
39.Kaczensky, P. Large carnivore depredation on livestock in Europe. Ursus. 11, 59–71 (1999).40.Patterson, B. D., Kasiki, S. M., Selempo, E. & Kays, R. W. Livestock predation by lions (Panthera leo) and other carnivores on ranches neighboring Tsavo National Parks, Kenya. Biol. Conserv. 119, 507–516 (2004).Article 

Google Scholar 
41.Sommers, A. P., Price, C. C., Urbigkit, C. D. & Peterson, E. M. Quantifying economic impacts of large-carnivore depredation on Bovine calves. J. Wildl. Manag. 74, 1425–1434 (2010).Article 

Google Scholar 
42.Wang, S. W. & Macdonald, D. W. Livestock predation by carnivores in Jigme Singye Wangchuck National Park, Bhutan. Biol. Conserv. 129, 558–565 (2006).Article 

Google Scholar 
43.Ballejo, F., Plaza, P. I. & Lambertucci, S. A. The productive, ecological, and perception problem of the “unacceptable” livestock losses due to scavenger birds. Biol. Conserv. 250, 108723 (2020).Article 

Google Scholar 
44.Toivonen, T. et al. Social media data for conservation science: A methodological overview. Biol. Conserv. 233, 298–315 (2019).Article 

Google Scholar 
45.Troumbis, A. Y. & Iosifidis, S. A decade of Google Trends-based Conservation culturomics research: A critical evaluation of an evolving epistemology. Biol. Conserv. 248, 108647 (2020).Article 

Google Scholar 
46.Buechley, E. R. & Şekercioğlu, Ç. H. The avian scavenger crisis: Looming extinctions, trophic cascades, and loss of critical ecosystem functions. Biol. Conserv. 198, 220–228 (2016).Article 

Google Scholar 
47.Ogada, D. L., Keesing, F. & Virani, M. Z. Dropping dead: Causes and consequences of vulture population declines worldwide. Ann. N. Y. Acad. Sci. 1249, 57–71 (2012).ADS 
PubMed 
Article 
PubMed Central 

Google Scholar 
48.Ogada, D. L. The power of poison: Pesticide poisoning of Africa’s wildlife. Ann. N. Y. Acad. Sci. 1322, 1–20 (2014).ADS 
CAS 
PubMed 
Article 

Google Scholar 
49.Plaza, P. I. & Lambertucci, S. A. What do we know about lead contamination in wild vultures and condors? A review of decades of research. Sci. Total Environ. 654, 409–417 (2019).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
50.Behmke, S. et al. Chronic lead exposure is epidemic in obligate scavenger populations in eastern North America. Environ. Int. 79, 51–55 (2015).CAS 
PubMed 
Article 

Google Scholar 
51.Grilli, M. G., Bildstein, K. L. & Lambertucci, S. A. Nature’s clean-up crew: Quantifying ecosystem services offered by a migratory avian scavenger on a continental scale. Ecosyst. Serv. 39, 100990 (2019).Article 

Google Scholar 
52.Plaza, P. I., Blanco, G. & Lambertucci, S. A. Implications of bacterial, viral and mycotic microorganisms in vultures for wildlife conservation, ecosystem services and public health. Ibis 162, 1109–1124 (2020).Article 

Google Scholar 
53.Lazer, D. M. et al. The science of fake news. Science 359, 1094–1096 (2018).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
54.Clement, J. YouTube-statistics & facts. statista.  https://www.statista.com/topics/2019/youtube/ (2019).55.Guerisoli, M. D. L. M., Luengos Vidal, E., Caruso, N., Giordano, A. J. & Lucherini, M. Puma–livestock conflicts in the Americas: A review of the evidence. Mammal Rev. 66, 33–43 (2020).Article 

Google Scholar 
56.R Core Team. A language and environment for statistical computing. (R Foundation for Statistical Computing, 2015).57.Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat soft. 67, 1–48  (2014). More

1.McFall-Ngai, M. et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl Acad. Sci. 110, 3229–3236 (2013).CAS 
PubMed 
PubMed Central 
Article 
ADS 

Google Scholar 
2.Horn, M. Chlamydiae as symbionts in eukaryotes. Annu. Rev. Microbiol. 62, 113–131 (2008).CAS 
PubMed 
Article 

Google Scholar 
3.Taylor-Brown, A., Vaughan, L., Greub, G., Timms, P. & Polkinghorne, A. Twenty years of research into Chlamydia-like organisms: a revolution in our understanding of the biology and pathogenicity of members of the phylum Chlamydiae. Pathog. Dis. 73, 1–15 (2015).CAS 
PubMed 
Article 

Google Scholar 
4.Wagner, M. & Horn, M. The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr. Opin. Biotechnol. 17, 241–249 (2006).CAS 
PubMed 
Article 

Google Scholar 
5.Rivas-Marín, E. & Devos, D. P. The Paradigms They Are a-Changin’: past, present and future of PVC bacteria research. Antonie van. Leeuwenhoek 111, 785–799 (2018).PubMed 
Article 

Google Scholar 
6.Elwell, C., Mirrashidi, K. & Engel, J. Chlamydia cell biology and pathogenesis. Nat. Rev. Microbiol. 14, 385–400 (2016).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
7.Collingro, A., Köstlbacher, S. & Horn, M. Chlamydiae in the Environment. Trends Microbiol. 28, 877–888 (2020).CAS 
PubMed 
Article 

Google Scholar 
8.Lagkouvardos, I. et al. Integrating metagenomic and amplicon databases to resolve the phylogenetic and ecological diversity of the Chlamydiae. ISME J. 8, 115–125 (2014).CAS 
PubMed 
Article 

Google Scholar 
9.Greub, G. & Raoult, D. Microorganisms resistant to free-living amoebae. Clin. Microbiol. Rev. 17, 413–433 (2004).PubMed 
PubMed Central 
Article 

Google Scholar 
10.Bar-On, Y. M., Phillips, R. & Milo, R. The biomass distribution on Earth. Proc. Natl Acad. Sci. 115, 6506–6511 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
11.Taylor-Brown, A., Madden, D. & Polkinghorne, A. Culture-independent approaches to chlamydial genomics. Micro. Genom. 4, e000145 (2018).
Google Scholar 
12.Sixt, B. S. & Valdivia, R. H. Molecular Genetic Analysis of Chlamydia Species. Annu. Rev. Microbiol. 70, 179–198 (2016).CAS 
PubMed 
Article 

Google Scholar 
13.Bachmann, N. L., Polkinghorne, A. & Timms, P. Chlamydia genomics: providing novel insights into chlamydial biology. Trends Microbiol. 22, 464–472 (2014).CAS 
PubMed 
Article 

Google Scholar 
14.Subtil, A. & Dautry-Varsat, A. Chlamydia: five years A.G. (after genome). Curr. Opin. Microbiol. 7, 85–92 (2004).CAS 
PubMed 
Article 

Google Scholar 
15.Collingro, A. et al. Unity in Variety—The Pan-Genome of the Chlamydiae. Mol. Biol. Evol. 28, 3253–3270 (2011).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
16.Taylor-Brown, A. et al. Metagenomic Analysis of Fish-Associated Ca. Parilichlamydiaceae Reveals Striking Metabolic Similarities to the Terrestrial Chlamydiaceae. Genom. Biol. Evol. 10, 2587–2595 (2018).Article 
CAS 

Google Scholar 
17.Baker, B. J., Lazar, C. S., Teske, A. P. & Dick, G. J. Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria. Microbiome 3, 14 (2015).PubMed 
PubMed Central 
Article 

Google Scholar 
18.Collingro, A. et al. Unexpected genomic features in widespread intracellular bacteria: evidence for motility of marine chlamydiae. ISME J. 11, 2334–2344 (2017).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
19.Dharamshi, J. E. et al. Marine Sediments Illuminate Chlamydiae Diversity and Evolution. Curr. Biol. 30, 1032–1048.e7 (2020).CAS 
PubMed 
Article 

Google Scholar 
20.Pillonel, T., Bertelli, C. & Greub, G. Environmental Metagenomic Assemblies Reveal Seven New Highly Divergent Chlamydial Lineages and Hallmarks of a Conserved Intracellular Lifestyle. Front. Microbiol. 9, 79 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
21.Taylor-Brown, A., Bachmann, N. L., Borel, N. & Polkinghorne, A. Culture-independent genomic characterisation of Candidatus Chlamydia sanzinia, a novel uncultivated bacterium infecting snakes. BMC Genom. 17, 710 (2016).Article 

Google Scholar 
22.Taylor-Brown, A. et al. Culture-independent genomics of a novel chlamydial pathogen of fish provides new insight into host-specific adaptations utilized by these intracellular bacteria. Environ. Microbiol. 19, 1899–1913 (2017).CAS 
PubMed 
Article 

Google Scholar 
23.Stairs, C. W. et al. Chlamydial contribution to anaerobic metabolism during eukaryotic evolution. Sci. Adv. 6, eabb7258 (2020).CAS 
PubMed 
PubMed Central 
Article 
ADS 

Google Scholar 
24.Brockhurst, M. A. et al. The Ecology and Evolution of Pangenomes. Curr. Biol. 29, R1094–R1103 (2019).CAS 
PubMed 
Article 

Google Scholar 
25.Nayfach, S. et al. A genomic catalog of Earth’s microbiomes. Nat. Biotechnol. 39, 499–509 (2020).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
26.Bowers, R. M. et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat. Biotechnol. 35, 725–731 (2017).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
27.Wu, D. et al. A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462, 1056–1060 (2009).CAS 
PubMed 
PubMed Central 
Article 
ADS 

Google Scholar 
28.Chen, I. A. et al. IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes. Nucleic Acids Res. 47, D666-D677 (2019).29.Schulz, F. et al. Towards a balanced view of the bacterial tree of life. Microbiome 5, 140 (2017).PubMed 
PubMed Central 
Article 

Google Scholar 
30.Subtil, A., Collingro, A. & Horn, M. Tracing the primordial Chlamydiae: extinct parasites of plants? Trends Plant Sci. 19, 36–43 (2014).CAS 
PubMed 
Article 

Google Scholar 
31.Cenci, U. et al. Biotic Host-Pathogen Interactions As Major Drivers of Plastid Endosymbiosis. Trends Plant Sci. 22, 316–328 (2017).CAS 
PubMed 
Article 

Google Scholar 
32.Blair, P. M. et al. Exploration of the Biosynthetic Potential of the Populus Microbiome. mSystems 3, e00045-18 (2018).33.Parks, D. H. et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 36, 996–1004 (2018).CAS 
PubMed 
Article 

Google Scholar 
34.Huerta-Cepas, J. et al. eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res. 44, D286–D293 (2016).CAS 
PubMed 
Article 

Google Scholar 
35.Miele, V., Penel, S. & Duret, L. Ultra-fast sequence clustering from similarity networks with SiLiX. BMC Bioinforma. 12, 116 (2011).Article 

Google Scholar 
36.Abby, S. S. & Rocha, E. P. C. The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems. PLoS Genet. 8, e1002983 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
37.Peters, J., Wilson, D. P., Myers, G., Timms, P. & Bavoil, P. M. Type III secretion à la Chlamydia. Trends Microbiol. 15, 241–251 (2007).CAS 
PubMed 
Article 

Google Scholar 
38.Archuleta, T. L. et al. The Chlamydia effector chlamydial outer protein N (CopN) sequesters tubulin and prevents microtubule assembly. J. Biol. Chem. 286, 33992–33998 (2011).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
39.Verma, A. & Maurelli, A. T. Identification of two eukaryote-like serine/threonine kinases encoded by Chlamydia trachomatis serovar L2 and characterization of interacting partners of Pkn1. Infect. Immun. 71, 5772–5784 (2003).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
40.Omsland, A., Sixt, B. S., Horn, M. & Hackstadt, T. Chlamydial metabolism revisited: interspecies metabolic variability and developmental stage-specific physiologic activities. FEMS Microbiol. Rev. 38, 779–801 (2014).CAS 
PubMed 
Article 

Google Scholar 
41.Schwöppe, C., Winkler, H. H. & Neuhaus, H. E. Properties of the glucose-6-phosphate transporter from Chlamydia pneumoniae (HPTcp) and the glucose-6-phosphate sensor from Escherichia coli (UhpC). J. Bacteriol. 184, 2108–2115 (2002).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
42.Tjaden, J. et al. Two nucleotide transport proteins in Chlamydia trachomatis, one for net nucleoside triphosphate uptake and the other for transport of energy. J. Bacteriol. 181, 1196–1202 (1999).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
43.Schmitz-Esser, S. et al. ATP/ADP translocases: a common feature of obligate intracellular amoebal symbionts related to Chlamydiae and Rickettsiae. J. Bacteriol. 186, 683–691 (2004).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
44.Haferkamp, I. et al. Tapping the nucleotide pool of the host: novel nucleotide carrier proteins of Protochlamydia amoebophila. Mol. Microbiol. 60, 1534–1545 (2006).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
45.Rosario, C. J. & Tan, M. The early gene product EUO is a transcriptional repressor that selectively regulates promoters of Chlamydia late genes. Mol. Microbiol. 84, 1097–1107 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
46.Belland, R. J. et al. Genomic transcriptional profiling of the developmental cycle of Chlamydia trachomatis. Proc. Natl Acad. Sci. U. S. A. 100, 8478–8483 (2003).CAS 
PubMed 
PubMed Central 
Article 
ADS 

Google Scholar 
47.Kislyuk, A. O., Haegeman, B., Bergman, N. H. & Weitz, J. S. Genomic fluidity: an integrative view of gene diversity within microbial populations. BMC Genom. 12, 32 (2011).Article 

Google Scholar 
48.McInerney, J. O., McNally, A. & O’Connell, M. J. Why prokaryotes have pangenomes. Nat. Microbiol. 2, 17040 (2017).CAS 
PubMed 
Article 

Google Scholar 
49.Wang, Z. & Wu, M. Comparative Genomic Analysis of Acanthamoeba Endosymbionts Highlights the Role of Amoebae as a ‘Melting Pot’ Shaping the Rickettsiales Evolution. Genom. Biol. Evol. 9, 3214–3224 (2017).CAS 
Article 

Google Scholar 
50.Moliner, C., Fournier, P.-E. & Raoult, D. Genome analysis of microorganisms living in amoebae reveals a melting pot of evolution. FEMS Microbiol. Rev. 34, 281–294 (2010).CAS 
PubMed 
Article 

Google Scholar 
51.Bertelli, C. et al. Sequencing and characterizing the genome of Estrella lausannensis as an undergraduate project: training students and biological insights. Front. Microbiol. 6, 101 (2015).PubMed 
PubMed Central 
Article 

Google Scholar 
52.Bertelli, C., Goesmann, A. & Greub, G. Criblamydia sequanensis Harbors a Megaplasmid Encoding Arsenite Resistance. Genom. Announc. 2, e00949–14 (2014).Article 

Google Scholar 
53.Köstlbacher, S., Collingro, A., Halter, T., Domman, D. & Horn, M. Coevolving Plasmids Drive Gene Flow and Genome Plasticity in Host-Associated Intracellular Bacteria. Curr. Biol. 31, 346–357.e3 (2021).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
54.Bertelli, C. et al. CRISPR System Acquisition and Evolution of an Obligate IntracellularChlamydia-Related Bacterium. Genom. Biol. Evol. 8, 2376–2386 (2016).CAS 
Article 

Google Scholar 
55.Benamar, S. et al. Developmental Cycle and Genome Analysis of Protochlamydia massiliensis sp. nov. a New Species in the Parachlamydiacae Family. Front. Cell. Infect. Microbiol. 7, 385 (2017).56.Panwar, P. et al. Influence of the polar light cycle on seasonal dynamics of an Antarctic lake microbial community. Microbiome 8, 116 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
57.Venn, A. A., Loram, J. E. & Douglas, A. E. Photosynthetic symbioses in animals. J. Exp. Bot. 59, 1069–1080 (2008).CAS 
PubMed 
Article 

Google Scholar 
58.Cavanaugh, C. M. Symbiotic chemoautotrophic bacteria in marine invertebrates from sulphide-rich habitats. Nature 302, 58–61 (1983).CAS 
Article 
ADS 

Google Scholar 
59.Hu, J., Jin, K., He, Z.-G. & Zhang, H. Citrate lyase CitE in Mycobacterium tuberculosis contributes to mycobacterial survival under hypoxic conditions. PLoS ONE 15, e0230786 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
60.Kantor, R. S. et al. Genome-Resolved Meta-Omics Ties Microbial Dynamics to Process Performance in Biotechnology for Thiocyanate Degradation. Environ. Sci. Technol. 51, 2944–2953 (2017).CAS 
PubMed 
Article 
ADS 

Google Scholar 
61.Wang, Z. et al. A new method for rapid genome classification, clustering, visualization, and novel taxa discovery from metagenome. https://doi.org/10.1101/812917.62.Sabehi, G. et al. New insights into metabolic properties of marine bacteria encoding proteorhodopsins. PLoS Biol. 3, e273 (2005).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
63.Croitoru, K. Faculty Opinions recommendation of Environmental genome shotgun sequencing of the Sargasso Sea. Faculty Opin.—Post-Publ. Peer Rev. Biomed. Lit. (2014). https://doi.org/10.3410/f.1017813.793496370.64.Gómez-Consarnau, L. et al. Proteorhodopsin phototrophy promotes survival of marine bacteria during starvation. PLoS Biol. 8, e1000358 (2010).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
65.Omsland, A., Sager, J., Nair, V., Sturdevant, D. E. & Hackstadt, T. Developmental stage-specific metabolic and transcriptional activity of Chlamydia trachomatis in an axenic medium. Proc. Natl Acad. Sci. 109, 19781–19785 (2012).CAS 
PubMed 
PubMed Central 
Article 
ADS 

Google Scholar 
66.Caspi, R. et al. The MetaCyc database of metabolic pathways and enzymes—a 2019 update. Nucleic Acids Res. 48, D445–D453 (2020).CAS 
PubMed 
Article 

Google Scholar 
67.Glasemacher, J., Bock, A. K., Schmid, R. & Schønheit, P. Purification and Properties of acetyl-CoA Synthetase (ADP-forming), an Archaeal Enzyme of Acetate Formation and ATP Synthesis, From the Hyperthermophile Pyrococcus Furiosus. Eur. J. Biochem. 244, 561–567 (1997).CAS 
PubMed 
Article 

Google Scholar 
68.Stairs, C. W., Leger, M. M. & Roger, A. J. Diversity and origins of anaerobic metabolism in mitochondria and related organelles. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370, 20140326 (2015).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
69.Leger, M. M., Gawryluk, R. M. R., Gray, M. W. & Roger, A. J. Evidence for a hydrogenosomal-type anaerobic ATP generation pathway in Acanthamoeba castellanii. PLoS ONE 8, e69532 (2013).CAS 
PubMed 
PubMed Central 
Article 
ADS 

Google Scholar 
70.Novák, L. et al. Arginine deiminase pathway enzymes: evolutionary history in metamonads and other eukaryotes. BMC Evol. Biol. 16, 197 (2016).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
71.Benoit, S. L., Maier, R. J., Sawers, R. G. & Greening, C. Molecular Hydrogen Metabolism: a Widespread Trait of Pathogenic Bacteria and Protists. Microbiol. Mol. Biol. Rev. 84, e00092–19 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
72.Søndergaard, D., Pedersen, C. N. S. & Greening, C. HydDB: a web tool for hydrogenase classification and analysis. Sci. Rep. 6, 34212 (2016).PubMed 
PubMed Central 
Article 
ADS 
CAS 

Google Scholar 
73.Kleiner, M. et al. Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use. Proc. Natl Acad. Sci. U. S. A. 109, E1173–E1182 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
74.Schut, G. J. & Adams, M. W. W. The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J. Bacteriol. 191, 4451–4457 (2009).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
75.Greening, C. et al. Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival. ISME J. 10, 761–777 (2016).CAS 
PubMed 
Article 

Google Scholar 
76.Hou, S. et al. Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. Biol. Direct 3, 26 (2008).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
77.Berney, M., Greening, C., Conrad, R., Jacobs, W. R. Jr & Cook, G. M. An obligately aerobic soil bacterium activates fermentative hydrogen production to survive reductive stress during hypoxia. Proc. Natl Acad. Sci. U. S. A. 111, 11479–11484 (2014).CAS 
PubMed 
PubMed Central 
Article 
ADS 

Google Scholar 
78.Kaji, M. et al. The hydA gene encoding the H(2)-evolving hydrogenase of Clostridium perfringens: molecular characterization and expression of the gene. FEMS Microbiol. Lett. 181, 329–336 (1999).CAS 
PubMed 
Article 

Google Scholar 
79.Lindmark, D. G., Muller, M. & Shio, H. Hydrogenosomes in Trichomonas vaginalis. J. Parasitol. 61, 552 (1975).Article 

Google Scholar 
80.Edgar, R. C. Updating the 97% identity threshold for 16S ribosomal RNA OTUs. Bioinformatics 34, 2371–2375 (2018).CAS 
PubMed 
Article 

Google Scholar 
81.Lagkouvardos, I. et al. IMNGS: A comprehensive open resource of processed 16S rRNA microbial profiles for ecology and diversity studies. Sci. Rep. 6, 33721 (2016).CAS 
PubMed 
PubMed Central 
Article 
ADS 

Google Scholar 
82.Stride, M. C. et al. Molecular characterization of ‘Candidatus Parilichlamydia carangidicola,’ a novel Chlamydia-like epitheliocystis agent in yellowtail kingfish, Seriola lalandi (Valenciennes), and the proposal of a new family, ‘Candidatus Parilichlamydiaceae’ fam. nov. (order Chlamydiales). Appl. Environ. Microbiol. 79, 1590–1597 (2013).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
83.Draghi, A. et al. Characterization of ‘Candidatus Piscichlamydia salmonis’ (Order Chlamydiales), a Chlamydia-Like Bacterium Associated With Epitheliocystis in Farmed Atlantic Salmon (Salmo salar). J. Clin. Microbiol. 42, 5286–5297 (2004).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
84.Neuendorf, E. et al. Chlamydia caviae infection alters abundance but not composition of the guinea pig vaginal microbiota. Pathog. Dis. 73, ftv019 (2015).85.Kelly, J. et al. Composition and diversity of mucosa-associated microbiota along the entire length of the pig gastrointestinal tract; dietary influences. Environ. Microbiol. 19, 1425–1438 (2017).CAS 
PubMed 
Article 

Google Scholar 
86.Kelly, M. S. et al. The Nasopharyngeal Microbiota of Children With Respiratory Infections in Botswana. Pediatr. Infect. Dis. J. 36, e211–e218 (2017).PubMed 
PubMed Central 
Article 

Google Scholar 
87.Liechty, E. R. et al. The levonorgestrel-releasing intrauterine system is associated with delayed endocervical clearance of Chlamydia trachomatis without alterations in vaginal microbiota. Pathog. Dis. 73, ftv070 (2015).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
88.Ganz, H. H. et al. Community-Level Differences in the Microbiome of Healthy Wild Mallards and Those Infected by Influenza A Viruses. mSystems 2, e00188–16 (2017).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
89.Pizzetti, I. et al. Chlamydial seasonal dynamics and isolation of ‘Candidatus Neptunochlamydia vexilliferae’ from a Tyrrhenian coastal lake. Environ. Microbiol. 18, 2405–2417 (2016).CAS 
PubMed 
Article 

Google Scholar 
90.Nylund, A. et al. Genotyping of Candidatus Syngnamydia salmonis (chlamydiales; Simkaniaceae) co-cultured in Paramoeba perurans (amoebozoa; Paramoebidae). Arch. Microbiol. 200, 859–867 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
91.Kahane, S., Gonen, R., Sayada, C., Elion, J. & Friedman, M. G. Description and partial characterization of a new Chlamydia-like microorganism. FEMS Microbiol. Lett. 109, 329–333 (1993).CAS 
PubMed 
Article 

Google Scholar 
92.Vouga, M., Baud, D. & Greub, G. Simkania negevensis, an insight into the biology and clinical importance of a novel member of the Chlamydiales order. Crit. Rev. Microbiol. 43, 62–80 (2017).CAS 
PubMed 
Article 

Google Scholar 
93.Ziegler, M. et al. Coral bacterial community structure responds to environmental change in a host-specific manner. Nat. Commun. 10, 3092 (2019).PubMed 
PubMed Central 
Article 
ADS 
CAS 

Google Scholar 
94.Anantharaman, K. et al. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat. Commun. 7, 13219 (2016).CAS 
PubMed 
PubMed Central 
Article 
ADS 

Google Scholar 
95.Torres-Beltrán, M. et al. A compendium of geochemical information from the Saanich Inlet water column. Sci. Data 4, 170159 (2017).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
96.Hawley, A. K. et al. A compendium of multi-omic sequence information from the Saanich Inlet water column. Sci. Data 4, 170160 (2017).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
97.Orsi, W., Song, Y. C., Hallam, S. & Edgcomb, V. Effect of oxygen minimum zone formation on communities of marine protists. ISME J. 6, 1586–1601 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
98.Köstlbacher, S. et al. Draft Genome Sequences of Bacterium STE3 and sp. Strain AcF84. Endosymbionts spp. Microbiol. Resour. Announc. 9, e00220–e00220 (2020).PubMed 

Google Scholar 
99.Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).MathSciNet 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
100.Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genom. Res. 25, 1043–1055 (2015).CAS 
Article 

Google Scholar 
101.Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
102.Gurevich, A., Saveliev, V., Vyahhi, N. & Tesler, G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072–1075 (2013).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
103.Hendrickx, F. et al. A masculinizing supergene underlies an exaggerated male reproductive morph in a spider. https://doi.org/10.1101/2021.02.09.430505.104.Philippe, H. et al. Mitigating Anticipated Effects of Systematic Errors Supports Sister-Group Relationship between Xenacoelomorpha and Ambulacraria. Curr. Biol. 29, 1818–1826.e6 (2019).CAS 
PubMed 
Article 

Google Scholar 
105.Minh, B. Q., Nguyen, M. A. T. & von Haeseler, A. Ultrafast approximation for phylogenetic bootstrap. Mol. Biol. Evol. 30, 1188–1195 (2013).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
106.Le, S. Q. & Gascuel, O. An improved general amino acid replacement matrix. Mol. Biol. Evol. 25, 1307–1320 (2008).CAS 
PubMed 
Article 

Google Scholar 
107.Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A. & Jermiin, L. S. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
108.Quang, L. S., Gascuel, O. & Lartillot, N. Empirical profile mixture models for phylogenetic reconstruction. Bioinformatics 24, 2317–2323 (2008).CAS 
Article 

Google Scholar 
109.Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: improving the Ultrafast Bootstrap Approximation. Mol. Biol. Evol. 35, 518–522 (2018).CAS 
PubMed 
Article 

Google Scholar 
110.Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).CAS 
PubMed 
Article 

Google Scholar 
111.Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 47, W256–W259 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
112.Olm, M. R., Brown, C. T., Brooks, B. & Banfield, J. F. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 11, 2864–2868 (2017).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
113.Wang, H.-C., Minh, B. Q., Susko, E. & Roger, A. J. Modeling Site Heterogeneity with Posterior Mean Site Frequency Profiles Accelerates Accurate Phylogenomic Estimation. Syst. Biol. 67, 216–235 (2018).CAS 
PubMed 
Article 

Google Scholar 
114.Matsen, F. A., Kodner, R. B. & Armbrust, E. V. pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinforma. 11, 538 (2010).Article 

Google Scholar 
115.Hausmann, B. et al. Peatland Acidobacteria with a dissimilatory sulfur metabolism. ISME J. 12, 1729–1742 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
116.Konstantinidis, K. T., Rosselló-Móra, R. & Amann, R. Uncultivated microbes in need of their own taxonomy. ISME J. 11, 2399–2406 (2017).PubMed 
PubMed Central 
Article 

Google Scholar 
117.Wickham, H. ggplot2: Elegant Graphics for Data Analysis. (Springer, 2016).118.Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genom. Res. 13, 2498–2504 (2003).CAS 
Article 

Google Scholar 
119.Jain, C., Rodriguez-R, L. M., Phillippy, A. M., Konstantinidis, K. T. & Aluru, S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat. Commun. 9, 5114 (2018).PubMed 
PubMed Central 
Article 
ADS 
CAS 

Google Scholar 
120.Huerta-Cepas, J. et al. Fast Genome-Wide Functional Annotation through Orthology Assignment by eggNOG-Mapper. Mol. Biol. Evol. 34, 2115–2122 (2017).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
121.Maistrenko, O. M. et al. Disentangling the impact of environmental and phylogenetic constraints on prokaryotic within-species diversity. ISME J. 14, 1247–1259 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
122.Snipen, L. & Liland, K. H. micropan: an R-package for microbial pan-genomics. BMC Bioinforma. 16, 79 (2015).Article 
CAS 

Google Scholar 
123.R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2020).124.Benjamini, Y. & Hochberg, Y. Controlling the False Discovery Rate: a Practical and Powerful Approach to Multiple Testing. J. R. Stat. Soc.: Ser. B (Methodol.) 57, 289–300 (1995).MathSciNet 
MATH 

Google Scholar 
125.Kanehisa, M., Sato, Y. & Morishima, K. BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences. J. Mol. Biol. 428, 726–731 (2016).CAS 
PubMed 
Article 

Google Scholar 
126.Quevillon, E. et al. InterProScan: protein domains identifier. Nucleic Acids Res. 33, W116–W120 (2005).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
127.El-Gebali, S. et al. The Pfam protein families database in 2019. Nucleic Acids Res. 47, D427–D432 (2019).CAS 
PubMed 
Article 

Google Scholar 
128.Haft, D. H., Selengut, J. D. & White, O. The TIGRFAMs database of protein families. Nucleic Acids Res. 31, 371–373 (2003).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
129.Krogh, A., Larsson, B., von Heijne, G. & Sonnhammer, E. L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567–580 (2001).CAS 
PubMed 
Article 

Google Scholar 
130.Guy, L., Kultima, J. R. & Andersson, S. G. E. genoPlotR: comparative gene and genome visualization in R. Bioinformatics 26, 2334–2335 (2010).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
131.Abby, S. S. & Rocha, E. P. C. Identification of Protein Secretion Systems in Bacterial Genomes Using MacSyFinder. Methods Mol. Biol. 1615, 1–21 (2017).PubMed 
Article 
CAS 

Google Scholar 
132.Abby, S. S. et al. Identification of protein secretion systems in bacterial genomes. Sci. Rep. 6, 1–14 (2016).Article 
CAS 

Google Scholar 
133.Couvin, D. et al. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res. 46, W246–W251 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
134.Criscuolo, A. & Gribaldo, S. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol. Biol. 10, 210 (2010).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
135.Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).CAS 
PubMed 
Article 

Google Scholar 
136.Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2012).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
137.Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
138.Pruesse, E., Peplies, J. & Glöckner, F. O. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823–1829 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
139.Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
140.Lemoine, F. et al. Renewing Felsenstein’s phylogenetic bootstrap in the era of big data. Nature 556, 452–456 (2018).CAS 
PubMed 
PubMed Central 
Article 
ADS 

Google Scholar  More