Philippa Kaur

Magallón, S., Sánchez-Reyes, L. L. & Gómez-Acevedo, S. L. Thirty clues to the exceptional diversification of flowering plants. Ann. Bot. 123, 491–503 (2019).PubMed 
Article 

Google Scholar 
Shi, J. J. & Rabosky, D. L. Speciation dynamics during the global radiation of extant bats. Evolution 69, 1528–1545 (2015).PubMed 
Article 

Google Scholar 
Nicolai, M. P. J. & Matzke, N. J. Trait-based range expansion aided in the global radiation of Crocodylidae. Glob. Ecol. Biogeogr. 28, 1244–1258 (2019).Article 

Google Scholar 
Coyne, J. A. & Orr, H. A. Speciation (Sinauer Associates, 2004).Price, T. & others. Speciation in Birds (Roberts and Co., 2008).Moyle, R. G., Filardi, C. E., Smith, C. E. & Diamond, J. Explosive Pleistocene diversification and hemispheric expansion of a “great speciator”. Proc. Natl Acad. Sci. USA 106, 1863–1868 (2009).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Van Bocxlaer, I. et al. Gradual adaptation toward a range-expansion phenotype initiated the global radiation of toads. Science 327, 679–682 (2010).ADS 
PubMed 
Article 
CAS 

Google Scholar 
Phillimore, A. B. & Price, T. D. in Speciation and Patterns on Diversity (eds Butlin, R., Bridle, J. & Schluter, D.) Ch. 13 (Cambridge Univ. Press, 2009).Price, T. D. et al. Niche filling slows the diversification of Himalayan songbirds. Nature 509, 222–225 (2014).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Nosil, P. Ecological Speciation (Oxford Univ. Press, 2012).Naciri, Y. & Linder, H. P. The genetics of evolutionary radiations. Biol. Rev. Camb. Philos. Soc. 95, 1055–1072 (2020).Price, T. D. & Sol, D. Introduction: genetics of colonizing species. Am. Nat. 172, S1–S3 (2008).PubMed 
Article 

Google Scholar 
Schluter, D. The Ecology of Adaptive Radiation (Oxford Univ. Press, 2000).Gill, F. & Donsker, D. IOC world bird list (v 8.1). 2018. (2018).Del Hoyo, J., Del Hoyo, J., Elliott, A. & Sargatal, J. Handbook of the Birds of the World Vol. 1 (Lynx edicions, 1992).Cassey, P. Are there body size implications for the success of globally introduced land birds? Ecography 24, 413–420 (2001).Article 

Google Scholar 
Fristoe, T. S., Iwaniuk, A. N. & Botero, C. A. Big brains stabilize populations and facilitate colonization of variable habitats in birds. Nat. Ecol. Evol. 1, 1706–1715 (2017).PubMed 
Article 

Google Scholar 
Sayol, F. et al. Environmental variation and the evolution of large brains in birds. Nat. Commun. 7, 1–8 (2016).Article 
CAS 

Google Scholar 
Sol, D. Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol. Lett. 5, 130–133 (2009).PubMed 
Article 

Google Scholar 
Lefebvre, L. & Sol, D. Brains, lifestyles and cognition: are there general trends? Brain. Behav. Evol. 72, 135–144 (2008).PubMed 
Article 

Google Scholar 
Jønsson, K. A. et al. A supermatrix phylogeny of corvoid passerine birds (Aves: Corvides). Mol. Phylogenet. Evol. 94, 87–94 (2016).PubMed 
Article 

Google Scholar 
Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–448 (2012).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Marki, P. Z. et al. Breeding system evolution influenced the geographic expansion and diversification of the core Corvoidea (Aves: Passeriformes). Evolution 69, 1874–1924 (2015).PubMed 
Article 

Google Scholar 
KessLer, J. E. Evolution of Corvids and their presence in the neogene and the quaternary in the Carpathian Basin. Ornis Hungarica 28, 121–168 (2020).Article 

Google Scholar 
Olson, S. L. & Rasmussen, P. C., others. Miocene and Pliocene birds from the Lee Creek Mine, North Carolina. Smithson Contrib. Paleobiol. 90, 233–365 (2001).
Google Scholar 
Rabosky, D. L. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS ONE 9, e89543 (2014).Alfaro, M. E. et al. Lineage-specific diversification rates and high turnover in the history of jawed vertebrates. Proc. Natl Acad. Sci. USA 106, 13410–13414 (2009).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Rabosky, D. L., Donnellan, S. C., Grundler, M. & Lovette, I. J. Analysis and visualization of complex macroevolutionary dynamics: an example from Australian scincid lizards. Syst. Biol. 63, 610–627 (2014).PubMed 
Article 

Google Scholar 
Louca, S. & Pennell, M. W. Extant timetrees are consistent with a myriad of diversification histories. Nature 580, 502–505 (2020).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Kulemeyer, C., Asbahr, K., Gunz, P., Frahnert, S. & Bairlein, F. Functional morphology and integration of corvid skulls-a 3D geometric morphometric approach. Front. Zool. 6, 2 (2009).PubMed 
PubMed Central 
Article 

Google Scholar 
Zeffer, A., Johansson, L. C. & Marmebro, Å. Functional correlation between habitat use and leg morphology in birds (Aves). Biol. J. Linn. Soc. 79, 461–484 (2003).Article 

Google Scholar 
Wang, X., McGowan, A. J. & Dyke, G. J. Avian wing proportions and flight styles: first step towards predicting the flight modes of Mesozoic birds. PLoS ONE 6, e28672 (2011).Corbin, C. E., Lowenberger, L. K. & Gray, B. L. Linkage and trade-off in trophic morphology and behavioural performance of birds. Funct. Ecol. 29, 808–815 (2015).Article 

Google Scholar 
Kennedy, J. D. et al. The influence of wing morphology upon the dispersal, geographical distributions and diversification of the Corvides (Aves; Passeriformes). Proc. R. Soc. B Biol. Sci. 283, 20161922 (2016).Article 

Google Scholar 
Pigot, A. L. et al. Macroevolutionary convergence connects morphological form to ecological function in birds. Nat. Ecol. Evol. 4, 230–239 (2020).PubMed 
Article 

Google Scholar 
Clavel, J., Escarguel, G. & Merceron, G. mvMORPH: an R package for fitting multivariate evolutionary models to morphometric data. Methods in Ecology and Evolution 6, 1311–1319 (2015).Uyeda, J. C., Caetano, D. S. & Pennell, M. W. Comparative analysis of principal components can be misleading. Syst. Biol. 64, 677–689 (2015).CAS 
PubMed 
Article 

Google Scholar 
Leyequién, E., de Boer, W. F. & Cleef, A. Influence of body size on coexistence of bird species. Ecol. Res. 22, 735–741 (2007).Article 

Google Scholar 
Grant, P. R. Bill size, body size, and the ecological adaptations of bird species to competitive situations on islands. Syst. Biol. 17, 319–333 (1968).CAS 
Article 

Google Scholar 
Meiri, S. & Dayan, T. On the validity of Bergmann’s rule. J. Biogeogr. 30, 331–351 (2003).Article 

Google Scholar 
Friedman, N. R. et al. Evolution of a multifunctional trait: shared effects of foraging ecology and thermoregulation on beak morphology, with consequences for song evolution. Proc. R. Soc. B 286, 20192474 (2019).PubMed 
PubMed Central 
Article 

Google Scholar 
Friedman, N. R., Harmáčková, L., Economo, E. P. & Remeš, V. Smaller beaks for colder winters: Thermoregulation drives beak size evolution in Australasian songbirds. Evolution 71, 2120–2129 (2017).PubMed 
Article 

Google Scholar 
Sheard, C. et al. Ecological drivers of global gradients in avian dispersal inferred from wing morphology. Nat. Commun. 11, 1–9 (2020).Article 
CAS 

Google Scholar 
Rabosky, D. L. et al. BAMM tools: an R package for the analysis of evolutionary dynamics on phylogenetic trees. Methods Ecol. Evol. 5, 701–707 (2014).Article 

Google Scholar 
Thomas, G. H. & Freckleton, R. P. MOTMOT: models of trait macroevolution on trees. Methods Ecol. Evol. 3, 145–151 (2012).CAS 
Article 

Google Scholar 
O’Meara, B. C., Ané, C., Sanderson, M. J. & Wainwright, P. C. Testing for different rates of continuous trait evolution using likelihood. Evolution 60, 922–933 (2006).PubMed 
Article 

Google Scholar 
Harmon, L. J., Schulte, J. A., Larson, A. & Losos, J. B. Tempo and mode of evolutionary radiation in iguanian lizards. Science 301, 961–964 (2003).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Slater, G. J., Price, S. A., Santini, F. & Alfaro, M. E. Diversity versus disparity and the radiation of modern cetaceans. Proc. R. Soc. B Biol. Sci. 277, 3097–3104 (2010).Article 

Google Scholar 
Sullivan, B. L. et al. eBird: A citizen-based bird observation network in the biological sciences. Biol. Conserv. 142, 2282–2292 (2009).Article 

Google Scholar 
Broennimann, O. et al. Measuring ecological niche overlap from occurrence and spatial environmental data. Glob. Ecol. Biogeogr. 21, 481–497 (2012).Article 

Google Scholar 
Heinrich, B. Ravens in Winter (Simon and Schuster, 2014).Taylor, A. H., Hunt, G. R., Medina, F. S. & Gray, R. D. Do new Caledonian crows solve physical problems through causal reasoning? Proc. R. Soc. B Biol. Sci. 276, 247–254 (2009).CAS 
Article 

Google Scholar 
Lefebvre, L., Reader, S. M. & Sol, D. Brains, innovations and evolution in birds and primates. Brain. Behav. Evol. 63, 233–246 (2004).PubMed 
Article 

Google Scholar 
Rensch, B. Increase of learning capability with increase of brain-size. Am. Nat. 90, 81–95 (1956).Article 

Google Scholar 
Roth, T. C., LaDage, L. D., Freas, C. A. & Pravosudov, V. V. Variation in memory and the hippocampus across populations from different climates: a common garden approach. Proc. R. Soc. B Biol. Sci. 279, 402–410 (2012).Article 

Google Scholar 
Olkowicz, S. et al. Birds have primate-like numbers of neurons in the forebrain. Proc. Natl Acad. Sci. USA 113, 7255–7260 (2016).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Sayol, F., Lefebvre, L. & Sol, D. Relative brain size and its relation with the associative pallium in birds. Brain. Behav. Evol. 87, 69–77 (2016).PubMed 
Article 

Google Scholar 
Garcia-Porta, J. & Ord, T. J. Key innovations and island colonization as engines of evolutionary diversification: a comparative test with the Australasian diplodactyloid geckos. J. Evol. Biol. 26, 2662–2680 (2013).Losos, J. B. & Ricklefs, R. E. Adaptation and diversification on islands. Nature 457, 830–836 (2009).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Stuart, Y. E. & Losos, J. B. Ecological character displacement: glass half full or half empty? Trends Ecol. Evol. 28, 402–408 (2013).PubMed 
Article 

Google Scholar 
Jenkins, D. G. et al. Does size matter for dispersal distance? Glob. Ecol. Biogeogr. 16, 415–425 (2007).Article 

Google Scholar 
Sol, D. et al. Evolutionary divergence in brain size between migratory and resident birds. PLoS ONE 5, e9617 (2010).Ducatez, S., Sol, D., Sayol, F. & Lefebvre, L. Behavioural plasticity is associated with reduced extinction risk in birds. Nat. Ecol. Evol. 4, 788–793 (2020).PubMed 
Article 

Google Scholar 
Sayol, F., Sol, D. & Pigot, A. L. Brain size and life history interact to predict urban tolerance in birds. Front. Ecol. Evol. 8, 58 (2020).Article 

Google Scholar 
Baltensperger, A. P. et al. Seasonal observations and machine-learning-based spatial model predictions for the common raven (Corvus corax) in the urban, sub-arctic environment of Fairbanks, Alaska. Polar Biol. 36, 1587–1599 (2013).Article 

Google Scholar 
Kövér, L. et al. Recent colonization and nest site selection of the Hooded Crow (Corvus corone cornix L.) in an urban environment. Landsc. Urban Plan. 133, 78–86 (2015).Article 

Google Scholar 
Oostra, V., Saastamoinen, M., Zwaan, B. J. & Wheat, C. W. Strong phenotypic plasticity limits potential for evolutionary responses to climate change. Nat. Commun. 9, 1–11 (2018).CAS 
Article 

Google Scholar 
Dukas, R. & Ratcliffe, J. M. Cognitive Ecology II (University of Chicago Press, 2009).Huey, R. B., Hertz, P. E. & Sinervo, B. Behavioral drive versus behavioral inertia in evolution: a null model approach. Am. Nat. 161, 357–366 (2003).PubMed 
Article 

Google Scholar 
Fox, R. J., Donelson, J. M., Schunter, C., Ravasi, T. & Gaitán-Espitia, J. D. Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. Philos. Trans. R. Soc. Lond. B Biol. Sci. 374, 20180174 (2019).Aboitiz, F. Behavior, body types and the irreversibility of evolution. Acta Biotheor. 38, 91–101 (1990).Wcislo, W. T. Behavioral environments and evolutionary change. Annu. Rev. Ecol. Syst. 20, 137–169 (1989).Article 

Google Scholar 
Sol, D., Stirling, D. G. & Lefebvre, L. Behavioral drive or behavioral inhibition in evolution: subspecific diversification in Holarctic passerines. Evolution 59, 2669–2677 (2005).PubMed 
Article 

Google Scholar 
Mayr, E., Mayr, E., Mayr, E. & Mayr, E. Animal Species and Evolution Vol. 797 (Belknap Press of Harvard University Press, 1963).Mayr, E. The emergence of evolutionary novelties. Evol. Darwin 1, 349–380 (1960).
Google Scholar 
Hardy, A. C. The Living Stream: Evolution and Man (Harper & Row, 1967).Wyles, J. S., Kunkel, J. G. & Wilson, A. C. Birds, behavior, and anatomical evolution. Proc. Natl Acad. Sci. USA 80, 4394–4397 (1983).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Plotkin, H. C. The Role of Behavior in Evolution (MIT press, 1988).Lande, R. Models of speciation by sexual selection on polygenic traits. Proc. Natl Acad. Sci. USA 78, 3721–3725 (1981).ADS 
MathSciNet 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
West-Eberhard, M. J. Phenotypic plasticity and the origins of diversity. Annu. Rev. Ecol. Syst. 20, 249–278 (1989).Article 

Google Scholar 
Sol, D. & Price, T. D. Brain size and the diversification of body size in birds. Am. Nat. 172, 170–177 (2008).PubMed 
Article 

Google Scholar 
Sayol, F., Lapiedra, O., Ducatez, S. & Sol, D. Larger brains spur species diversification in birds. Evolution 73, 2085–2093 (2019).PubMed 
Article 

Google Scholar 
Abascal, F., Zardoya, R. & Telford, M. J. TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res. 38, W7–W13 (2010).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Bouckaert, R. et al. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10, e1003537 (2014).Bouckaert, R., Alvarado-Mora, M. V. & Pinho, J. R., others. Evolutionary rates and HBV: issues of rate estimation with Bayesian molecular methods. Antivir. Ther. 18, 497–503 (2013).PubMed 
Article 

Google Scholar 
Rambaut, A. & Drummond, A. J. Tracer v1. 4. (2007).Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E. & Challenger, W. GEIGER: investigating evolutionary radiations. Bioinformatics 24, 129–131 (2008).CAS 
PubMed 
Article 

Google Scholar 
Louca, S. & Louca, M. S. Package ‘castor’. (2017).Rasband, W. S. et al. ImageJ. (1997).Rohlf, F. J. & Slice, D. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst. Biol. 39, 40–59 (1990).
Google Scholar 
Adams, D. C. & Otárola-Castillo, E. geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4, 393–399 (2013).Article 

Google Scholar 
Adams, D. C., Collyer, M., Kaliontzopoulou, A. & Sherratt, E. Geomorph: software for geometric morphometric analyses. (2016).Chira, A. M. & Thomas, G. H. The impact of rate heterogeneity on inference of phylogenetic models of trait evolution. J. Evol. Biol. 29, 2502–2518 (2016).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Rodríguez Casal, A. & Pateiro López, B. Generalizing the convex hull of a sample: the R package alphahull. J. Stat. Softw. 34, 1–28 (2010).Zelditch, M. L., Swiderski, D. L. & Sheets, H. D. Geometric Morphometrics for Biologists: A Primer (Academic Press, 2012).Clavel, J. & Morlon, H. Reliable phylogenetic regressions for multivariate comparative data: illustration with the MANOVA and application to the effect of diet on mandible morphology in Phyllostomid bats. Syst. Biol. 69, 927–943 (2020).CAS 
PubMed 
Article 

Google Scholar 
Dujardin, J.-P., Le Pont, F. & Baylac, M. Geographical versus interspecific differentiation of sand flies (Diptera: Psychodidae): a landmark data analysis. Bull. Entomol. Res. 93, 87–90 (2003).PubMed 
Article 

Google Scholar 
Sidlauskas, B. Continuous and arrested morphological diversification in sister clades of characiform fishes: a phylomorphospace approach. Evolution 62, 3135–3156 (2008).PubMed 
Article 

Google Scholar 
Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).Article 

Google Scholar 
International, B. BirdLife International and handbook of the birds of the world (2017) Bird species distribution maps of the world. (2017).Callaghan, C. T., Nakagawa, S. & Cornwell, W. K. Global abundance estimates for 9,700 bird species. Proc. Natl. Acad. Sci. USA 118, e2023170118 (2021).Hijmans, R. & van Etten, J. raster: raster: geographic data analysis and modeling. R. Packag. version 517, 2 (2014).
Google Scholar 
Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).Article 

Google Scholar 
Dray, S. & Dufour, A.-B., others. The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22, 1–20 (2007).Article 

Google Scholar 
Ho, L. S. T. et al. Package ‘phylolm’. (2018).Akaike, H. Selected Papers of Hirotugu Akaike (Springer, 1998).Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).CAS 
PubMed 
Article 

Google Scholar  More

A summary describing all plant architecture, flower, fruit, and yield, and phenological traits for each of the thirteen Phaseolus sp. and Vigna sp. landraces in the open field and the greenhouse conditions is provided in Supporting Tables S3, S4 and S5. Main effects Kruskal–Wallis tests are summarised in Table 1, and the interactions between treatment conditions (open field and greenhouse) and species, and landrace and climatic background are summarised in Table 2.Table 1 Main effects Kruskal–Wallis H tests for treatment (open field vs greenhouse conditions), species, landrace, and climatic background of the landraces.Full size tableTable 2 Kruskal–Wallis H tests for the interactions between treatment (open field and greenhouse) and species, landrace, or the climatic background.Full size tableI. Plant architecturePlants under high temperatures and low humidity in the greenhouse exhibited significant higher overall mean rank values than field plants for stem diameter, the degree of branch orientation, composite sheet length and width, and the terminal leaflet length. The size of the angle of the base of the terminal leaflet, however, was bigger in the field (Supporting Tables S3 and Table 1). There were overall significant differences for species and landrace for all studied characters (Table 1). The Kruskal–Wallis analyses of the interactions between treatment (open field vs greenhouse conditions) and species, climatic background, and landrace were significant for all the traits (p-value  More

Beerda, B., Schilder, M. B. H., Van Hooff, J. A., De Vries, H. W. & Mol, J. A. Chronic stress in dogs subjected to social and spatial restriction I. Behavioral responses. Physiol. Behav. 66, 233–242 (1999).CAS 
PubMed 
Article 

Google Scholar 
Rooney, N. J., Gaines, S. A. & Bradshaw, J. W. Behavioural and glucocorticoid responses of dogs (Canis familiaris) to kennelling: investigating mitigation of stress by prior habituation. Physiol. Behav. 92, 847–854. https://doi.org/10.1016/j.physbeh.2007.06.011 (2007).CAS 
PubMed 
Article 

Google Scholar 
Stephen, J. M. & Ledger, R. A. A longitudinal evaluation of urinary cortisol in kennelled dogs Canis familiaris. Physiol. Behav. 87, 911–916. https://doi.org/10.1016/j.physbeh.2006.02.015 (2006).CAS 
PubMed 
Article 

Google Scholar 
Mills, D., Karagiannis, C., Zulch, H. Stress its effects on health and behavior. Vet. Clin. North Am. Small Anim. Pract. 44, 525–541 (2014).Mormède, P. et al. Exploration of the hypothalamic–pituitary–adrenal function as a tool to evaluate animal welfare. Physiol. Behav. 92, 317–339 (2007).PubMed 
Article 

Google Scholar 
Hennessy, M. B. Using hypothalamic–pituitary–adrenal measures for assessing and reducing the stress of dogs in shelters: A review. Appl. Anim. Behav. Sci. 149, 1–12 (2013).Article 

Google Scholar 
Cobb, M. L., Iskandarani, K., Chinchilli, V. M. & Dreschel, N. A. A systematic review and meta-analysis of salivary cortisol measurement in domestic canines. Domest. Anim. Endocrinol. 57, 31–42 (2016).CAS 
PubMed 
Article 

Google Scholar 
Wester, V. L. & van Rossum, E. F. Clinical applications of cortisol measurements in hair. Eur. J. Endocrinol. 173, M1–M10 (2015).CAS 
PubMed 
Article 

Google Scholar 
Heimbürge, S., Kanitz, E. & Otten, W. The use of hair cortisol for the assessment of stress in animals. Gen. Comp. Endocrinol. 270, 10–17 (2019).PubMed 
Article 

Google Scholar 
Meyer, J. S. & Novak, M. A. Minireview: hair cortisol: A novel biomarker of hypothalamic-pituitary-adrenocortical activity. Endocrinology 153, 4120–4127 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Khoury, J. E., Bosquet Enlow, M., Plamondon, A. & Lyons-Ruth, K. The association between adversity and hair cortisol levels in humans: A meta-analysis. Psychoneuroendocrinology 103, 104–117 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Davenport, M. D., Tiefenbacher, S., Lutz, C. K., Novak, M. A. & Meyer, J. S. Analysis of endogenous cortisol concentrations in the hair of rhesus macaques. Gen. Comp. Endocrinol. 147, 255–261 (2006).CAS 
PubMed 
Article 

Google Scholar 
Greff, M. J. E. et al. Hair cortisol analysis: An update on methodological considerations and clinical applications. Clin. Biochem. 63, 1–9 (2019).CAS 
PubMed 
Article 

Google Scholar 
del Rosario, G. et al. Effects of adrenocorticotropic hormone challenge and age on hair cortisol concentrations in dairy cattle. Can. J. Vet. Res. 75, 216–221 (2011).
Google Scholar 
Macbeth, B. J., Cattet, M., Stenhouse, G. B., Gibeau, M. L. & Janz, D. M. Hair cortisol concentration as a noninvasive measure of long-term stress in free-ranging grizzly bears (Ursus arctos): considerations with implications for other wildlife. Can. J. Zool. 88, 935–949 (2010).CAS 
Article 

Google Scholar 
Accorsi, P. A. et al. Cortisol determination in hair and faeces from domestic cats and dogs. Gen. Comp. Endocrinol. 155, 398–402 (2008).CAS 
PubMed 
Article 

Google Scholar 
Bennett, A. & Hayssen, V. Measuring cortisol in hair and saliva from dogs: coat color and pigment differences. Domest. Anim. Endocrinol. 39, 171–180 (2010).CAS 
PubMed 
Article 

Google Scholar 
Bryan, H. M., Adams, A. G., Invik, R. M., Wynne-Edwards, K. E. & Smits, J. E. Hair as a meaningful measure of baseline cortisol levels over time in dogs. J. Am. Assoc. Lab. Anim. Sci. 52, 189–196 (2013).CAS 
PubMed 
PubMed Central 

Google Scholar 
Siniscalchi, M., McFarlane, J. R., Kauter, K. G., Quaranta, A. & Rogers, L. J. Cortisol levels in hair reflect behavioural reactivity of dogs to acoustic stimuli. Res. Vet. Sci. 94, 49–54 (2013).CAS 
PubMed 
Article 

Google Scholar 
Stella, J., Shreyer, T., Ha, J. & Croney, C. Improving canine welfare in commercial breeding (CB) operations: Evaluating rehoming candidates. Appl. Anim. Behav. Sci. 220, 104861. https://doi.org/10.1016/j.applanim.2019.104861 (2019).Article 

Google Scholar 
Nicholson, S. L. & Meredith, J. E. Should stress management be part of the clinical care provided to chronically ill dogs?. J. Vet. Behav. 10, 489–495 (2015).Article 

Google Scholar 
Maxwell, N., Buchanan, C. & Evans, N. Hair cortisol concentrations, as a measure of chronic activity within the hypothalamic-pituitary-adrenal axis, is elevated in dogs farmed for meat, relative to pet dogs South Korea. Anim. Welf. 28, 389–395 (2019).Article 

Google Scholar 
Roth, L. S., Faresjö, Å, Theodorsson, E., Jensen, P. Hair cortisol varies with season and lifestyle and relates to human interactions in German shepherd dogs. Sci. Rep. 6, 19631; https://doi.org/10.1038/srep19631 (2016).Packer, R. M. et al. What can we learn from the hair of the dog? Complex effects of endogenous and exogenous stressors on canine hair cortisol. PLoS ONE 14, e0216000. https://doi.org/10.1371/journal.pone.0216000 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Sundman, A. et al. Long-term stress levels are synchronized in dogs and their owners. Sci. Rep. 9, 7391; https://doi.org/10.1038/s41598-019-43851-x (2019).Höglin, A. et al. Long-term stress in dogs is related to the human-dog relationship and personality traits. Sci. Rep. 11, 8612; https://doi.org/10.1038/s41598-021-88201-y (2021).Bowland, G. B. et al. Fur color and nutritional status predict hair cortisol concentrations of dogs in Nicaragua. Front. Vet. Sci. 7, 565346. https://doi.org/10.3389/fvets.2020.565346 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
Veronesi, M. C. et al. Coat and claws as new matrices for noninvasive long-term cortisol assessment in dogs from birth up to 30 days of age. Theriogenology 84, 791–796 (2015).CAS 
PubMed 
Article 

Google Scholar 
Davenport, M. D., Lutz, C. K., Tiefenbacher, S., Novak, M. A. & Meyer, J. S. A rhesus monkey model of self-injury: Effects of relocation stress on behavior and neuroendocrine function. Biol. Psychiatry 63, 990–996 (2008).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
van der Laan, J. E., Vinke, C. M., van der Borg, J. A. M. & Arndt, S. S. Restless nights? Nocturnal activity as a useful indicator of adaptability of shelter housed dogs. Appl. Anim. Behav. Sci. 241, 105377. https://doi.org/10.1016/j.applanim.2021.105377 (2021).Article 

Google Scholar 
Pollinger, J. P. et al. Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 464, 898–902 (2010).ADS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Voith, V. L., Ingram, E., Mitsouras, K. & Irizarry, K. Comparison of adoption agency breed identification and DNA breed identification of dogs. J. Appl. Anim. Welf. Sci. 12, 253–262 (2009).CAS 
PubMed 
Article 

Google Scholar 
Gunter, L. M., Barber, R. T. & Wynne, C. D. L. A canine identity crisis: Genetic breed heritage testing of shelter dogs. PLoS ONE 13, e0202633. https://doi.org/10.1371/journal.pone.0202633 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Pinheiro, J., Bates, D., DebRoy, S. & Sarkar, D., R Core Team. Nlme: linear and nonlinear mixed effects models. R package version 3. 1–148 (2020).Protopopova, A. & Gunter, L. Adoption and relinquishment interventions at the animal shelter: a review. Anim. Welf. 26, 35–48 (2017).Article 

Google Scholar 
Müntener, T., Doherr, M. G., Guscetti, F., Suter, M. M. & Welle, M. M. The canine hair cycle – a guide for the assessment of morphological and immunohistochemical criteria. Vet. Dermatol. 22, 383–395 (2011).PubMed 
Article 

Google Scholar 
Wennig, R. Potential problems with the interpretation of hair analysis results. Forensic Sci. Int. 107, 5–12 (2000).CAS 
PubMed 
Article 

Google Scholar 
Heimbürge, S., Kanitz, E., Tuchscherer, A. & Otten, W. Within a hair’s breadth – Factors influencing hair cortisol levels in pigs and cattle. Gen. Comp. Endocrinol. 288, 113359. https://doi.org/10.1016/j.ygcen.2019.113359 (2020).CAS 
PubMed 
Article 

Google Scholar 
Diaz, S. F., Torres, S. M., Dunstan, R. W. & Lekcharoensuk, C. An analysis of canine hair re-growth after clipping for a surgical procedure. Vet. Dermatol. 15, 25–30 (2004).PubMed 
Article 

Google Scholar 
Zeugswetter, F., Bydzovsky, N., Kampner, D. & Schwendenwein, I. Tailored reference limits for urine corticoid:creatinine ratio in dogs to answer distinct clinical questions. Vet. Rec. 167, 997–1001 (2010).CAS 
PubMed 
Article 

Google Scholar 
Jones, S. et al. Use of accelerometers to measure stress levels in shelter dogs. J. Appl. Anim. Welf. Sci. 17, 18–28 (2014).CAS 
PubMed 
Article 

Google Scholar 
Gunter, L. M., Feuerbacher, E. N., Gilchrist, R. J. & Wynne, C. D. Evaluating the effects of a temporary fostering program on shelter dog welfare. PeerJ 7, e6620. https://doi.org/10.7717/peerj.6620 (2019).PubMed 
PubMed Central 
Article 

Google Scholar 
Van den Brom, W. E. & Biewenga, W. J. Assessment of glomerular filtration rate in normal dogs: analysis of the 51Cr-EDTA clearance and its relation to several endogenous parameters of glomerular filtration. Res. Vet. Sci. 30, 152–157 (1981).PubMed 
Article 

Google Scholar 
Sandri, M., Colussi, A., Perrotta, M. G. & Stefanon, B. Salivary cortisol concentration in healthy dogs is affected by size, sex, and housing context. J. Vet. Behav. 10, 302–306 (2015).Article 

Google Scholar 
Haase, C. G., Long, A. K. & Gillooly, J. F. Energetics of stress: linking plasma cortisol levels to metabolic rate in mammals. Biol. Lett. 12, 20150867. https://doi.org/10.1098/rsbl.2015.0867 (2016).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Garnier, F., Benoit, E., Virat, M., Ochoa, R. & Delatour, P. Adrenal cortical response in clinically normal dogs before and after adaptation to a housing environment. Lab. Anim. 24, 40–43 (1990).CAS 
PubMed 
Article 

Google Scholar 
Beerda, B. et al. Chronic stress in dogs subjected to social and spatial restriction. II. Hormonal and immunological responses. Physiol. Behav. 66, 243–254 (1999).Rincón-Cortés, M., Herman, J. P., Lupien, S., Maguire, J. & Shansky, R. M. Stress: Influence of sex, reproductive status and gender. Neurobiol. Stress 10, 100155. https://doi.org/10.1016/j.ynstr.2019.100155 (2019).PubMed 
PubMed Central 
Article 

Google Scholar 
Oyola, M. G. & Handa, R. J. Hypothalamic–pituitary–adrenal and hypothalamic–pituitary–gonadal axes: sex differences in regulation of stress responsivity. Stress 20, 476–494 (2017).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Willen, R. M., Mutwill, A., MacDonald, L. J., Schiml, P. A. & Hennessy, M. B. Factors determining the effects of human interaction on the cortisol levels of shelter dogs. Appl. Anim. Behav. Sci. 186, 41–48 (2017).Article 

Google Scholar 
Protopopova, A. Effects of sheltering on physiology, immune function, behavior, and the welfare of dogs. Physiol. Behav. 159, 95–103 (2016).CAS 
PubMed 
Article 

Google Scholar 
Mesarcova, L., Kottferova, J., Skurkova, L., Leskova, L. & Kmecova, N. Analysis of cortisol in dog hair-a potential biomarker of chronic stress: a review. Vet. Med. (Praha) 62, 363–376 (2017).CAS 
Article 

Google Scholar 
Neumann, A. et al. Predicting hair cortisol levels with hair pigmentation genes: a possible hair pigmentation bias. Sci. Rep. 7, 8529 (2017).ADS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Romero, L. M. & Beattie, U. K. Common myths of glucocorticoid function in ecology and conservation. J. Exp. Zool. A. Ecol. Integr. Physiol. https://doi.org/10.1002/jez.2459 (2021).PubMed 
Article 

Google Scholar 
Heimbürge, S., Kanitz, E., Tuchscherer, A. & Otten, W. Is it getting in the hair? – Cortisol concentrations in native, regrown and segmented hairs of cattle and pigs after repeated ACTH administrations. Gen. Comp. Endocrinol. 295, 113534. https://doi.org/10.1016/j.ygcen.2020.113534 (2020).CAS 
PubMed 
Article 

Google Scholar 
Van Ockenburg, S. L. et al. The relationship between 63 days of 24-h urinary free cortisol and hair cortisol levels in 10 healthy individuals. Psychoneuroendocrinology 73, 142–147 (2016).PubMed 
Article 

Google Scholar 
Short, S. J. et al. Correspondence between hair cortisol concentrations and 30-day integrated daily salivary and weekly urinary cortisol measures. Psychoneuroendocrinology 71, 12–18 (2016).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Mack, Z. & Fokidis, H. B. A novel method for assessing chronic cortisol concentrations in dogs using the nail as a source. Domest. Anim. Endocrinol. 59, 53–57 (2017).CAS 
PubMed 
Article 

Google Scholar  More

Notomi, T. et al. Loop-mediated isothermal amplification of DNA. Nucleic Acids Res. https://doi.org/10.1093/nar/28.12.e63 (2000).Article 

Google Scholar 
Nagamine, K., Hase, T. & Notomi, T. Accelerated reaction by loop-mediated isothermal amplification using loop primers. Mol. Cell. Probes 16, 223–229. https://doi.org/10.1006/mcpr.2002.0415 (2002).CAS 
Article 

Google Scholar 
Nagamine, K., Watanabe, K., Ohtsuka, K., Hase, T. & Notomi, T. Loop-mediated isothermal amplification reaction using a nondenatured template. Clin. Chem. 47, 1742–1743 (2001).CAS 
Article 

Google Scholar 
Thai, H. T. C. et al. Development and evaluation of a novel loop-mediated isothermal amplification method for rapid detection of severe acute respiratory syndrome coronavirus. J. Clin. Microbiol. 42, 1956–1961. https://doi.org/10.1128/jcm.42.5.1956-1961.2004 (2004).CAS 
Article 

Google Scholar 
Geojith, G., Dhanasekaran, S., Chandran, S. P. & Kenneth, J. Efficacy of loop mediated isothermal amplification (LAMP) assay for the laboratory identification of Mycobacterium tuberculosis isolates in a resource limited setting. J. Microbiol. Methods 84, 71–73. https://doi.org/10.1016/j.mimet.2010.10.015 (2011).CAS 
Article 

Google Scholar 
Saengsawang, N. et al. Development of a fluorescent distance-based paper device using loop-mediated isothermal amplification to detect Escherichia coli in urine. Analyst 145, 8077–8086. https://doi.org/10.1039/d0an01306d (2020).CAS 
Article 

Google Scholar 
Yoshikawa, R. et al. Development and evaluation of a rapid and simple diagnostic assay for COVID-19 based on loop-mediated isothermal amplification. Plos Neglect. Trop. Dis. 14, 14. https://doi.org/10.1371/journal.pntd.000885 (2021).Article 

Google Scholar 
Kim, J. et al. Development and evaluation of a multiplex loop-mediated isothermal amplification (LAMP) assay for differentiation of Mycobacterium tuberculosis and non-tuberculosis mycobacterium in clinical samples. PLoS ONE 16, 11. https://doi.org/10.1371/journal.pone.0244753 (2021).CAS 
Article 

Google Scholar 
Hongjaisee, S. et al. Rapid visual detection of hepatitis C virus using a reverse transcription loop-mediated isothermal ampli fi cation assay. Int. J. Infect. Dis. 102, 440–445. https://doi.org/10.1016/j.ijid.2020.10.082 (2021).CAS 
Article 

Google Scholar 
Niessen, L. & Vogel, R. F. Detection of Fusarium graminearum DNA using a loop-mediated isothermal amplification (LAMP) assay. Int. J. Food Microbiol. 140, 183–191. https://doi.org/10.1016/j.ijfoodmicro.2010.03.036 (2010).CAS 
Article 

Google Scholar 
Ren, W. C., Liu, N. & Li, B. H. Development and application of a LAMP method for rapid detection of apple blotch caused by Marssonina coronaria. Crop Prot. 141, 6. https://doi.org/10.1016/j.cropro.2020.105452 (2021).CAS 
Article 

Google Scholar 
Kong, G. H. et al. Detection of Peronophythora litchii on lychee by loop-mediated isothermal amplification assay. Crop Prot. 139, 6. https://doi.org/10.1016/j.cropro.2020.105370 (2021).CAS 
Article 

Google Scholar 
Zhou, Q. J. et al. Simultaneous detection of multiple bacterial and viral aquatic pathogens using a fluorogenic loop-mediated isothermal amplification-based dual-sample microfluidic chip. J. Fish Dis. https://doi.org/10.1111/jfd.13325 (2020).Article 

Google Scholar 
Huang, H. L. et al. Molecular method for rapid detection of the red tide dinoflagellate Karenia mikimotoi in the coastal region of Xiangshan Bay, China. J. Microbiol. Methods 168, 7. https://doi.org/10.1016/j.mimet.2019.105801 (2020).CAS 
Article 

Google Scholar 
Sridapan, T. et al. Rapid detection of Clostridium perfringens in food by loop-mediated isothermal amplification combined with a lateral flow biosensor. PLoS ONE 16, 14. https://doi.org/10.1371/journal.pone.0245144 (2021).CAS 
Article 

Google Scholar 
Xiong, X. et al. Using real time fluorescence loop-mediated isothermal amplification for rapid species authentication of Atlantic salmon (Salmo salar). J. Food Compos. Anal. 95, 7. https://doi.org/10.1016/j.jfca.2020.103659 (2021).CAS 
Article 

Google Scholar 
Huang, C. G., Hsu, J. C., Haymer, D. S., Lin, G. C. & Wu, W. J. Rapid identification of the Mediterranean fruit fly (Diptera: Tephritidae) by loop-mediated isothermal amplification. J. Econ. Entomol. 102, 1239–1246 (2009).CAS 
Article 

Google Scholar 
Ide, T., Kanzaki, N., Ohmura, W. & Okabe, K. Molecular identification of an invasive wood-boring insect Lyctus brunneus (Coleoptera: Bostrichidae: Lyctinae) using frass by loop-mediated isothermal amplification and nested PCR assays. J. Econ. Entomol. 109, 1410–1414. https://doi.org/10.1093/jee/tow030 (2016).CAS 
Article 

Google Scholar 
Stainton, K., Hall, J., Budge, G. E., Boonham, N. & Hodgetts, J. Rapid molecular methods for in-field and laboratory identification of the yellow-legged Asian hornet (Vespa velutina nigrithorax). J. Appl. Entomol. 142, 610–616. https://doi.org/10.1111/jen.12506 (2018).CAS 
Article 

Google Scholar 
Agarwal, A., Cunningham, J. P., Valenzuela, I. & Blacket, M. J. A diagnostic LAMP assay for the destructive grapevine insect pest, phylloxera (Daktulosphaira vitifoliae). Sci. Rep. 10, 10. https://doi.org/10.1038/s41598-020-77928-9 (2020).CAS 
Article 

Google Scholar 
Rizzo, D. et al. Molecular identification of Anoplophora glabripennis (Coleoptera: Cerambycidae) from frass by loop-mediated isothermal amplification. J. Econ. Entomol. 113, 2911–2919. https://doi.org/10.1093/jee/toaa206 (2020).CAS 
Article 

Google Scholar 
Hsieh, C. H., Wang, H. Y., Chen, Y. F. & Ko, C. C. Loop-mediated isothermal amplification for rapid identification of biotypes B and Q of the globally invasive pest Bemisia tabaci, and studying population dynamics. Pest Manag. Sci. 68, 1206–1213. https://doi.org/10.1002/ps.3298 (2012).CAS 
Article 

Google Scholar 
Williams, M. R. et al. Isothermal amplification of environmental DNA (eDNA) for direct field-based monitoring and laboratory confirmation of Dreissena sp. PLoS ONE 12, 18. https://doi.org/10.1371/journal.pone.0186462 (2017).CAS 
Article 

Google Scholar 
Ponting, S., Tomkies, V. & Stainton, K. Rapid identification of the invasive small hive beetle (Aethina tumida) using LAMP. Pest Manag. Sci. 77, 1476–1481. https://doi.org/10.1002/ps.6168 (2020).CAS 
Article 

Google Scholar 
Davis, C. N. et al. Rapid detection of Galba truncatula in water sources on pasture-land using loop-mediated isothermal amplification for control of trematode infections. Parasites Vectors 13, 11. https://doi.org/10.1186/s13071-020-04371-0 (2020).CAS 
Article 

Google Scholar 
Carvalho, J. et al. Faster monitoring of the invasive alien species (IAS) Dreissena polymorpha in river basins through isothermal amplification. Sci. Rep. 11, 10. https://doi.org/10.1038/s41598-021-89574-w (2021).CAS 
Article 

Google Scholar 
Treguier, A. et al. Environmental DNA surveillance for invertebrate species: Advantages and technical limitations to detect invasive crayfish Procambarus clarkii in freshwater ponds. J. Appl. Ecol. 51, 871–879. https://doi.org/10.1111/1365-2664.12262 (2014).CAS 
Article 

Google Scholar 
Cai, W. et al. Using eDNA to detect the distribution and density of invasive crayfish in the Honghe-Hani rice terrace World Heritage site. PLoS ONE https://doi.org/10.1371/journal.pone.0177724 (2017).Article 

Google Scholar 
Wilcox, T. M. et al. Understanding environmental DNA detection probabilities: A case study using a stream-dwelling char Salvelinus fontinalis. Biol. Conserv. 194, 209–216. https://doi.org/10.1016/j.biocon.2015.12.023 (2016).Article 

Google Scholar 
Hunter, M. E., Ferrante, J. A., Meigs-Friend, G. & Ulmer, A. Improving eDNA yield and inhibitor reduction through increased water volumes and multi-filter isolation techniques. Sci. Rep. https://doi.org/10.1038/s41598-019-40977-w (2019).Article 

Google Scholar 
Twardochleb, L. A., Olden, J. D. & Larson, E. R. A global meta-analysis of the ecological impacts of nonnative crayfish. Freshw. Sci. 32, 1367–1382. https://doi.org/10.1899/12-203.1 (2013).Article 

Google Scholar 
Andruszkiewicz, A. E., Zhang, W. G. & Govindarajan, A. F. Environmental DNA shedding and decay rates from diverse animal forms and thermal regimes. Environ. DNA 3, 492–514. https://doi.org/10.1002/edn3.141 (2021).Article 

Google Scholar 
Stedtfeld, R. D. et al. Static self-directed sample dispensing into a series of reaction wells on a microfluidic card for parallel genetic detection of microbial pathogens. Biomed. Microdev. 17, 89. https://doi.org/10.1007/s10544-015-9994-1 (2015).CAS 
Article 

Google Scholar 
Koloren, Z., Sotiriadou, I. & Karanis, P. Investigations and comparative detection of Cryptosporidium species by microscopy, nested PCR and LAMP in water supplies of Ordu, Middle Black Sea, Turkey. Ann. Trop. Med. Parasitol. 105, 607–615. https://doi.org/10.1179/2047773211y.0000000011 (2011).CAS 
Article 

Google Scholar 
Sabike, I. I. et al. Use of direct LAMP screening of broiler fecal samples for Campylobacter jejuni and Campylobacter coli in the positive flock identification strategy. Front. Microbiol. 7, 1582. https://doi.org/10.3389/fmicb.2016.01582 (2016).Article 

Google Scholar 
Gahlawat, S. K., Ellis, A. E. & Collet, B. A sensitive loop-mediated isothermal amplification (LAMP) method for detection of Renibacterium salmoninarum, causative agent of bacterial kidney disease in salmonids. J. Fish Dis. 32, 491–497. https://doi.org/10.1111/j.1365-2761.2009.01005.x (2009).CAS 
Article 

Google Scholar 
Levy, J. et al. Methods for rapid and effective PCR-based detection of ‘Candidatus Liberibacter solanacearum’ from the insect vector Bactericera cockerelli: Streamlining the DNA extraction/purification process. J. Econ. Entomol. 106, 1440–1445. https://doi.org/10.1603/ec12419 (2013).CAS 
Article 

Google Scholar 
Kaneko, H., Kawana, T., Fukushima, E. & Suzutani, T. Tolerance of loop-mediated isothermal amplification to a culture medium and biological substances. J. Biochem. Biophys. Methods 70, 499–501. https://doi.org/10.1016/j.jbbm.2006.08.008 (2007).CAS 
Article 

Google Scholar 
Curtis, A. N., Tiemann, J. S., Douglass, S. A., Davis, M. A. & Larson, E. R. High stream flows dilute environmental DNA (eDNA) concentrations and reduce detectability. Divers. Distrib. 27, 1918–1931. https://doi.org/10.1111/ddi.13196 (2020).Article 

Google Scholar 
Mauvisseau, Q. et al. Environmental DNA as an efficient tool for detecting invasive crayfishes in freshwater ponds. Hydrobiologia 805, 163–175. https://doi.org/10.1007/s10750-017-3288-y (2018).CAS 
Article 

Google Scholar 
RStudioTeam. Boston (ed. PBC) (2020).Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).Book 

Google Scholar  More

Sagan, L. On the origin of mitosing cells. J. Theor. Biol. 14, 255–274 (1967).CAS 
PubMed 
Article 

Google Scholar 
Taylor, F. J. R. Implications and extensions of the serial endosymbiosis theory of the origin of eukaryotes. Taxon 23, 229–258 (1974).Article 

Google Scholar 
Margulis, L. Serial endosymbiotic theory (SET) and composite individuality. Microbiol. Today 31, 172–175 (2004).
Google Scholar 
Mereschkowsky, C. Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol. Centralbl. 25, 593–604 (1905).
Google Scholar 
Wallin, I. E. On the nature of mitochondria. IX. Demonstration of the bacterial nature of mitochondria. Am. J. Anat. 36, 131–149 (1925).Article 

Google Scholar 
Martin, W. F. Physiology, anaerobes, and the origin of mitosing cells 50 years on. J. Theor. Biol. 434, 2–10 (2017).CAS 
PubMed 
Article 

Google Scholar 
Müller, M. et al. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. Rev. 76, 444–495 (2012).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Spang, A. et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521, 173–179 (2015).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Imachi, H. et al. Isolation of an archaeon at the prokaryote–eukaryote interface. Nature 577, 519–525 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Morris, B. E. L., Henneberger, R., Huber, H. & Moissl-Eichinger, C. Microbial syntrophy: interaction for the common good. FEMS Microbiol. Rev. 37, 384–406 (2013).CAS 
PubMed 
Article 

Google Scholar 
Martin, W. & Müller, M. The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41 (1998).CAS 
PubMed 
Article 

Google Scholar 
Moreira, D. & Lopez-Garcia, P. Symbiosis between methanogenic archaea and delta-proteobacteria as the origin of eukaryotes: the syntrophic hypothesis. J. Mol. Evol. 47, 517–530 (1998).CAS 
PubMed 
Article 

Google Scholar 
Sousa, F. L., Neukirchen, S., Allen, J. F., Lane, N. & Martin, W. F. Lokiarchaeon is hydrogen dependent. Nat. Microbiol. 1, 16034 (2016).CAS 
PubMed 
Article 

Google Scholar 
Spang, A. et al. Proposal of the reverse flow model for the origin of the eukaryotic cell based on comparative analyses of Asgard archaeal metabolism. Nat. Microbiol. 4, 1138–1148 (2019).CAS 
PubMed 
Article 

Google Scholar 
López-García, P. & Moreira, D. The syntrophy hypothesis for the origin of eukaryotes revisited. Nat. Microbiol. 5, 655–667 (2020).PubMed 
Article 
CAS 

Google Scholar 
Eme, L., Sharpe, S. C., Brown, M. W. & Roger, A. J. in The Origin and Evolution of Eukaryotes (eds. Keeling, P. J. & Koonin, E. V.) 165–180 (Cold Spring Harbor Perspectives in Biology, 2014).Betts, H. C. et al. Integrated genomic and fossil evidence illuminates life’s early evolution and eukaryote origin. Nat. Ecol. Evol. 2, 1556–1562 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
Porter, S. M. Insights into eukaryogenesis from the fossil record. Interface Focus 10, 20190105 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
Agić, H. in Prebiotic Chemistry and the Origin of Life (eds. Neubeck, A. & McMahon, S.) 255–289 (Springer International, 2021).Lyons, T. W., Reinhard, C. T. & Planavsky, N. J. The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506, 307–315 (2014).CAS 
PubMed 
Article 

Google Scholar 
Lenton, T. M. & Daines, S. J. Biogeochemical transformations in the history of the ocean. Ann. Rev. Mar. Sci. 9, 31–58 (2017).PubMed 
Article 

Google Scholar 
Lenton, T. M. On the use of models in understanding the rise of complex life. Interface Focus 10, 20200018 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
Liu, P. et al. Triple oxygen isotope constraints on atmospheric O2 and biological productivity during the mid-Proterozoic. Proc. Natl Acad. Sci. USA 118, e2105074118 (2021).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Mentel, M. & Martin, W. Energy metabolism among eukaryotic anaerobes in light of Proterozoic ocean chemistry. Philos. Trans. R. Soc. Lond. B 363, 2717–2729 (2008).Article 

Google Scholar 
Zimorski, V., Mentel, M., Tielens, A. G. M. & Martin, W. F. Energy metabolism in anaerobic eukaryotes and Earth’s late oxygenation. Free Radic. Biol. Med. 140, 279–294 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Martin, W. F., Tielens, A. G. M. & Mentel, M. Mitochondria and Anaerobic Energy Metabolism in Eukaryotes: Biochemistry and Evolution (Walter de Gruyter, 2020).Hall, J. B. The nature of the host in the origin of the eukaryote cell. J. Theor. Biol. 38, 413–418 (1973).CAS 
PubMed 
Article 

Google Scholar 
Stanier, R. Y. in Organization and Control in Prokaryotic and Eukaryotic Cells (eds. Charles, H. P. & Knight, B. C. J. G.) vol. 20, 1–38 (Cambridge Univ. Press, 1970).De Duve, C. Origin of mitochondria. Science 182, 85 (1973).PubMed 
Article 

Google Scholar 
Andersson, S. G. & Kurland, C. G. Origins of mitochondria and hydrogenosomes. Curr. Opin. Microbiol. 2, 535–541 (1999).CAS 
PubMed 
Article 

Google Scholar 
Cavalier-Smith, T. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int. J. Syst. Evol. Microbiol. 52, 297–354 (2002).CAS 
PubMed 
Article 

Google Scholar 
de Duve, C. The origin of eukaryotes: a reappraisal. Nat. Rev. Genet. 8, 395–403 (2007).PubMed 
Article 
CAS 

Google Scholar 
Knoll, A. H. & Nowak, M. A. The timetable of evolution. Sci. Adv. 3, e1603076 (2017).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Martin, W. F. & Müller, M. Origin of Mitochondria and Hydrogenosomes (Springer, 2007).Lindmark, D. G. & Müller, M. Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. J. Biol. Chem. 248, 7724–7728 (1973).CAS 
PubMed 
Article 

Google Scholar 
Müller, M. in Origin of Mitochondria and Hydrogenosomes (eds. Martin, W. F. & Müller, M.) 1–10 (Springer, 2007).Zillig, W. et al. Did eukaryotes originate by a fusion event? Endocytobiosis Cell Res. 6, 1–25 (1989).
Google Scholar 
Embley, T. M. & Martin, W. Eukaryotic evolution, changes and challenges. Nature 440, 623–630 (2006).CAS 
PubMed 
Article 

Google Scholar 
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 370, 20140326 (2015).Article 
CAS 

Google Scholar 
Roger, A. J., Muñoz-Gómez, S. A. & Kamikawa, R. The origin and diversification of mitochondria. Curr. Biol. 27, R1177–R1192 (2017).CAS 
PubMed 
Article 

Google Scholar 
Zachar, I. & Szathmáry, E. Breath-giving cooperation: critical review of origin of mitochondria hypotheses. Biol. Direct 12, 19 (2017).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Eme, L., Spang, A., Lombard, J., Stairs, C. W. & Ettema, T. J. G. Archaea and the origin of eukaryotes. Nat. Rev. Microbiol. 15, 711–723 (2018).Article 
CAS 

Google Scholar 
Stairs, C. W. et al. Microbial eukaryotes have adapted to hypoxia by horizontal acquisitions of a gene involved in rhodoquinone biosynthesis. eLife 7, e34292 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
Martin, W. F. Too much eukaryote LGT. Bioessays 39, 1700115 (2017).Article 

Google Scholar 
Leger, M. M., Eme, L., Stairs, C. W. & Roger, A. J. Demystifying eukaryote lateral gene transfer (response to Martin 2017 https://doi.org/10.1002/bies.201700115). Bioessays 40, e1700242 (2018).Martin, W. Mosaic bacterial chromosomes: a challenge en route to a tree of genomes. Bioessays 21, 99–104 (1999).CAS 
PubMed 
Article 

Google Scholar 
Nagies, F. S. P., Brueckner, J., Tria, F. D. K. & Martin, W. F. A spectrum of verticality across genes. PLoS Genet. 16, e1009200 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Guy, L. & Ettema, T. J. G. The archaeal ‘TACK’ superphylum and the origin of eukaryotes. Trends Microbiol. 19, 580–587 (2011).CAS 
PubMed 
Article 

Google Scholar 
Williams, T. A., Foster, P. G., Cox, C. J. & Embley, T. M. An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504, 231–236 (2013).CAS 
PubMed 
Article 

Google Scholar 
McInerney, J. O., O’Connell, M. J. & Pisani, D. The hybrid nature of the Eukaryota and a consilient view of life on Earth. Nat. Rev. Microbiol. 12, 449–455 (2014).CAS 
PubMed 
Article 

Google Scholar 
Raymann, K., Brochier-Armanet, C. & Gribaldo, S. The two-domain tree of life is linked to a new root for the Archaea. Proc. Natl Acad. Sci. USA 112, 6670–6675 (2015).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Williams, T. A., Cox, C. J., Foster, P. G., Szöllősi, G. J. & Embley, T. M. Phylogenomics provides robust support for a two-domains tree of life. Nat. Ecol. Evol. 4, 138–147 (2020).PubMed 
Article 

Google Scholar 
Zaremba-Niedzwiedzka, K. et al. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541, 353–358 (2017).CAS 
PubMed 
Article 

Google Scholar 
López-García, P. & Moreira, D. Cultured Asgard archaea shed light on eukaryogenesis. Cell 181, 232–235 (2020).PubMed 
Article 
CAS 

Google Scholar 
Martin, W. F., Tielens, A. G. M., Mentel, M., Garg, S. G. & Gould, S. B. The physiology of phagocytosis in the context of mitochondrial origin. Microbiol. Mol. Biol. Rev. 81, e00008–17 (2017).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Berkner, L. V. & Marshall, L. C. History of major atmospheric components. Proc. Natl Acad. Sci. USA 53, 1215–1226 (1965).CAS 
PubMed Central 
Article 

Google Scholar 
Stolper, D. A., Revsbech, N. P. & Canfield, D. E. Aerobic growth at nanomolar oxygen concentrations. Proc. Natl Acad. Sci. USA 107, 18755–18760 (2010).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Degli Esposti, M., Mentel, M., Martin, W. & Sousa, F. L. Oxygen reductases in alphaproteobacterial genomes: physiological evolution from low to high oxygen environments. Front. Microbiol. 10, 499 (2019).PubMed 
PubMed Central 
Article 

Google Scholar 
Berg, J. et al. How low can they go? Aerobic respiration by microorganisms under apparent anoxia. FEMS Microbiol. Rev. https://doi.org/10.1093/femsre/fuac006 (2022).Cloud, P. Cosmos, Earth, and Man: A Short History of the Universe (Yale Univ. Press, 1978).Pichler, H. & Riezman, H. Where sterols are required for endocytosis. Biochim. Biophys. Acta 1666, 51–61 (2004).CAS 
PubMed 
Article 

Google Scholar 
Hoshino, Y. & Gaucher, E. A. Evolution of bacterial steroid biosynthesis and its impact on eukaryogenesis. Proc. Natl Acad. Sci. USA 118, e2101276118 (2021).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Waldbauer, J. R., Newman, D. K. & Summons, R. E. Microaerobic steroid biosynthesis and the molecular fossil record of Archean life. Proc. Natl Acad. Sci. USA 108, 13409–13414 (2011).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Valentine, D. L. in Symbiosis: Mechanisms and Model Systems (ed. Seckbach, J.) 147–161 (Springer, 2002).Canfield, D. E. & Thamdrup, B. Towards a consistent classification scheme for geochemical environments, or, why we wish the term ‘suboxic’ would go away. Geobiology 7, 385–392 (2009).CAS 
PubMed 
Article 

Google Scholar 
McInerney, M. J., Sieber, J. R. & Gunsalus, R. P. Syntrophy in anaerobic global carbon cycles. Curr. Opin. Biotechnol. 20, 623–632 (2009).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Schink, B. Synergistic interactions in the microbial world. Antonie Van Leeuwenhoek 81, 257–261 (2002).CAS 
PubMed 
Article 

Google Scholar 
Stams, A. J. M. & Plugge, C. M. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat. Rev. Microbiol. 7, 568–577 (2009).CAS 
PubMed 
Article 

Google Scholar 
Embley, T. M., van der Giezen, M., Horner, D. S., Dyal, P. L. & Foster, P. Mitochondria and hydrogenosomes are two forms of the same fundamental organelle. Philos. Trans. R. Soc. Lond. B 358, 191–201 (2003). discussion 201–2.CAS 
Article 

Google Scholar 
Donoghue, P. C. J. & Purnell, M. A. Distinguishing heat from light in debate over controversial fossils. Bioessays 31, 178–189 (2009).PubMed 
Article 

Google Scholar 
Brocks, J. J., Logan, G. A., Buick, R. & Summons, R. E. Archean molecular fossils and the early rise of eukaryotes. Science 285, 1033–1036 (1999).CAS 
PubMed 
Article 

Google Scholar 
Rasmussen, B., Fletcher, I. R., Brocks, J. J. & Kilburn, M. R. Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455, 1101–1104 (2008).CAS 
PubMed 
Article 

Google Scholar 
French, K. L. et al. Reappraisal of hydrocarbon biomarkers in Archean rocks. Proc. Natl Acad. Sci. USA 112, 5915–5920 (2015).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Brocks, J. J. et al. The rise of algae in Cryogenian oceans and the emergence of animals. Nature 548, 578–581 (2017).CAS 
PubMed 
Article 

Google Scholar 
Hoshino, Y. et al. Cryogenian evolution of stigmasteroid biosynthesis. Sci. Adv. 3, e1700887 (2017).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Bengtson, S. et al. Fungus-like mycelial fossils in 2.4-billion-year-old vesicular basalt. Nat. Ecol. Evol. 1, 141 (2017).PubMed 
Article 

Google Scholar 
Butterfield, N. J. Probable Proterozoic fungi. Paleobiology 31, 165–182 (2005).Article 

Google Scholar 
Butterfield, N. J. Early evolution of the Eukaryota. Palaeontology 58, 5–17 (2015).Article 

Google Scholar 
Berbee, M. L. et al. Genomic and fossil windows into the secret lives of the most ancient fungi. Nat. Rev. Microbiol. 18, 717–730 (2020).CAS 
PubMed 
Article 

Google Scholar 
Lamb, D. M., Awramik, S. M., Chapman, D. J. & Zhu, S. Evidence for eukaryotic diversification in the 1800 million-year-old Changzhougou Formation, North China. Precambrian Res. 173, 93–104 (2009).CAS 
Article 

Google Scholar 
Javaux, E. J., Knoll, A. H. & Walter, M. R. Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412, 66–69 (2001).CAS 
PubMed 
Article 

Google Scholar 
Butterfield, N. J. Modes of pre-Ediacaran multicellularity. Precambrian Res. 173, 201–211 (2009).CAS 
Article 

Google Scholar 
Peng, Y., Bao, H. & Yuan, X. New morphological observations for Paleoproterozoic acritarchs from the Chuanlinggou Formation, North China. Precambrian Res. 168, 223–232 (2009).CAS 
Article 

Google Scholar 
Javaux, E. J. in Origins and Evolution of Life: An Astrobiological Perspective (eds Gargaud, M., López-García, P. & Martin, H.) 414–449 (Cambridge Univ. Press, 2011).Stairs, C. W. & Ettema, T. J. G. The archaeal roots of the eukaryotic dynamic actin cytoskeleton. Curr. Biol. 30, R521–R526 (2020).CAS 
PubMed 
Article 

Google Scholar 
Carlisle, E. M., Jobbins, M., Pankhania, V., Cunningham, J. A. & Donoghue, P. C. J. Experimental taphonomy of organelles and the fossil record of early eukaryote evolution. Sci. Adv. 7, eabe9487 (2021).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Han, T. M. & Runnegar, B. Megascopic eukaryotic algae from the 2.1-billion-year-old negaunee iron-formation, Michigan. Science 257, 232–235 (1992).CAS 
PubMed 
Article 

Google Scholar 
Javaux, E. J. & Lepot, K. The Paleoproterozoic fossil record: implications for the evolution of the biosphere during Earth’s middle-age. Earth-Sci. Rev. 176, 68–86 (2018).CAS 
Article 

Google Scholar 
Agić, H., Moczydłowska, M. & Yin, L. Diversity of organic-walled microfossils from the early Mesoproterozoic Ruyang Group, North China Craton – A window into the early eukaryote evolution. Precambrian Res. 297, 101–130 (2017).Article 
CAS 

Google Scholar 
Pang, K. et al. The nature and origin of nucleus-like intracellular inclusions in Paleoproterozoic eukaryote microfossils. Geobiology 11, 499–510 (2013).CAS 
PubMed 

Google Scholar 
Bengtson, S., Belivanova, V., Rasmussen, B. & Whitehouse, M. The controversial ‘Cambrian’ fossils of the Vindhyan are real but more than a billion years older. Proc. Natl Acad. Sci. USA 106, 7729–7734 (2009).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Bengtson, S., Sallstedt, T., Belivanova, V. & Whitehouse, M. Three-dimensional preservation of cellular and subcellular structures suggests 1.6 billion-year-old crown-group red algae. PLoS Biol. 15, e2000735 (2017).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Tang, Q., Pang, K., Yuan, X. & Xiao, S. A one-billion-year-old multicellular chlorophyte. Nat. Ecol. Evol. 4, 543–549 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
Bykova, N. et al. Seaweeds through time: morphological and ecological analysis of Proterozoic and early Paleozoic benthic macroalgae. Precambrian Res. 350, 105875 (2020).CAS 
Article 

Google Scholar 
Maloney, K. M. et al. New multicellular marine macroalgae from the early Tonian of northwestern Canada. Geology 49, 743–747 (2021).CAS 
Article 

Google Scholar 
Tang, Q. et al. The Proterozoic macrofossil Tawuia as a coenocytic eukaryote and a possible macroalga. Palaeogeogr. Palaeoclimatol. Palaeoecol. 576, 110485 (2021).Article 

Google Scholar 
Sforna, M. C. et al. Intracellular bound chlorophyll residues identify 1 Gyr-old fossils as eukaryotic algae. Nat. Commun. 13, 146 (2022).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Strother, P. K. et al. A possible billion-year-old holozoan with differentiated multicellularity. Curr. Biol. 31, 2658–2665.e2 (2021).CAS 
PubMed 
Article 

Google Scholar 
Loron, C. C. et al. Early fungi from the Proterozoic era in Arctic Canada. Nature 570, 232–235 (2019).CAS 
PubMed 
Article 

Google Scholar 
Bonneville, S. et al. Molecular identification of fungi microfossils in a Neoproterozoic shale rock. Sci. Adv. 6, eaax7599 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Gibson, T. M. et al. Precise age of Bangiomorpha pubescens dates the origin of eukaryotic photosynthesis. Geology 46, 135–138 (2018).CAS 
Article 

Google Scholar 
Butterfield, N. J. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26, 386–404 (2000).Article 

Google Scholar 
Husson, J. M. & Peters, S. E. Nature of the sedimentary rock record and its implications for Earth system evolution. Emerg. Top. Life Sci. 2, 125–136 (2018).CAS 
PubMed 
Article 

Google Scholar 
Donoghue, P. C. J. & Yang, Z. The evolution of methods for establishing evolutionary timescales. Philos. Trans. R. Soc. Lond. B 371, 20160020 (2016).Article 

Google Scholar 
Berney, C. & Pawlowski, J. A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record. Proc. Biol. Sci. 273, 1867–1872 (2006).CAS 
PubMed 
PubMed Central 

Google Scholar 
Chernikova, D., Motamedi, S., Csürös, M., Koonin, E. V. & Rogozin, I. B. A late origin of the extant eukaryotic diversity: divergence time estimates using rare genomic changes. Biol. Direct 6, 26 (2011).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Parfrey, L. W., Lahr, D. J. G., Knoll, A. H. & Katz, L. A. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc. Natl Acad. Sci. USA 108, 13624–13629 (2011).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Shih, P. M. & Matzke, N. J. Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins. Proc. Natl Acad. Sci. USA 110, 12355–12360 (2013).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Canfield, D. E. The early history of atmospheric oxygen: homage to Robert M. Garrels. Annu. Rev. Earth Planet. Sci. 33, 1–36 (2005).CAS 
Article 

Google Scholar 
Kump, L. R. The rise of atmospheric oxygen. Nature 451, 277–278 (2008).CAS 
PubMed 
Article 

Google Scholar 
Holland, H. D. When did the Earth’s atmosphere become oxic? A reply. Geochem. N. 100, 20–22 (1999).
Google Scholar 
Holland, H. D. Volcanic gases, black smokers, and the great oxidation event. Geochim. Cosmochim. Acta 66, 3811–3826 (2002).CAS 
Article 

Google Scholar 
Farquhar, J., Bao, H. & Thiemens, M. Atmospheric influence of Earth’s earliest sulfur cycle. Science 289, 756–759 (2000).CAS 
PubMed 
Article 

Google Scholar 
Poulton, S. W. et al. A 200-million-year delay in permanent atmospheric oxygenation. Nature 592, 232–236 (2021).CAS 
PubMed 
Article 

Google Scholar 
Hodgskiss, M. S. W. & Sperling, E. A. A prolonged, two-step oxygenation of Earth’s early atmosphere: support from confidence intervals. Geology https://doi.org/10.1130/g49385.1 (2021).Article 

Google Scholar 
Fischer, W. W., Hemp, J. & Johnson, J. E. Evolution of oxygenic photosynthesis. Annu. Rev. Earth Planet. Sci. 44, 647–683 (2016).CAS 
Article 

Google Scholar 
Sánchez-Baracaldo, P. & Cardona, T. On the origin of oxygenic photosynthesis and Cyanobacteria. N. Phytol. 225, 1440–1446 (2020).Article 

Google Scholar 
Fournier, G. P. et al. The Archean origin of oxygenic photosynthesis and extant cyanobacterial lineages. Proc. Biol. Sci. 288, 20210675 (2021).CAS 
PubMed 
PubMed Central 

Google Scholar 
Cardona, T., Sánchez-Baracaldo, P., Rutherford, A. W. & Larkum, A. W. Early Archean origin of Photosystem II. Geobiology 17, 127–150 (2019).CAS 
PubMed 
Article 

Google Scholar 
Eigenbrode, J. L. & Freeman, K. H. Late Archean rise of aerobic microbial ecosystems. Proc. Natl Acad. Sci. USA 103, 15759–15764 (2006).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Daines, S. J. & Lenton, T. M. The effect of widespread early aerobic marine ecosystems on methane cycling and the Great Oxidation. Earth Planet. Sci. Lett. 434, 42–51 (2016).CAS 
Article 

Google Scholar 
Crowe, S. A. et al. Atmospheric oxygenation three billion years ago. Nature 501, 535–538 (2013).CAS 
PubMed 
Article 

Google Scholar 
Planavsky, N. J. et al. Evidence for oxygenic photosynthesis half a billion years before the Great Oxidation Event. Nat. Geosci. 7, 283–286 (2014).CAS 
Article 

Google Scholar 
Daye, M. et al. Light-driven anaerobic microbial oxidation of manganese. Nature 576, 311–314 (2019).PubMed 
Article 
CAS 

Google Scholar 
Slotznick, S. P. et al. Reexamination of 2.5-Ga ‘whiff’ of oxygen interval points to anoxic ocean before GOE. Sci. Adv. 8, eabj7190 (2022).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Soo, R. M., Hemp, J., Parks, D. H., Fischer, W. W. & Hugenholtz, P. On the origins of oxygenic photosynthesis and aerobic respiration in Cyanobacteria. Science 355, 1436–1440 (2017).CAS 
PubMed 
Article 

Google Scholar 
Jabłońska, J. & Tawfik, D. S. The evolution of oxygen-utilizing enzymes suggests early biosphere oxygenation. Nat. Ecol. Evol. 5, 442–448 (2021).PubMed 
Article 

Google Scholar 
Mentel, M., Röttger, M., Leys, S., Tielens, A. G. M. & Martin, W. F. Of early animals, anaerobic mitochondria, and a modern sponge. Bioessays 36, 924–932 (2014).PubMed 
Article 

Google Scholar 
Lenton, T. M. et al. Earliest land plants created modern levels of atmospheric oxygen. Proc. Natl Acad. Sci. USA 113, 9704–9709 (2016).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Krause, A. J. et al. Stepwise oxygenation of the Paleozoic atmosphere. Nat. Commun. 9, 4081 (2018).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Daines, S. J., Mills, B. J. W. & Lenton, T. M. Atmospheric oxygen regulation at low Proterozoic levels by incomplete oxidative weathering of sedimentary organic carbon. Nat. Commun. 8, 14379 (2017).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Canfield, D. E. A new model for Proterozoic ocean chemistry. Nature 396, 450–453 (1998).CAS 
Article 

Google Scholar 
Sperling, E. A. et al. Statistical analysis of iron geochemical data suggests limited late Proterozoic oxygenation. Nature 523, 451–454 (2015).CAS 
PubMed 
Article 

Google Scholar 
Planavsky, N. J. et al. Low mid-Proterozoic atmospheric oxygen levels and the delayed rise of animals. Science 346, 635–638 (2014).CAS 
PubMed 
Article 

Google Scholar 
Cole, D. B. et al. A shale-hosted Cr isotope record of low atmospheric oxygen during the Proterozoic. Geology 44, 555–558 (2016).CAS 
Article 

Google Scholar 
Wang, C. et al. Strong evidence for a weakly oxygenated ocean-atmosphere system during the Proterozoic. Proc. Natl Acad. Sci. USA 119, e2116101119 (2022).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Reinhard, C. T., Planavsky, N. J., Olson, S. L., Lyons, T. W. & Erwin, D. H. Earth’s oxygen cycle and the evolution of animal life. Proc. Natl Acad. Sci. USA 113, 8933–8938 (2016).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Poulton, S. W. & Canfield, D. E. Ferruginous conditions: a dominant feature of the ocean through Earth’s history. Elements 7, 107–112 (2011).CAS 
Article 

Google Scholar 
Gilleaudeau, G. J. et al. Uranium isotope evidence for limited euxinia in mid-Proterozoic oceans. Earth Planet. Sci. Lett. 521, 150–157 (2019).CAS 
Article 

Google Scholar 
Cole, D. B. et al. On the co-evolution of surface oxygen levels and animals. Geobiology 319, 55 (2020).
Google Scholar 
Friese, A. et al. Organic matter mineralization in modern and ancient ferruginous sediments. Nat. Commun. 12, 2216 (2021).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Sperling, E. A., Knoll, A. H. & Girguis, P. R. The ecological physiology of Earth’s second oxygen revolution. Annu. Rev. Ecol. Evol. Syst. 46, 215–235 (2015).Article 

Google Scholar 
Knoll, A. H. Paleobiological perspectives on early eukaryotic evolution. Cold Spring Harb. Perspect. Biol. 6, a016121 (2014).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Cohen, P. A. & Kodner, R. B. The earliest history of eukaryotic life: uncovering an evolutionary story through the integration of biological and geological data. Trends Ecol. Evol. https://doi.org/10.1016/j.tree.2021.11.005 (2021).Szathmáry, E. & Smith, J. M. The major evolutionary transitions. Nature 374, 227–232 (1995).PubMed 
Article 

Google Scholar 
Lane, N. & Martin, W. The energetics of genome complexity. Nature 467, 929–934 (2010).CAS 
PubMed 
Article 

Google Scholar 
Theissen, U., Hoffmeister, M., Grieshaber, M. & Martin, W. Single eubacterial origin of eukaryotic sulfide: quinone oxidoreductase, a mitochondrial enzyme conserved from the early evolution of eukaryotes during anoxic and sulfidic times. Mol. Biol. Evol. 20, 1564–1574 (2003).CAS 
PubMed 
Article 

Google Scholar 
Martin, W. et al. Early cell evolution, eukaryotes, anoxia, sulfide, oxygen, fungi first (?), and a tree of genomes revisited. IUBMB Life 55, 193–204 (2003).Gould, S. B. et al. Adaptation to life on land at high O2 via transition from ferredoxin-to NADH-dependent redox balance. Proc. Biol. Sci. 286, 20191491 (2019).CAS 
PubMed 
PubMed Central 

Google Scholar 
Mills, D. B. The origin of phagocytosis in Earth history. Interface Focus 10, 20200019 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
Nguyen, K. et al. Absence of biomarker evidence for early eukaryotic life from the Mesoproterozoic Roper Group: searching across a marine redox gradient in mid-Proterozoic habitability. Geobiology 17, 247–260 (2019).CAS 
PubMed 
Article 

Google Scholar 
Lyons, T. W., Diamond, C. W., Planavsky, N. J., Reinhard, C. T. & Li, C. Oxygenation, life, and the planetary system during Earth’s middle history: an overview. Astrobiology 21, 906–923 (2021).PubMed 
PubMed Central 
Article 

Google Scholar 
Gray, M. W. & Doolittle, W. F. Has the endosymbiont hypothesis been proven? Microbiol. Rev. 46, 1–42 (1982).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Gray, M. W., Burger, G. & Lang, B. F. Mitochondrial evolution. Science 283, 1476–1481 (1999).CAS 
PubMed 
Article 

Google Scholar 
Yang, D., Oyaizu, Y., Oyaizu, H., Olsen, G. J. & Woese, C. R. Mitochondrial origins. Proc. Natl Acad. Sci. USA 82, 4443–4447 (1985).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Woese, C. R. Bacterial evolution. Microbiol. Rev. 51, 221–271 (1987).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Martijn, J., Vosseberg, J., Guy, L., Offre, P. & Ettema, T. J. G. Deep mitochondrial origin outside the sampled alphaproteobacteria. Nature 557, 101–105 (2018).CAS 
PubMed 
Article 

Google Scholar 
Muñoz-Gómez, S. A. et al. Site-and-branch-heterogeneous analyses of an expanded dataset favour mitochondria as sister to known Alphaproteobacteria. Nat. Ecol. Evol. 6, 253–262 (2022).Fan, L. et al. Phylogenetic analyses with systematic taxon sampling show that mitochondria branch within Alphaproteobacteria. Nat. Ecol. Evol. 4, 1213–1219 (2020).PubMed 
Article 

Google Scholar 
Richards, T. A. & van der Giezen, M. Evolution of the Isd11–IscS complex reveals a single α-proteobacterial endosymbiosis for all eukaryotes. Mol. Biol. Evol. 23, 1341–1344 (2006).CAS 
PubMed 
Article 

Google Scholar 
Sapp, J. in Origin of Mitochondria and Hydrogenosomes (eds. Martin, W. F. & Müller, M.) 57–83 (Springer, 2007).Poole, A. M. & Gribaldo, S. Eukaryotic origins: how and when was the mitochondrion acquired? Cold Spring Harb. Perspect. Biol. 6, a015990 (2014).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Cavalier-Smith, T. in Endocytobiology II (eds Schenk, H. E. A. & Schwemmler, W. S.) 1027–1034 (de Gruyter, 1983).Martijn, J. & Ettema, T. J. G. From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell. Biochem. Soc. Trans. 41, 451–457 (2013).CAS 
PubMed 
Article 

Google Scholar 
Canfield, D. E. Oxygen: a Four Billion Year History (Princeton Univ. Press, 2014).Holland, H. D. in Petrologic Studies: a Volume in Honor of A. F. Buddington (eds Engel, A. E. J., James, H. L. & Leonard, B. F.) 447–477 (Geological Society of America, 1962).Cloud, P. E. Jr. Significance of the Gunflint (Precambrian) microflora: photosynthetic oxygen may have had important local effects before becoming a major atmospheric gas. Science 148, 27–35 (1965).PubMed 
Article 

Google Scholar 
Rivera, M. C. & Lake, J. A. The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431, 152–155 (2004).CAS 
PubMed 
Article 

Google Scholar 
Pisani, D., Cotton, J. A. & McInerney, J. O. Supertrees disentangle the chimerical origin of eukaryotic genomes. Mol. Biol. Evol. 24, 1752–1760 (2007).CAS 
PubMed 
Article 

Google Scholar 
Esser, C., Martin, W. & Dagan, T. The origin of mitochondria in light of a fluid prokaryotic chromosome model. Biol. Lett. 3, 180–184 (2007).CAS 
PubMed 
Article 

Google Scholar  More

Azam, F. & Malfatti, F. Microbial structuring of marine ecosystems. Nat. Rev. Microbiol. 5, 782–791 (2007).CAS 
Article 

Google Scholar 
Blackburn, N., Fenchel, T. & Mitchell, J. Microscale nutrient patches in planktonic habitats shown by chemotactic bacteria. Science 282, 2254–2256 (1998).CAS 
Article 

Google Scholar 
Stocker, R. Marine microbes see a sea of gradients. Science 338, 628 (2012).CAS 
Article 

Google Scholar 
Levin, S. A. The problem of pattern and scale in ecology. Ecology 73, 1943–1967 (1992).Article 

Google Scholar 
Azam, F. Microbial control of oceanic carbon flux: the plot thickens. Science 280, 694–696 (1998).CAS 
Article 

Google Scholar 
Strom, S. L. Microbial ecology of ocean biogeochemistry: a community perspective. Science 320, 1043–1045 (2008).CAS 
Article 

Google Scholar 
Sarmento, H. & Gasol, J. M. Use of phytoplankton-derived dissolved organic carbon by different types of bacterioplankton. Env. Microbiol. 14, 2348–2360 (2012).CAS 
Article 

Google Scholar 
Grossart, H.-P., Riemann, L. & Azam, F. Bacterial motility in the sea and its ecological implications. Aquat. Microb. Ecol. 25, 247–258 (2001).Article 

Google Scholar 
Brumley, D. R. et al. Bacteria push the limits of chemotactic precision to navigate dynamic chemical gradients. Proc. Natl Acad. Sci. USA 116, 10792–10797 (2019).CAS 
Article 

Google Scholar 
Fenchel, T. Eppur si muove: many water column bacteria are motile. Aquat. Microb. Ecol. 24, 197–201 (2001).Article 

Google Scholar 
Son, K., Menolascina, F. & Stocker, R. Speed-dependent chemotactic precision in marine bacteria. Proc. Natl Acad. Sci. USA 113, 8624–8629 (2016).CAS 
Article 

Google Scholar 
Fenchel, T. Microbial behavior in a heterogeneous world. Science 296, 1068–1071 (2002).CAS 
Article 

Google Scholar 
Kiørboe, T. & Jackson, G. A. Marine snow, organic solute plumes, and optimal chemosensory behavior of bacteria. Limnol. Oceanogr. 46, 1309–1318 (2001).Article 

Google Scholar 
Lambert, B. S., Fernandez, V. I. & Stocker, R. Motility drives bacterial encounter with particles responsible for carbon export throughout the ocean. Limnol. Oceanogr. Lett. 4, 113–118 (2019).Article 

Google Scholar 
Wadhams, G. H. & Armitage, J. P. Making sense of it all: bacterial chemotaxis. Nat. Rev. Mol. Cell. Biol. 5, 1024–1037 (2004).CAS 
Article 

Google Scholar 
Stocker, R., Seymour, J. R., Samadani, A., Hunt, D. E. & Polz, M. F. Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches. Proc. Natl Acad. Sci. USA 105, 4209–4214 (2008).CAS 
Article 

Google Scholar 
Raina, J.-B., Fernandez, V., Lambert, B., Stocker, R. & Seymour, J. R. The role of microbial motility and chemotaxis in symbiosis. Nat. Rev. Microbiol. 17, 284–294 (2019).CAS 
Article 

Google Scholar 
Seymour, J. R., Amin, S. A., Raina, J.-B. & Stocker, R. Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships. Nat. Microbiol. 2, 17065 (2017).CAS 
Article 

Google Scholar 
Bell, W. & Mitchell, R. Chemotactic and growth responses of marine bacteria to algal extracellular products. Biol. Bull. 143, 265–277 (1972).Article 

Google Scholar 
Smriga, S., Fernandez, V. I., Mitchell, J. G. & Stocker, R. Chemotaxis toward phytoplankton drives organic matter partitioning among marine bacteria. Proc. Natl Acad. Sci. USA 113, 1576–1581 (2016).CAS 
Article 

Google Scholar 
Amin, S. A. et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522, 98–101 (2015).CAS 
Article 

Google Scholar 
Lambert, B. S. et al. A microfluidics-based in situ chemotaxis assay to study the behaviour of aquatic microbial communities. Nat. Microbiol. 2, 1344–1349 (2017).CAS 
Article 

Google Scholar 
Larsen, M. H., Blackburn, N., Larsen, J. L. & Olsen, J. E. Influences of temperature, salinity and starvation on the motility and chemotactic response of Vibrio anguillarum. Microbiology 150, 1283–1290 (2004).CAS 
Article 

Google Scholar 
Rinke, C. et al. Validation of picogram- and femtogram-input DNA libraries for microscale metagenomics. PeerJ 4, e2486 (2016).Article 

Google Scholar 
Becker, J. et al. Closely related phytoplankton species produce similar suites of dissolved organic matter. Front. Microbiol. 5, 111 (2014).Article 

Google Scholar 
Vraspir, J. M. & Butler, A. Chemistry of marine ligands and siderophores. Annu. Rev. Mar. Sci. 1, 43–63 (2009).Article 

Google Scholar 
Tagliabue, A. et al. The integral role of iron in ocean biogeochemistry. Nature 543, 51–59 (2017).CAS 
Article 

Google Scholar 
Hopkinson, B. M. & Morel, F. M. M. The role of siderophores in iron acquisition by photosynthetic marine microorganisms. BioMetals 22, 659–669 (2009).CAS 
Article 

Google Scholar 
Amin, S. A. et al. Photolysis of iron–siderophore chelates promotes bacterial–algal mutualism. Proc. Natl Acad. Sci. USA 106, 17071–17076 (2009).CAS 
Article 

Google Scholar 
Croft, M. T., Lawrence, A. D., Raux-Deery, E., Warren, M. J. & Smith, A. G. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438, 90–93 (2005).CAS 
Article 

Google Scholar 
Helliwell, K. E. The roles of B vitamins in phytoplankton nutrition: new perspectives and prospects. New Phytol. 216, 62–68 (2017).CAS 
Article 

Google Scholar 
Berg, G. Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl. Microbiol. Biotechnol. 84, 11–18 (2009).CAS 
Article 

Google Scholar 
Christie, P. J., Whitaker, N. & González-Rivera, C. Mechanism and structure of the bacterial type IV secretion systems. Biochim. Biophys. Acta 1843, 1578–1591 (2014).CAS 
Article 

Google Scholar 
Preston, G. M. Metropolitan microbes: type III secretion in multihost symbionts. Cell Host Microbe 2, 291–294 (2007).CAS 
Article 

Google Scholar 
Deakin, W. J. & Broughton, W. J. Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat. Rev. Microbiol. 7, 312–320 (2009).CAS 
Article 

Google Scholar 
Luo, H. & Moran, M. A. Evolutionary ecology of the marine Roseobacter clade. Microbiol. Mol. Biol. Rev. 78, 573–587 (2014).Article 

Google Scholar 
Rolland, J. L., Stien, D., Sanchez-Ferandin, S. & Lami, R. Quorum sensing and quorum quenching in the phycosphere of phytoplankton: a case of chemical interactions in ecology. J. Chem. Ecol. 42, 1201–1211 (2016).CAS 
Article 

Google Scholar 
Fei, C. et al. Quorum sensing regulates ‘swim-or-stick’ lifestyle in the phycosphere. Environ. Microbiol. 22, 4761–4778 (2020).CAS 
Article 

Google Scholar 
Landa, M., Burns, A. S., Roth, S. J. & Moran, M. A. Bacterial transcriptome remodeling during sequential co-culture with a marine dinoflagellate and diatom. ISME J. 11, 2677 (2017).CAS 
Article 

Google Scholar 
Rinke, C. et al. A phylogenomic and ecological analysis of the globally abundant Marine Group II archaea (Ca. Poseidoniales ord. nov.). ISME J. 13, 663–675 (2019).CAS 
Article 

Google Scholar 
Fenchel, T. & Blackburn, N. Motile chemosensory behaviour of phagotrophic protists: mechanisms for and efficiency in congregating at food patches. Protist 150, 325–336 (1999).CAS 
Article 

Google Scholar 
Hughes, D. J. et al. Impact of nitrogen availability upon the electron requirement for carbon fixation in Australian coastal phytoplankton communities. 63, 1891–1910 (2018).Sumner, L. W. et al. Proposed minimum reporting standards for chemical analysis. Metabolomics 3, 211–221 (2007).CAS 
Article 

Google Scholar 
Chong, J., Wishart, D. S. & Xia, J. Using MetaboAnalyst 4.0 for comprehensive and integrative metabolomics data analysis. Curr. Protoc. Bioinformatics 68, e86 (2019).Article 

Google Scholar 
Xia, J. & Wishart, D. S. Web-based inference of biological patterns, functions and pathways from metabolomic data using MetaboAnalyst. Nat. Protoc. 6, 743–760 (2011).CAS 
Article 

Google Scholar 
Lambert, B. S. & Raina, J.-B. Fabrication and deployment of the in situ chemotaxis assay (ISCA). protocols.io https://doi.org/10.17504/protocols.io.kztcx6n (2019).Ritchie, R. J. Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth. Res. 89, 27–41 (2006).CAS 
Article 

Google Scholar 
Marie, D., Partensky, F., Jacquet, S. & Vaulot, D. Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl. Environ. Microbiol. 63, 186–193 (1997).CAS 
Article 

Google Scholar 
Bramucci, A. R. et al. Microvolume DNA extraction methods for microscale amplicon and metagenomic studies. ISME Commun. 1, 79 (2021).Article 

Google Scholar 
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).CAS 
Article 

Google Scholar 
Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https://doi.org/10.48550/arXiv.1303.3997 (2013).Boyd, J. A., Woodcroft, B. J. & Tyson, G. W. GraftM: a tool for scalable, phylogenetically informed classification of genes within metagenomes. Nucleic Acids Res. 46, e59 (2018).Article 

Google Scholar 
Kuever, J., Rainey, F. A. & Widdel, F. In Bergey’s Manual of Systematics of Archaea and Bacteria https://doi.org/10.1002/9781118960608.obm00084 (2015).Bianchi, D., Weber, T. S., Kiko, R. & Deutsch, C. Global niche of marine anaerobic metabolisms expanded by particle microenvironments. Nat. Geosci. 11, 263–268 (2018).CAS 
Article 

Google Scholar 
Liu, X. et al. Wide distribution of anaerobic ammonium-oxidizing bacteria in the water column of the South China Sea: implications for their survival strategies. Divers. Distrib. 27, 1893–19003 (2021).Article 

Google Scholar 
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 
Article 

Google Scholar 
Suzek, B. E., Huang, H., McGarvey, P., Mazumder, R. & Wu, C. H. UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics 23, 1282–1288 (2007).CAS 
Article 

Google Scholar 
Kanehisa, M. & Goto, S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 28, 27–30 (2000).CAS 
Article 

Google Scholar 
Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59 (2014).Article 

Google Scholar 
Paulson, J. N., Stine, O. C., Bravo, H. C. & Pop, M. Differential abundance analysis for microbial marker-gene surveys. Nat. Methods 10, 1200 (2013).CAS 
Article 

Google Scholar 
McMurdie, P. J. & Holmes, S. Waste not, want not: why rarefying microbiome data is inadmissible. PLOS Comput. Biol. 10, e1003531 (2014).Article 

Google Scholar 
Berges, J. A., Franklin, D. J. & Harrison, P. J. Evolution of an artificial seawater medium: improvements in enriched seawater, artificial water over the last two decades. J. Phycol. 37, 1138–1145 (2001).Article 

Google Scholar 
Lane, D. In Nucleic Acid Techniques in Bacterial Systematics (eds Stackebrandt, E. & Goodfellow, M.) 115–175 (1991).Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods 13, 581–583 (2016).CAS 
Article 

Google Scholar 
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).Article 

Google Scholar 
Oksanen, J. et al. Package ‘Vegan’ Community Ecology Package Version 2 (2013).Durham, B. P. et al. Sulfonate-based networks between eukaryotic phytoplankton and heterotrophic bacteria in the surface ocean. Nat. Microbiol. 4, 1706–1715 (2019).CAS 
Article 

Google Scholar 
Durham, B. P. et al. Recognition cascade and metabolite transfer in a marine bacteria–phytoplankton model system. Environ. Microbiol. 19, 3500–3513 (2017).CAS 
Article 

Google Scholar 
Durham, B. P. et al. Cryptic carbon and sulfur cycling between surface ocean plankton. Proc. Natl Acad. Sci. USA 112, 453–457 (2015).CAS 
Article 

Google Scholar 
Landa, M. et al. Sulfur metabolites that facilitate oceanic phytoplankton–bacteria carbon flux. ISME J. 13, 2536–2550 (2019).CAS 
Article 

Google Scholar  More

Boyce DG, Lewis MR, Worm B. Global phytoplankton decline over the past century. Nature. 2010;466:591–6.CAS 
Article 

Google Scholar 
Bonachela JA, Klausmeier CA, Edwards KF, Litchman E, Levin SA. The role of phytoplankton diversity in the emergent oceanic stoichiometry. J Plankton Res. 2016;38:1021–35.CAS 
Article 

Google Scholar 
Falkowski PG. The role of phytoplankton photosynthesis in global biogeochemical cycles. Photosynth Res. 1994;39:235–58.CAS 
Article 

Google Scholar 
Longhurst A. Seasonal cycles of pelagic production and consumption. Prog Oceanogr. 1995;36:77–167.Article 

Google Scholar 
Li WKW, Glen Harrison W, Head EJH. Coherent assembly of phytoplankton communities in diverse temperate ocean ecosystems. Proc R Soc B Biol Sci. 2006;273:1953–60.Article 

Google Scholar 
Bolaños LM, Karp-Boss L, Choi CJ, Worden AZ, Graff JR, Haëntjens N, et al. Small phytoplankton dominate western North Atlantic biomass. ISME J. 2020;14:1–12.Article 

Google Scholar 
Buttigieg PL, Fadeev E, Bienhold C, Hehemann L, Offre P, Boetius A. Marine microbes in 4D—using time series observation to assess the dynamics of the ocean microbiome and its links to ocean health. Curr Opin Microbiol. 2018;43:169–85.Article 

Google Scholar 
Hirata T, Aiken J, Hardman-Mountford N, Smyth TJ, Barlow RG. An absorption model to determine phytoplankton size classes from satellite ocean colour. Remote Sens Environ. 2008;112:3153–9.Article 

Google Scholar 
Li WKW, Dickie PM. Monitoring phytoplankton, bacterioplankton, and virioplankton in a coastal inlet (Bedford Basin) by flow cytometry. Cytometry. 2001;44:236–46.CAS 
Article 

Google Scholar 
Karl DM, Lukas R. The Hawaii Ocean Time-series (HOT) program: background, rationale and field implementation. Deep Sea Res Part II Top Stud Oceanogr. 1996;43:129–56.CAS 
Article 

Google Scholar 
Steinberg DK, Carlson CA, Bates NR, Johnson RJ, Michaels AF, Knap AH. Overview of the US JGOFS Bermuda Atlantic Time-series Study (BATS): a decade-scale look at ocean biology and biogeochemistry. Deep Sea Res Part II Top Stud Oceanogr. 2001;48:1405–47.CAS 
Article 

Google Scholar 
Harris R. The L4 time-series: the first 20 years. J Plankton Res. 2010;32:577–83.Article 

Google Scholar 
Hunter-Cevera KR, Neubert MG, Olson RJ, Solow AR, Shalapyonok A, Sosik HM. Physiological and ecological drivers of early spring blooms of a coastal phytoplankter. Science. 2016;354:326–9.CAS 
Article 

Google Scholar 
Shi Q, Wallace D. A 3-year time series of volatile organic iodocarbons in Bedford Basin, Nova Scotia: a northwestern Atlantic fjord. Ocean Sci. 2018;14:1385–403.CAS 
Article 

Google Scholar 
Crawford A, Shore J, Shan S. Measurement of tidal currents using an autonomous underwater vehicle. IEEE J Ocean Eng 2021;1–13.Kerrigan EA, Kienast M, Thomas H, Wallace DWR. Using oxygen isotopes to establish freshwater sources in Bedford Basin, Nova Scotia, a Northwestern Atlantic fjord. Estuar Coast Shelf Sci. 2017;199:96–104.CAS 
Article 

Google Scholar 
Shan S, Sheng J. Examination of circulation, flushing time and dispersion in Halifax Harbour of Nova Scotia. Water Qual Res J. 2012;47:353–74.CAS 
Article 

Google Scholar 
Clayton S, Dutkiewicz S, Jahn O, Follows MJ. Dispersal, eddies, and the diversity of marine phytoplankton. Limnol Oceanogr Fluids Environ. 2013;3:182–97.Article 

Google Scholar 
Barton AD, Dutkiewicz S, Flierl G, Bragg J, Follows MJ. Patterns of diversity in marine phytoplankton. Science. 2010;327:1509–11.CAS 
Article 

Google Scholar 
Dutkiewicz S, Cermeno P, Jahn O, Follows MJ, Hickman AE, Taniguchi DAA, et al. Dimensions of marine phytoplankton diversity. Biogeosciences. 2020;17:609–34.Article 

Google Scholar 
Righetti D, Vogt M, Gruber N, Psomas A, Zimmermann NE. Global pattern of phytoplankton diversity driven by temperature and environmental variability. Sci Adv. 2019;5:eaau6253.Article 

Google Scholar 
Li WKW. Annual average abundance of heterotrophic bacteria and Synechococcus in surface ocean waters. Limnol Oceanogr. 1998;43:1746–53.Article 

Google Scholar 
DFO Canada. AZMP Bulletin PMZA. 2006. DFO.Cullen JJ, Doolittle WF, Levin SA, Li WKW. Patterns and prediction in microbial oceanography. Oceanography. 2007;20:34–46.Article 

Google Scholar 
El‐Swais H, Dunn KA, Bielawski JP, Li WKW, Walsh DA. Seasonal assemblages and short-lived blooms in coastal north-west Atlantic Ocean bacterioplankton. Environ Microbiol. 2015;17:3642–61.Article 

Google Scholar 
Georges AA, El-Swais H, Craig SE, Li WK, Walsh DA. Metaproteomic analysis of a winter to spring succession in coastal northwest Atlantic Ocean microbial plankton. ISME J. 2014;8:1301–13.CAS 
Article 

Google Scholar 
Conover SAM. Nitrogen utilization during spring blooms of marine phytoplankton in Bedford Basin, Nova Scotia, Canada. Mar Biol. 1975;32:247–61.CAS 
Article 

Google Scholar 
Lehman PW. Comparison of chlorophyll a and carotenoid pigments as predictors of phytoplankton biomass. Mar Biol. 1981;65:237–44.CAS 
Article 

Google Scholar 
Siddig AAH, Ellison AM, Ochs A, Villar-Leeman C, Lau MK. How do ecologists select and use indicator species to monitor ecological change? Insights from 14 years of publication in Ecological Indicators. Ecol Indic. 2016;60:223–30.Article 

Google Scholar 
Zorz J, Willis C, Comeau AM, Langille MGI, Johnson CL, Li WKW, et al. Drivers of regional bacterial community structure and diversity in the Northwest Atlantic Ocean. Front Microbiol 2019;10.Comeau AM, Douglas GM, Langille MGI. Microbiome Helper: a custom and streamlined workflow for microbiome research. mSystems. 2017;2:e00127–16.CAS 
Article 

Google Scholar 
Comeau AM, Li WKW, Tremblay J-É, Carmack EC, Lovejoy C. Arctic Ocean microbial community structure before and after the 2007 record sea ice minimum. PLOS ONE. 2011;6:e27492.CAS 
Article 

Google Scholar 
Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18:1403–14.CAS 
Article 

Google Scholar 
Walters W, Hyde ER, Berg-Lyons D, Ackermann G, Humphrey G, Parada A, et al. Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal Internal Transcribed Spacer marker gene primers for microbial community surveys. mSystems. 2015;1:e00009–15.Article 

Google Scholar 
Willis C, Desai D, LaRoche J. Influence of 16S rRNA variable region on perceived diversity of marine microbial communities of the Northern North Atlantic. FEMS Microbiol Lett. 2019;366:1–9.Article 

Google Scholar 
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–7.CAS 
Article 

Google Scholar 
Decelle J, Romac S, Stern RF, Bendif EM, Zingone A, Audic S, et al. PhytoREF: a reference database of the plastidial 16S rRNA gene of photosynthetic eukaryotes with curated taxonomy. Mol Ecol Resour. 2015;15:1435–45.CAS 
Article 

Google Scholar 
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–96.CAS 
Article 

Google Scholar 
NCBI Resource Coordinators. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2018;46:D8–13.Article 

Google Scholar 
R Core Team. R: A language and environment for statistical computing. 2020. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/RStudio Team. RStudio: Integrated Development for R. 2020. RStudio, Inc., Boston, MA. http://www.rstudio.com/.Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10.CAS 
Article 

Google Scholar 
Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL. NCBI BLAST: a better web interface. Nucleic Acids Res. 2008;36:W5–9.CAS 
Article 

Google Scholar 
Cáceres MD, Legendre P. Associations between species and groups of sites: indices and statistical inference. Ecology. 2009;90:3566–74.Article 

Google Scholar 
Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7.CAS 
Article 

Google Scholar 
Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33:1870–4.CAS 
Article 

Google Scholar 
Oksanen J, Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: community ecology package. R package version. 2019;2:5–6. https://CRAN.R-project.org/package=vegan.
Google Scholar 
Wickham H. ggplot2: Elegant graphics for data analysis. 2016. Springer-Verlag, New York.Sohm JA, Ahlgren NA, Thomson ZJ, Williams C, Moffett JW, Saito MA, et al. Co-occurring Synechococcus ecotypes occupy four major oceanic regimes defined by temperature, macronutrients and iron. ISME J. 2016;10:333–45.CAS 
Article 

Google Scholar 
Ahlgren NA, Rocap G. Diversity and distribution of marine Synechococcus: multiple gene phylogenies for consensus classification and development of qPCR assays for sensitive measurement of clades in the ocean. Front Microbiol. 2012;3:1–24.Article 

Google Scholar 
Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K, Salazar G, et al. Structure and function of the global ocean microbiome. Science. 2015;348:1261359.Article 

Google Scholar 
Logares R, Sunagawa S, Salazar G, Cornejo‐Castillo FM, Ferrera I, Sarmento H, et al. Metagenomic 16S rDNA Illumina tags are a powerful alternative to amplicon sequencing to explore diversity and structure of microbial communities. Environ Microbiol. 2014;16:2659–71.CAS 
Article 

Google Scholar 
Faust K, Raes J. CoNet app: inference of biological association networks using Cytoscape. F1000Research. 2016;5:1519.Article 

Google Scholar 
Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, Workman C, et al. Integration of biological networks and gene expression data using Cytoscape. Nat Protoc. 2007;2:2366–82.CAS 
Article 

Google Scholar 
Fuhrman JA, Cram JA, Needham DM. Marine microbial community dynamics and their ecological interpretation. Nat Rev Microbiol. 2015;13:133–46.CAS 
Article 

Google Scholar 
Cram JA, Chow C-ET, Sachdeva R, Needham DM, Parada AE, Steele JA, et al. Seasonal and interannual variability of the marine bacterioplankton community throughout the water column over ten years. ISME J. 2015;9:563–80.Article 

Google Scholar 
Schoemann V, Becquevort S, Stefels J, Rousseau V, Lancelot C. Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J Sea Res. 2005;53:43–66.CAS 
Article 

Google Scholar 
Li W, Dickie P, Spry J. Plankton monitoring programme in the Bedford Basin, 1991-1997. 1998. Canadian Data Report of Fisheries and Aquatic Sciences 1036. Ocean Sciences Division, Maritimes Region, Fisheries and Oceans Canada.Bork P, Bowler C, Vargas C, de, Gorsky G, Karsenti E, Wincker P. Tara Oceans studies plankton at planetary scale. Science. 2015;348:873–873.CAS 
Article 

Google Scholar 
Callahan BJ, McMurdie PJ, Holmes SP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J. 2017;11:2639–43.Article 

Google Scholar 
McLachlan JL, Seguel MR, Fritz L. Tetreutreptia pomquetensis gen. et sp. nov. (Euglenophyceae): a quadriflagellate, phototrophic marine Euglenoid. J Phycol. 1994;30:538–44.Article 

Google Scholar 
Edlund MB, Stoermer EF. Resting spores of the freshwater diatoms Acanthoceras and Urosolenia. J Paleolimnol. 1993;9:55–61.Article 

Google Scholar 
Tomas CR. Marine Phytoplankton: a guide to naked flagellates and coccolithophorids. 2012. Academic Press.Haas S, Robicheau BM, Rakshit S, Tolman J, Algar CK, LaRoche J, et al. Physical mixing in coastal waters controls and decouples nitrification via biomass dilution. Proc Natl Acad Sci. 2021;118:e2004877118.CAS 
Article 

Google Scholar 
Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, et al. The evolution of modern eukaryotic phytoplankton. Science. 2004;305:354–60.CAS 
Article 

Google Scholar 
Needham DM, Sachdeva R, Fuhrman JA. Ecological dynamics and co-occurrence among marine phytoplankton, bacteria and myoviruses shows microdiversity matters. ISME J. 2017;11:1614–29.Article 

Google Scholar 
Choi CJ, Bachy C, Jaeger GS, Poirier C, Sudek L, Sarma VVSS, et al. Newly discovered deep-branching marine plastid lineages are numerically rare but globally distributed. Curr Biol. 2017;27:R15–16.CAS 
Article 

Google Scholar 
Yoo YD, Seong KA, Kim HS, Jeong HJ, Yoon EY, Park J, et al. Feeding and grazing impact by the bloom-forming euglenophyte Eutreptiella eupharyngea on marine eubacteria and cyanobacteria. Harmful Algae. 2018;73:98–109.Article 

Google Scholar 
Dasilva CR, Li WKW, Lovejoy C. Phylogenetic diversity of eukaryotic marine microbial plankton on the Scotian Shelf Northwestern Atlantic Ocean. J Plankton Res. 2014;36:344–63.CAS 
Article 

Google Scholar 
Bolaños LM, Choi CJ, Worden AZ, Baetge N, Carlson CA, Giovannoni SJ. Seasonality of the microbial community composition in the North Atlantic. Front Mar Sci. 2021;8:23.Article 

Google Scholar 
Monier A, Worden AZ, Richards TA. Phylogenetic diversity and biogeography of the Mamiellophyceae lineage of eukaryotic phytoplankton across the oceans. Environ Microbiol Rep. 2016;8:461–9.CAS 
Article 

Google Scholar 
Irion S, Christaki U, Berthelot H, L’Helguen S, Jardillier L. Small phytoplankton contribute greatly to CO2-fixation after the diatom bloom in the Southern Ocean. ISME J. 2021;15:2509–22.CAS 
Article 

Google Scholar 
Choi CJ, Jimenez V, Needham D, Poirier C, Bachy C, Alexander H, et al. Seasonal and geographical transitions in eukaryotic phytoplankton community structure in the Atlantic and Pacific Oceans. Front Microbiol. 2020;11:2187.
Google Scholar 
Leblanc K, Quéguiner B, Diaz F, Cornet V, Michel-Rodriguez M, Durrieu de Madron X, et al. Nanoplanktonic diatoms are globally overlooked but play a role in spring blooms and carbon export. Nat Commun. 2018;9:953.Article 

Google Scholar 
Lundholm N, Hasle GR. Fragilariopsis (Bacillariophyceae) of the Northern Hemisphere – morphology, taxonomy, phylogeny and distribution, with a description of F. pacifica sp. nov. Phycologia. 2010;49:438–60.Article 

Google Scholar 
Martínez-pérez C, Mohr W, Löscher CR, Dekaezemacker J, Littmann S, Yilmaz P, et al. The small unicellular diazotrophic symbiont, UCYN-A, is a key player in the marine nitrogen cycle. Nat Microbiol. 2016;1:16163.Article 

Google Scholar 
Zehr JP, Shilova IN, Farnelid HM, Muñoz-Marín M, del C, Turk-Kubo KA. Unusual marine unicellular symbiosis with the nitrogen-fixing cyanobacterium UCYN-A. Nat Microbiol. 2016;2:1–11.
Google Scholar 
Worden AZ, Janouskovec J, McRose D, Engman A, Welsh RM, Malfatti S, et al. Global distribution of a wild alga revealed by targeted metagenomics. Curr Biol. 2012;22:R675–77.CAS 
Article 

Google Scholar 
Altenburger A, Blossom HE, Garcia-Cuetos L, Jakobsen HH, Carstensen J, Lundholm N, et al. Dimorphism in cryptophytes—The case of Teleaulax amphioxeia/Plagioselmis prolonga and its ecological implications. Sci Adv. 2020;6:eabb1611.CAS 
Article 

Google Scholar 
Kling JD, Lee MD, Fu F, Phan MD, Wang X, Qu P, et al. Transient exposure to novel high temperatures reshapes coastal phytoplankton communities. ISME J. 2020;14:413–24.CAS 
Article 

Google Scholar 
Chassot E, Bonhommeau S, Dulvy NK, Mélin F, Watson R, Gascuel D, et al. Global marine primary production constrains fisheries catches. Ecol Lett. 2010;13:495–505.Article 

Google Scholar 
Gentry RR, Froehlich HE, Grimm D, Kareiva P, Parke M, Rust M, et al. Mapping the global potential for marine aquaculture. Nat Ecol Evol. 2017;1:1317–24.Article 

Google Scholar 
Benway HM, Lorenzoni L, White AE, Fiedler B, Levine NM, Nicholson DP, et al. Ocean time series observations of changing marine ecosystems: an era of integration, synthesis, and societal applications. Front Mar Sci. 2019;6:393.Article 

Google Scholar 
Rigosi A, Fleenor W, Rueda F. State-of-the-art and recent progress in phytoplankton succession modelling. Environ Rev. 2010;18:423–40.Article 

Google Scholar 
Daniels CJ, Poulton AJ, Esposito M, Paulsen ML, Bellerby R, St John M, et al. Phytoplankton dynamics in contrasting early stage North Atlantic spring blooms: composition, succession, and potential drivers. Biogeosciences. 2015;12:2395–409.Article 

Google Scholar 
Masuda Y, Yamanaka Y, Hirata T, Nakano H. Competition and community assemblage dynamics within a phytoplankton functional group: Simulation using an eddy-resolving model to disentangle deterministic and random effects. Ecol Model. 2017;343:1–14.Article 

Google Scholar 
Percopo I, Siano R, Cerino F, Sarno D, Zingone A. Phytoplankton diversity during the spring bloom in the northwestern Mediterranean Sea. Botanica Marina. 2011;54:243–67.Article 

Google Scholar 
Sun J, Liu D. Geometric models for calculating cell biovolume and surface area for phytoplankton. J Plankton Res. 2003;25:1331–46.Article 

Google Scholar 
Agawin N, Duarte C, Agustí S, Vaqué D. Effect of N:P ratios on response of Mediterranean picophytoplankton to experimental nutrient inputs. Aquat Microb Ecol. 2004;34:57–67.Article 

Google Scholar 
Bertilsson S, Berglund O, Karl DM, Chisholm SW. Elemental composition of marine Prochlorococcus and Synechococcus: Implications for the ecological stoichiometry of the sea. Limnology Oceanogr. 2003;48:1721–31.CAS 
Article 

Google Scholar 
Tomas CR. Identifying Marine Phytoplankton. 1997. Elsevier.Harrison PJ, Zingone A, Mickelson MJ, Lehtinen S, Ramaiah N, Kraberg AC, et al. Cell volumes of marine phytoplankton from globally distributed coastal data sets. Estuarine, Coastal Shelf Sci. 2015;162:130–42.CAS 
Article 

Google Scholar 
Guillou L, Chrétiennot-Dinet M-J, Medlin LK, Claustre H, Goër SL, Vaulot D. Bolidomonas: a new genus with two species belonging to a new algal class, the Bolidophyceae (Heterokonta). J Phycol. 1999;35:368–81.Article 

Google Scholar  More

RESEARCH BRIEFINGS
20 April 2022

Protected areas are a cornerstone of conservation policies, but many are not benefiting target species. These areas need to be managed better if they are to achieve conservation goals. More