Ecology

1.
Boyd ES, Amenabar MJ, Poudel S, Templeton AS. Bioenergetic constraints on the origin of autotrophic metabolism. Philos Trans R Soc A. 2020;378:1471–2962.
Article  CAS  Google Scholar 
2.
Boyd ES, Schut GJ, Adams MWW, Peters JW. Hydrogen metabolism and the evolution of biological respiration. Microbe. 2014;9:361–7.
Google Scholar 

3.
Hoehler TM. Biogeochemistry of dihydrogen (H2). In: Sigel H, and Sigel R (eds.). Metal ions in biological systems. Vol 43. (Taylor & Francis Group, Boca Raton, FL, 2005) pp 9-48.

4.
Weiss MC, Sousa FL, Mrnjavac N, Neukirchen S, Roettger M, Nelson-Sathi S, et al. The physiology and habitat of the last universal common ancestor. Nat Microbiol. 2016;1:1–8.
Google Scholar 

5.
McCollom TM, Klein F, Robbins M, Moskowitz B, Berquó TS, Jöns N, et al. Temperature trends for reaction rates, hydrogen generation, and partitioning of iron during experimental serpentinization of olivine. Geochim Cosmochim Acta. 2016;181:175–200.
CAS  Article  Google Scholar 

6.
Schulte M, Blake D, Hoehler T, McCollom T. Serpentinization and its implications for life on the early Earth and Mars. Astrobiology. 2006;6:364–76.
CAS  PubMed  Article  Google Scholar 

7.
Russell M, Hall A, Martin W. Serpentinization as a source of energy at the origin of life. Geobiology. 2010;8:355–71.
CAS  PubMed  Article  Google Scholar 

8.
Seewald JS, Zolotov MY, McCollom T. Experimental investigation of single carbon compounds under hydrothermal conditions. Geochim Cosmochim Acta. 2006;70:446–60.
CAS  Article  Google Scholar 

9.
McCollom TM, Seewald JS. Abiotic synthesis of organic compounds in deep-sea hydrothermal environments. Chem Rev. 2007;107:382–401.
CAS  PubMed  Article  Google Scholar 

10.
Twing KI, Brazelton WJ, Kubo MDY, Hyer AJ, Cardace D, Hoehler TM, et al. Serpentinization-influenced groundwater harbors extremely low diversity microbial communities adapted to high pH. Front Microbiol. 2017;8:308.
PubMed  PubMed Central  Article  Google Scholar 

11.
Brazelton WJ, Nelson B, Schrenk MO. Metagenomic evidence for H2 oxidation and H2 production by serpentinite-hosted subsurface microbial communities. Front Microbiol. 2012;2:268.
PubMed  PubMed Central  Article  Google Scholar 

12.
Morrill PL, Brazelton WJ, Kohl L, Rietze A, Miles SM, Kavanagh H, et al. Investigations of potential microbial methanogenic and carbon monoxide utilization pathways in ultra-basic reducing springs associated with present-day continental serpentinization: the Tablelands, NL, CAN. Front Microbiol. 2014;5:613.
PubMed  PubMed Central  Article  Google Scholar 

13.
Crespo-Medina M, Twing KI, Sánchez-Murillo R, Brazelton WJ, McCollom TM, Schrenk MO. Methane dynamics in a tropical serpentinizing environment: the Santa Elena Ophiolite, Costa Rica. Front Microbiol. 2017;8:916.
PubMed  PubMed Central  Article  Google Scholar 

14.
Woycheese KM, Meyer-Dombard DR, Cardace D, Argayosa AM, Arcilla CA. Out of the dark: transitional subsurface-to-surface microbial diversity in a terrestrial serpentinizing seep (Manleluag, Pangasinan, the Philippines). Front Microbiol. 2015;6:44.
PubMed  PubMed Central  Article  Google Scholar 

15.
Neubeck A, Sun L, Müller B, Ivarsson M, Hosgörmez H, Özcan D, et al. Microbial community structure in a serpentine-hosted abiotic gas seepage at the Chimaera Ophiolite, Turkey. Appl Environ Microbiol. 2017;83:e03430–16.
PubMed  PubMed Central  Article  Google Scholar 

16.
Lang SQ, Früh-Green G, Bernasconi SM, Brazelton WJ, Schrenk MO, McGonigle JM. Deeply-sourced formate fuels sulfate reducers but not methanogens at Lost City hydrothermal field. Sci Rep. 2018;8:1–10.
Article  CAS  Google Scholar 

17.
Brazelton WJ, Morrill PL, Szponar N, Schrenk MO. Bacterial communities associated with subsurface geochemical processes in continental serpentinite springs. Appl Environ Microbiol. 2013;79:3906–16.
CAS  PubMed  PubMed Central  Article  Google Scholar 

18.
Fones EM, Colman DR, Kraus EA, Nothaft DB, Poudel S, Rempfert KR, et al. Physiological adaptations to serpentinization in the Samail Ophiolite, Oman. ISME J. 2019;13:1750–62.
CAS  PubMed  PubMed Central  Article  Google Scholar 

19.
Rempfert KR, Miller HM, Bompard N, Nothaft D, Matter JM, Kelemen P, et al. Geological and geochemical controls on subsurface microbial life in the Samail Ophiolite, Oman. Front Microbiol. 2017;8:56.
PubMed  PubMed Central  Article  Google Scholar 

20.
Kelemen PB, Matter J, Streit EE, Rudge JF, Curry WB, Blusztajn J. Rates and mechanisms of mineral carbonation in peridotite: natural processes and recipes for enhanced, in situ CO2 capture and storage. Annu Rev Earth Planet Sci. 2011;39:545–76.
CAS  Article  Google Scholar 

21.
Canovas PA, Hoehler T, Shock EL. Geochemical bioenergetics during low-temperature serpentinization: an example from the Samail ophiolite, Sultanate of Oman. J Geophys Res. 2017;122:1821–47.
Article  Google Scholar 

22.
Suzuki S, Ishii S, Wu A, Cheung A, Tenney A, Wanger G, et al. Microbial diversity in The Cedars, an ultrabasic, ultrareducing, and low salinity serpentinizing ecosystem. Proc Natl Acad Sci USA. 2013;110:15336–41.
CAS  PubMed  Article  Google Scholar 

23.
Brazelton WJ, Thornton CN, Hyer A, Twing KI, Longino AA, Lang SQ, et al. Metagenomic identification of active methanogens and methanotrophs in serpentinite springs of the Voltri Massif, Italy. Peer J. 2017;5:e2945.
PubMed  Article  CAS  Google Scholar 

24.
Morrill PL, Kuenen JG, Johnson OJ, Suzuki S, Rietze A, Sessions AL, et al. Geochemistry and geobiology of a present-day serpentinization site in California: The Cedars. Geochim Cosmochim Acta. 2013;109:222–40.
CAS  Article  Google Scholar 

25.
Miller HM, Matter JM, Kelemen P, Ellison ET, Conrad ME, Fierer N, et al. Modern water/rock reactions in Oman hyperalkaline peridotite aquifers and implications for microbial habitability. Geochim Cosmochim Acta. 2016;179:217–41.
CAS  Article  Google Scholar 

26.
Russell MJ, Martin W. The rocky roots of the acetyl-CoA pathway. Trends Biochem Sci. 2004;29:358–63.
CAS  PubMed  Article  Google Scholar 

27.
Martin WF, Weiss MC, Neukirchen S, Nelson-Sathi S, Sousa FL. Physiology, phylogeny, and LUCA. Microbial. Cell. 2016;3:582–7.
Google Scholar 

28.
Ueno Y, Yamada K, Yoshida N, Maruyama S, Isozake Y. Evidence from fluid inclusions for microbial methanogenesis in the early Archaean era. Nature. 2006;440:516–9.
CAS  PubMed  Article  Google Scholar 

29.
Moore EK, Jelen BI, Giovannelli D, Raanan H, Falkowski PG. Metal availability and the expanding network of microbial metabolisms in the Archaean eon. Nat Geosci. 2017;10:629–36.
CAS  Article  Google Scholar 

30.
Etiope G, Vadillo I, Whiticar MJ, Marques JM, Carreira PM, Tiago I, et al. Abiotic methane seepage in the Ronda peridotite massif, southern Spain. Appl Geochem. 2016;66:101–13.
CAS  Google Scholar 

31.
Proskurowski G, Lilley MD, Seewald JS, Früh-Green G, Olson EJ, Lupton JE, et al. Abiogenic hydrocarbon production at Lost City hydrothermal field. Science. 2008;319:604–7.
CAS  PubMed  Article  Google Scholar 

32.
Etiope G. Methane origin in the Samail ophiolite: Comment on “Modern water/rock reactions in Oman hyperalkaline peridotite aquifers and implications for microbial habitability”. Geochim Cosmochim Acta. 2017;197:467–70.
CAS  Article  Google Scholar 

33.
Miller HM, Matter JM, Kelemen P, Ellison ET, Conrad ME, Fierer N, et al. Reply to “Methane origin in the Samail ophiolite: Comment on ‘Modern water/rock reactions in Oman hyperalkaline peridotite aquifers and implications for microbial habitability’”. Geochim Cosmochim Acta. 2017;197:471–3.
CAS  Article  Google Scholar 

34.
Miller HM, Chaudhry N, Conrad ME, Markus B, Kopf SH, Templeton AS. Large carbon isotope variability during methanogenesis under alkaline conditions. Geochim Cosmochim Acta. 2018;237:18–31.
CAS  Article  Google Scholar 

35.
Bradley AS, Hayes JM, Summons RE. Extraordinary 13C enrichment of diether lipids at the Lost City Hydrothermal Field indicates a carbon-limited ecosystem. Geochim Cosmochim Acta. 2009;73:102–18.
CAS  Article  Google Scholar 

36.
Zwicker J, Birgel D, Bach W, Richoz S, Smrzka D, Grasemann B, et al. Evidence for archaeal methanogenesis within veins at the onshore serpentinite-hosted Chimaera seeps, Turkey. Chem Geol. 2018;483:567–80.
CAS  Article  Google Scholar 

37.
Kraus EA, Stamps BW, Rempfert KR, Nothaft DB, Boyd ES, Matter JM, et al. Biological methane cycling in serpentinization-impacted fluids of the Samail ophiolite of Oman. AGU Fall Meeting Abstracts. 2018; (abstract #V13E-0139).

38.
Miller HM, Mayhew LE, Ellison ET, Kelemen P, Kubo M, Templeton AS. Low temperature hydrogen production during experimental hydration of partially-serpentinized dunite. Geochim Cosmochim Acta. 2017;209:161–83.
CAS  Article  Google Scholar 

39.
Neal C, Stanger G. Hydrogen generation from mantle source rocks in Oman. Earth Planet Sci Lett. 1983;66:315–20.
CAS  Article  Google Scholar 

40.
Streit E, Kelemen P, Eiler J. Coexisting serpentine and quartz from carbonate-bearing serpentinized peridotite in the Samail Ophiolite, Oman. Contrib Miner Petr. 2012;164:821–37.
CAS  Article  Google Scholar 

41.
Chavagnac V, Monnin C, Ceuleneer G, Boulart C, Hoareau G. Characterization of hyperalkaline fluids produced by low-temperature serpentinization of mantle peridotites in the Oman and Ligurian ophiolites. Geochem Geophys. 2013;14:2496–522.
CAS  Article  Google Scholar 

42.
Mervine EM, Humphris SE, Sims KWW, Kelemen PB, Jenkins WJ. Carbonation rates of peridotite in the Samail Ophiolite, Sultanate of Oman, constrained through 14C dating and stable isotopes. Geochim Cosmochim Acta. 2014;126:371–97.
CAS  Article  Google Scholar 

43.
Kang DWD, Froula J, Egan R, Wang Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ. 2015;3:e1165.
PubMed  PubMed Central  Article  CAS  Google Scholar 

44.
Stepanauskas R, Fergusson EA, Brown J, Poulton NJ, Tupper B, Labonté JM, et al. Improved genome recovery and integrated cell-size analyses of individual uncultured microbial cells and viral particles. Nat Commun. 2017;8:84.
PubMed  PubMed Central  Article  CAS  Google Scholar 

45.
Colman DR, Lindsay MR, Boyd ES. Mixing of meteoric and geothermal fluids supports hyperdiverse chemosynthetic hydrothermal communities. Nat Commun. 2019;10:1–13.
Article  CAS  Google Scholar 

46.
Wu M, Scott AJ. Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2. J Bioinform. 2012;28:1033–4.
CAS  Article  Google Scholar 

47.
Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, et al. Fast, scalable generation of highquality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 2011;7:539.
PubMed  PubMed Central  Article  Google Scholar 

48.
Nguyen LT, Schmidt HA, von Haesler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32:268–74.
CAS  PubMed  PubMed Central  Article  Google Scholar 

49.
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haesler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14:587.
CAS  PubMed  PubMed Central  Article  Google Scholar 

50.
Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 2010;11:119.
Article  CAS  Google Scholar 

51.
Seemann T. Prokka: rapid prokaryotic genome annotation. J Bioinform. 2014;30:2068–9.
CAS  Article  Google Scholar 

52.
Kanehisa M, Goto S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28:27–30.
CAS  PubMed  PubMed Central  Article  Google Scholar 

53.
Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 2007;35:W182–5.
PubMed  PubMed Central  Article  Google Scholar 

54.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10.
CAS  PubMed  PubMed Central  Article  Google Scholar 

55.
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.
CAS  PubMed  PubMed Central  Article  Google Scholar 

56.
Greening C, Biswas A, Carere CR, Jackson CJ, Taylor MC, Stott MB, et al. Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival. ISME J. 2016;10:761–77.
CAS  PubMed  Article  Google Scholar 

57.
Peters JW, Schut GJ, Boyd ES, Mulder DW, Shepard EM, Broderick JB, et al. [FeFe]-and [NiFe]-hydrogenase diversity, mechanism, and maturation. BBA-Mol Cell Res. 2015;1853:1350–69.
CAS  Google Scholar 

58.
Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 2016;45:D200–3.
PubMed  PubMed Central  Article  CAS  Google Scholar 

59.
Marçais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL, Zimin A. MUMmer4: a fast and versatile genome alignment system. PLoS Comput Biol. 2018;14:e1005944.
PubMed  PubMed Central  Article  CAS  Google Scholar 

60.
R Core Team, R: a language and environment for statistical computing. Version 3.0.1. R Foundation for Statistical Computing. 2013.

61.
Leplae R, Lima-Mendez G, Toussaint A. ACLAME: a CLAssification of Mobile genetic Elements, update 2010. Nucleic Acids Res. 2010;38:D57–D61.
CAS  PubMed  Article  Google Scholar 

62.
Lefort V, Longueville J-E, Gascuel O. SMS: smart model selection in PhyML. Mol Biol Evol. 2017;34:2422–4.
CAS  PubMed  PubMed Central  Article  Google Scholar 

63.
Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–21.
CAS  PubMed  Article  Google Scholar 

64.
Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PloS One. 2010;5:e11147.
PubMed  PubMed Central  Article  CAS  Google Scholar 

65.
Harrison KJ, Crécy-Lagard V, Zallot R. Gene Graphics: a genomic neighborhood data visualization web application. J Bioinform. 2018;34:1406–8.
CAS  Article  Google Scholar 

66.
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, and O’Hara RB vegan: community ecology package. R Foundation for Statistical Computing. 2015.

67.
Bowers RM, Kyrpides NC, Stepanauskas R, Harmon-Smith M, Doud D, Reddy TBK, et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat Biotechnol. 2017;25:725–31.
Article  CAS  Google Scholar 

68.
Suzuki S, Ishii S, Hoshino T, Rietze A, Tenney A, Morrill PL, et al. Unusual metabolic diversity of hyperalkaliphilic microbial communities associated with subterranean serpentinization at The Cedars. ISME J. 2017;11:2584–98.
PubMed  PubMed Central  Article  Google Scholar 

69.
Giovannoni SJ, Thrash JC, Temperton B. Implications of streamlining theory for microbial ecology. ISME J. 2014;8:1553–65.
PubMed  PubMed Central  Article  Google Scholar 

70.
Thauer RK, Kaster AK, Seedorf H, Buckel W, Hedderich R. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol. 2008;6:579–91.
CAS  PubMed  Article  Google Scholar 

71.
Hendrickson EL, Leigh JA. Roles of coenzyme F420-reducing hydrogenases and hydrogen-and F420-dependent methylenetetrahydromethanopterin dehydrogenases in reduction of F420 and production of hydrogen during methanogenesis. J Bacteriol. 2008;190:4818–21.
CAS  PubMed  PubMed Central  Article  Google Scholar 

72.
Goldman AD, Leigh JA, Samudrala R. Comprehensive computational analysis of Hmd enzymes and paralogs in methanogenic Archaea. BMC Evol Biol. 2009;9:199.
PubMed  PubMed Central  Article  CAS  Google Scholar 

73.
Tersteegen A, Hedderich R. Methanobacterium thermoautotrophicum encodes two multisubunit membrane‐bound [NiFe] hydrogenases: transcription of the operons and sequence analysis of the deduced proteins. Eur J Biochem. 1999;264:930–43.
CAS  PubMed  Article  Google Scholar 

74.
Lie TJ, Costa KC, Lupa B, Korpole S, Whitman WB, Leigh JA. Essential anaplerotic role for the energy-converting hydrogenase Eha in hydrogenotrophic methanogenesis. Proc Natl Acad Sci USA. 2012;109:15473–8.
CAS  PubMed  Article  Google Scholar 

75.
Thauer RK. The Wolfe cycle comes full circle. Proc Natl Acad Sci USA. 2012;109:15084–5.
CAS  PubMed  Article  Google Scholar 

76.
Costa KC, Wong PM, Wang T, Lie TJ, Dodsworth JA, Swanson I, et al. Protein complexing in a methanogen suggests electron bifurcation and electron delivery from formate to heterodisulfide reductase. Proc Natl Acad Sci USA. 2010;107:11050–5.
CAS  PubMed  Article  Google Scholar 

77.
Greening C, Ahmed FA, Mohamed AE, Lee BM, Pandey G, Warden AC, et al. Physiology, biochemistry, and applications of F420-and Fo-dependent redox reactions. Microbiol Mol Biol Rev. 2016;80:451–93.
CAS  PubMed  PubMed Central  Article  Google Scholar 

78.
Yan Z, Ferry JG. Electron bifurcation and confurcation in methanogenesis and reverse methanogenesis. Front Microbiol. 2018;9:1322.
PubMed  PubMed Central  Article  Google Scholar 

79.
Costa KC, Lie TJ, Xia Q, Leigh JA. VhuD facilitates electron flow from H2 or formate to heterodisulfide reductase in Methanococcus maripaludis. J Bacteriol. 2013;195:5160–5.
CAS  PubMed  PubMed Central  Article  Google Scholar 

80.
Schauer NL, Ferry JG. Properties of formate dehydrogenase in Methanobacterium formicicum. J Bacteriol. 1982;150:1–7.
CAS  PubMed  PubMed Central  Article  Google Scholar 

81.
Schauer NL, Ferry JG, Honek JF, Orme-Johnson WH, Walsh C. Mechanistic studies of the coenzyme F420-reducing formate dehydrogenase from Methanobacterium formicicum. Biochemistry. 1986;25:7163–8.
CAS  PubMed  Article  Google Scholar 

82.
Mills DJ, Vitt S, Strauss M, Shima S, Vonck J. De novo modeling of the F420-reducing [NiFe]-hydrogenase from a methanogenic archaeon by cryo-electron microscopy. Elife. 2013;2:e00218.
PubMed  PubMed Central  Article  Google Scholar 

83.
Schut GJ, Boyd ES, Peters JW, Adams MWW. The modular respiratory complexes involved in hydrogen and sulfur metabolism by heterotrophic hyperthermophilic archaea and their evolutionary implications. FEMS Microbiol Rev. 2013;37:182–203.
CAS  PubMed  Article  Google Scholar 

84.
Hamamoto T, Hashimoto M, Hino M, Kitada M, Seto Y, Kudo T, et al. Characterization of a gene responsible for the Na+/H+ antiporter system of alkalophilic Bacillus species strain C125. Mol Microbiol. 1994;14:939–46.
CAS  PubMed  Article  Google Scholar 

85.
Buckel W, Thauer RK. Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation. BBA-Bioenerg. 2013;1827:94–113.
CAS  Article  Google Scholar 

86.
Boone DR, Johnson RL, Liu Y. Diffusion of the interspecies electron carriers H2 and formate in methanogenic ecosystems and its implications in the measurement of Km for H2 or formate uptake. Appl Environ Microbiol. 1989;55:1735–41.
CAS  PubMed  PubMed Central  Article  Google Scholar 

87.
Suzuki S, Nealson KH, Ishii S. Genomic and in-situ transcriptomic characterization of the candidate phylum NPL-UPL2 from highly alkaline highly reducing serpentinized groundwater. Front Micrbiol. 2018;9:3141.
Article  Google Scholar 

88.
Lang SQ, Butterfield DA, Schulte M, Kelley DS, Lilley MD. Elevated concentrations of formate, acetate and dissolved organic carbon found at the Lost City hydrothermal field. Geochim Cosmochim Acta. 2010;74:941–52.
CAS  Article  Google Scholar 

89.
McCollom TM, Seewald JS. Experimental constraints on the hydrothermal reactivity of organic acids and acid anions: I. Formic acid and formate. Geochim Cosmochim Acta. 2003;67:3625–44.  
CAS  Article  Google Scholar 

90.
Zeng Y, Liu J. Short-chain carboxylates in fluid inclusions in minerals. Appl Geochem. 2000;15:13–25.
CAS  Article  Google Scholar 

91.
Brazelton WJ, Baross JA. Abundant transposases encoded by the metagenome of a hydrothermal chimney biofilm. ISME J. 2009;3:1420–4.
CAS  PubMed  Article  Google Scholar 

92.
Zhang J, Kasciukovic T, White MF. The CRISPR associated protein Cas4 Is a 5′ to 3′ DNA exonuclease with an iron-sulfur cluster. PloS One. 2012;7:e47232.
CAS  PubMed  PubMed Central  Article  Google Scholar 

93.
Rath D, Amlinger L, Rath A, Lundgren M. The CRISPR-Cas immune system: biology, mechanisms and applications. Biochimie. 2015;117:119–28.
CAS  PubMed  Article  Google Scholar 

94.
Jansen R, van Embden JDA, Gaastra W, Schouls LM. Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol. 2002;43:1565–75.
CAS  PubMed  PubMed Central  Article  Google Scholar 

95.
Reno ML, Held NL, Fields CJ, Burke PV, Whitaker RJ. Biogeography of the Sulfolobus islandicus pan-genome. Proc Natl Acad Sci USA. 2009;106:8605–10.
CAS  PubMed  Article  Google Scholar 

96.
Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, et al. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome.”. Proc Natl Acad Sci USA. 2005;102:13950–5.
CAS  PubMed  Article  Google Scholar 

97.
Labonté JM, Field EK, Lau M, Chivian D, Van Heerden E, Wommack KE, et al. Single cell genomics indicates horizontal gene transfer and viral infections in a deep subsurface Firmicutes population. Front Microbiol. 2015;6:349.
PubMed  PubMed Central  Google Scholar 

98.
Karnachuk OV, Frank YA, Lukina AP, Kadnikov VV, Beletsky AV, Mardanov AV, et al. Domestication of previously uncultivated Candidatus Desulforudis audaxviator from a deep aquifer in Siberia sheds light on its physiology and evolution. ISME J. 2019;13:1947–59.
CAS  PubMed  PubMed Central  Article  Google Scholar 

99.
Paul BG, Burstein D, Castelle CJ, Handa S, Arambula D, Czornyj E, et al. Retroelement-guided protein diversificiation abounds in vast lineages of bacteria and archaea. Nat Microbiol. 2017;2:17045.
CAS  PubMed  PubMed Central  Article  Google Scholar 

100.
Dirix G, Monsieurs P, Dombrecht B, Daniels R, Marchal K, Vanderleyden J, et al. Peptide signal molecules and bacteriocins in Gram-negative bacteria: a genome-wide in silico screening for peptides containing a double-glycine leader sequence and their cognate transporters. Peptides. 2004;25:1425–40.
CAS  PubMed  Article  Google Scholar  More

1.
Hylander, W. L., Johnson, K. R. & Picq, P. G. Masticatory-stress hypotheses and the supraorbital region of primates. Am. J. Phys. Anthropol. 86, 1–36 (1991).
CAS  PubMed  Article  PubMed Central  Google Scholar 
2.
Taylor, A. B. Diet and mandibular morphology in African apes. Int. J. Primatol. 27, 181–201 (2006).
Article  Google Scholar 

3.
Vogel, E. R. et al. Functional ecology and evolution of hominoid molar enamel thickness: Pan troglodytes schweinfurthii and Pongo pygmaeus wurmbii. J. Hum. Evol. 55, 60–74 (2008).
PubMed  Article  PubMed Central  Google Scholar 

4.
Strait, D. S. et al. The feeding biomechanics and dietary ecology of Australopithecus africanus. Proc. Natl. Acad. Sci. U. S. A. 106, 2124–2129 (2009).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

5.
Daegling, D. J. & McGraw, W. S. Functional morphology of the mangabey mandibular corpus: Relationship to dental specializations and feeding behavior. Am. J. Phys. Anthropol. 134, 50–62 (2007).
PubMed  Article  PubMed Central  Google Scholar 

6.
Daegling, D. J. et al. Hard-object feeding in sooty mangabeys (Cercocebus atys) and interpretation of early hominin feeding ecology. PLoS ONE 6, e23095 (2011).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

7.
Hylander, W. L. Mandibular function in Galago crassicaudatus and Macaca fascicularis: An in vivo approach to stress analysis of the mandible. J. Morphol. 159, 253–296 (1979).
CAS  PubMed  Article  PubMed Central  Google Scholar 

8.
Hylander, W. L. Stress and strain in the mandibular symphysis of primates: A test of competing hypotheses. Am. J. Phys. Anthropol. 64, 1–46 (1984).
CAS  PubMed  Article  PubMed Central  Google Scholar 

9.
Ungar, P. S. Patterns of ingestive behavior and anterior tooth use differences in sympatric anthropoid primates. Am. J. Phys. Anthropol. 95, 197–219 (1994).
CAS  PubMed  Article  PubMed Central  Google Scholar 

10.
Yamashita, N. Food procurement and tooth use in two sympatric lemur species. Am. J. Phys. Anthropol. 121, 125–133 (2003).
PubMed  Article  Google Scholar 

11.
McGraw, W. S., Vick, A. E. & Daegling, D. J. Sex and age differences in the diet and ingestive behaviors of sooty mangabeys (Cercocebus atys) in the Tai Forest, Ivory Coast. Am. J. Phys. Anthropol. 144, 140–153 (2011).
PubMed  Article  Google Scholar 

12.
McGraw, W. S. et al. Feeding and oral processing behaviors of two colobine monkeys in Tai Forest, Ivory Coast. J. Hum. Evol. 98, 90–102 (2016).
PubMed  Article  Google Scholar 

13.
Ross, C. F., Iriarte-Diaz, J., Reed, D. A., Stewart, T. A. & Taylor, A. B. In vivo bone strain in the mandibular corpus of Sapajus during a range of oral food processing behaviors. J. Hum. Evol. 98, 36–65 (2016).
PubMed  Article  Google Scholar 

14.
Ross, C. F. et al. In vivo bone strain and finite-element modeling of the craniofacial haft in catarrhine primates. J. Anat. 218, 112–141 (2011).
PubMed  Article  Google Scholar 

15.
Smith, R. J. Comparative functional morphology of maximum mandibular opening (gape) in primates. In Food Acquisition and Processing in Primates (eds Chivers, D. J. et al.) 231–255 (Plenum Press, New York, 1984).
Google Scholar 

16.
Daegling, D. J. Mandibular morphology and diet in the genus Cebus. Int. J. Primatol. 13, 545–570 (1992).
Article  Google Scholar 

17.
Daegling, D. J. Relationship of bone utilization and biomechanical competence in hominoid mandibles. Arch. Oral Biol. 52, 51–63 (2007).
PubMed  Article  PubMed Central  Google Scholar 

18.
Daegling, D. J. & Grine, F. E. Mandibular biomechanics and the paleontological evidence for the evolution of human diet. In Evolution of the Human Diet: The Known, the Unknown, and the Unknowable (ed. Ungar, P. S.) 77–105 (Oxford University Press, New York, 2006).
Google Scholar 

19.
Ross, C. F., Iriarte-Diaz, J. & Nunn, C. L. Innovative approaches to the relationship between diet and mandibular morphology in primates. Int. J. Primatol. 33, 632–660 (2012).
Article  Google Scholar 

20.
Chalk, J. et al. Age-related variation in the mechanical properties of foods processed by Sapajus libidinosus. Am. J. Phys. Anthropol. 159, 199–209 (2016).
PubMed  Article  PubMed Central  Google Scholar 

21.
Vinyard, C. J., Thompson, C. L., Doherty, A. & Robl, N. Preference and consequences: A preliminary look at whether preference impacts oral processing in non-human primates. J. Hum. Evol. 98, 27–35 (2016).
PubMed  Article  PubMed Central  Google Scholar 

22.
Strait, D. S. et al. Craniofacial strain patterns during premolar loading: implications for human evolution. In Primate Craniofacial Function and Biology (eds Vinyard, C. J. et al.) 173–198 (Springer, New York, 2008).
Google Scholar 

23.
Ravosa, M. J. Functional assessment of subfamily variation in maxillomandibular morphology among Old World monkeys. Am. J. Phys. Anthropol. 82, 199–212 (1990).
CAS  PubMed  Article  Google Scholar 

24.
Ravosa, M. J. Jaw morphology and function in living and fossil Old World monkeys. Int. J. Primatol. 17, 909–932 (1996).
Article  Google Scholar 

25.
Wright, B. W. et al. Taking a big bite: Working together to better understand the evolution of feeding in primates. Am. J. Primatol. 81, e22981 (2019).
PubMed  Google Scholar 

26.
Greaves, W. S. The jaw lever system in ungulates: A new model. J. Zool. 184, 271–285 (1978).
Article  Google Scholar 

27.
Spencer, M. A. Force production in the primate masticatory system: Electromyographic tests of biomechanical hypotheses. J. Hum. Evol. 34, 25–54 (1998).
CAS  PubMed  Article  PubMed Central  Google Scholar 

28.
Wright, B. W. Craniodental biomechanics and dietary toughness in the genus Cebus. J. Hum. Evol. 48, 473–492 (2005).
PubMed  Article  PubMed Central  Google Scholar 

29.
Wright, B. W. Ecological distinctions in diet, food toughness, and masticatory anatomy in a community of six Neotropical primates in Guyana, South America. Ph.D. Dissertation, University of Illinois at Urbana-Champaign (2004).

30.
Liu, Q. et al. Kinematics and energetics of nut-cracking in wild capuchin monkeys (Cebus libidinosus) in Piauí, Brazil. Am. J. Phys. Anthropol. 138, 210–220 (2009).
CAS  PubMed  Article  PubMed Central  Google Scholar 

31.
Taylor, A. B. & Vinyard, C. J. Jaw-muscle fiber architecture in tufted capuchins favors generating relatively large muscle forces without compromising jaw gape. J. Hum. Evol. 57, 710–720 (2009).
PubMed  PubMed Central  Article  Google Scholar 

32.
Wright, B. W. et al. Fallback foraging as a way of life: Using dietary toughness to compare the fallback signal among capuchins and implications for interpreting morphological variation. Am. J. Phys. Anthropol. 140, 687–699 (2009).
PubMed  Article  Google Scholar 

33.
Kay, R. F. The nut-crackers—A new theory of the adaptations of the Ramapithecinae. Am. J. Phys. Anthropol. 55, 141–151 (1981).
Article  Google Scholar 

34.
Masterson, T. Cranial form in Cebus: An ontogenetic analysis of cranial form and sexual dimorphism. Ph.D. Dissertation, University of Wisconsin (1996).

35.
Thiery, G. & Sha, J. C. M. Low occurrence of molar use in black-tufted capuchin monkeys: Should adaptation to seed ingestion be inferred from molars in primates? Palaeogeogr. Palaeoclimatol. Palaeoecol. 109853 (2020).

36.
Ottoni, E. B. & Izar, P. Capuchin monkey tool use: Overview and implications. Evol. Anthropol. 17, 171–178 (2008).
Article  Google Scholar 

37.
Taylor, A. B., Vogel, E. R. & Dominy, N. J. Food material properties and mandibular load resistance abilities in large-bodied hominoids. J. Hum. Evol. 55, 604–616 (2008).
PubMed  Article  PubMed Central  Google Scholar 

38.
Vogel, E. R. et al. Food mechanical properties, feeding ecology, and the mandibular morphology of wild orangutans. J. Hum. Evol. 75, 110–124 (2014).
PubMed  Article  Google Scholar 

39.
Ashby, M. F. Materials Selection in Mechanical Design (Pergamon Press, Oxford, 2002).
Google Scholar 

40.
Lucas, P. W. Dental Functional Morphology: How Teeth Work (Cambridge University Press, Cambridge, 2004).
Google Scholar 

41.
Marshall, A. J. & Wrangham, R. W. Evolutionary consequences of fallback foods. Int. J. Primatol. 28, 1219 (2007).
Article  Google Scholar 

42.
Foegeding, E. A. et al. A comprehensive approach to understanding textural properties of semi-and soft-solid foods. J. Text. Stud. 42, 103–129 (2011).
Article  Google Scholar 

43.
Herring, S. W. & Herring, S. E. The superficial masseter and gape in mammals. Am. Nat. 108, 561–576 (1974).
Article  Google Scholar 

44.
Perry, J. M. & Hartstone-Rose, A. Maximum ingested food size in captive strepsirrhine primates: Scaling and the effects of diet. Am. J. Phys. Anthropol. 142, 625–635 (2010).
PubMed  Article  Google Scholar 

45.
Hylander, W. L. Functional links between canine height and jaw gape in catarrhines with special reference to early hominins. Am. J. Phys. Anthropol. 150, 247–259 (2013).
PubMed  Article  PubMed Central  Google Scholar 

46.
Izawa, K. Foods and feeding behavior of monkeys in the upper Amazon basin. Primates 16, 295–316 (1975).
Article  Google Scholar 

47.
Izawa, K. Foods and feeding behavior of wild black-capped capuchin (Cebus apella). Primates 20, 57–76 (1979).
Article  Google Scholar 

48.
Izawa, K. & Mizuno, A. Palm-fruit cracking behavior of wild black-capped capuchin (Cebus apella). Primates 18, 773–792 (1977).
Article  Google Scholar 

49.
Fogaça, M. D. Comportamento alimentar e propriedades físicas dos alimentos consumidos por macacos-prego (Sapajus nigritus), no Parque Estadual Carlos Botelho, SP. Ph.D. Dissertation, Universidade de São Paulo (2014).

50.
Bouvier, M. Biomechanical scaling of mandibular dimensions in New World monkeys. Int. J. Primatol. 7, 551–567 (1986).
Article  Google Scholar 

51.
Taylor, A. B., Eng, C. M., Anapol, F. C. & Vinyard, C. J. The functional significance of jaw-muscle fiber architecture in tree-gouging marmosets. In The Smallest Anthropoids (eds Ford, S. M. et al.) 381–394 (Springer, Boston, 2009).
Google Scholar 

52.
McGraw, W. S., Vick, A. E. & Daegling, D. J. Dietary variation and food hardness in sooty mangabeys (Cercocebus atys): Implications for fallback foods and dental adaptation. Am. J. Phys. Anthropol. 154, 413–423 (2014).
PubMed  Article  PubMed Central  Google Scholar 

53.
McGraw, W. S. & Daegling, D. J. Primate feeding and foraging: Integrating studies of behavior and morphology. Annu. Rev. Anthropol. 41, 203–219 (2012).
Article  Google Scholar 

54.
Terborgh, J. W. Five New World Primates (Princeton University Press, Princeton, 1983).
Google Scholar 

55.
Oliveira, P. S. & Marquis, R. J. The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna (Columbia University Press, New York, 2002).
Google Scholar 

56.
Howard, A. S., Bernardes, N., Nibbelink, L., Biondi, A., Presotto, D. M., Fragaszy, M. & Madden. A maximum entropy model of the bearded capuchin monkey habitat incorporating topography and spectral unmixing analysis. ISPRS Ann. Photogramm. Remote Sens. Spat. Inf. Sci. 1, 7–11 (2012).

57.
Izar, P. et al. Flexible and conservative features of social systems in tufted capuchin monkeys: Comparing the socioecology of Sapajus libidinosus and Sapajus nigritus. Am. J. Primatol. 74, 315–331 (2012).
PubMed  Article  PubMed Central  Google Scholar 

58.
Chalk-Wilayto, J., Ossi-Lupo, K. & Raguet-Schofield, M. Growing up tough: Comparing the effects of food toughness on juvenile feeding in Sapajus libidinosus and Trachypithecus phayrei crepusculus. J. Hum. Evol. 98, 76–89 (2016).
PubMed  Article  PubMed Central  Google Scholar 

59.
Altmann, J. Observational study of behavior: Sampling methods. Behaviour 49, 227–266 (1974).
CAS  PubMed  Article  PubMed Central  Google Scholar 

60.
Darvell, B. W., Lee, P. K. D., Yuen, T. D. B. & Lucas, P. W. A portable fracture toughness tester for biological materials. Meas. Sci. Technol. 7, 954 (1996).
ADS  CAS  Article  Google Scholar 

61.
Lucas, P. W. et al. Field kit to characterize physical, chemical and spatial aspects of potential primate foods. Folia Primatol. 72, 11–25 (2001).
CAS  Article  Google Scholar 

62.
Lucas, P. W. et al. Indentation as a technique to assess the mechanical properties of fallback foods. Am. J. Phys. Anthropol. 140, 643–652 (2009).
PubMed  Article  Google Scholar 

63.
Lucas, P. W. et al. Measuring the toughness of primate foods and its ecological value. Int. J. Primatol. 33, 598–610 (2011).
Article  Google Scholar 

64.
Berthaume, M. A. Food mechanical properties and dietary ecology. Am. J. Phys. Anthropol. 159, 79–104 (2016).
Article  Google Scholar 

65.
van Casteren, A., Venkataraman, V., Ennos, A. R. & Lucas, P. W. Novel developments in field mechanics. J. Hum. Evol. 98, 5–17 (2016).
PubMed  Article  Google Scholar 

66.
Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biometr. J. 50, 346–363 (2008).
MathSciNet  MATH  Article  Google Scholar 

67.
R Core Team. R: a language and environment for statistical computing. (R Foundation for Statistical Computing, Vienna, 2017).

68.
Hiiemae, K. M. & Kay, R. F. Evolutionary trends in the dynamics of primate mastication. Craniofac. Biol. Primates 3, 28–64 (1973).
Google Scholar 

69.
Santos, L. P. C. D. Parâmetros nutricionais da dieta de duas populações de macacos-prego: Sapajus libidinosus no ecótono cerrado/caatinga e Sapajus nigritus na Mata Atlântica. Ph.D. dissertation, Universidade de São Paulo, São Paulo, Brazil (2015). More

1.
Bögner, D. Life under climate change scenarios: sea urchins’ cellular mechanisms for reproductive success. J. Mar. Sci. Eng. 4, 28 (2016).
Article  Google Scholar 
2.
Milazzo, M. et al. Ocean acidification affects fish spawning but not paternity at CO2 seeps. Proc. R. Soc. B Biol. Sci. 283, 20161021 (2016).
Article  CAS  Google Scholar 

3.
Faria, A. M. et al. Reproductive trade-offs in a temperate reef fish under high pCO2 levels. Mar. Environ. Res. 137, 8–15 (2018).
CAS  PubMed  Article  Google Scholar 

4.
Amundsen, T. Sex roles and sexual selection: lessons from a dynamic model system. Curr. Zool. 64, 363–392 (2018).
PubMed  PubMed Central  Article  Google Scholar 

5.
Borg, Å. A., Forsgren, E. & Amundsen, T. Seasonal change in female choice for male size in the two-spotted goby. Anim. Behav. 72, 763–771 (2006).
Article  Google Scholar 

6.
Skolbekken, R. & Utne-Palm, A. C. Parental investment of male two-spotted goby, Gobiusculus flavescens (Fabricius). J. Exp. Mar. Biol. Ecol. 261, 137–157 (2001).
CAS  PubMed  Article  Google Scholar 

7.
Utne-Palm, A. C., Eduard, K., Jensen, K. H., Mayer, I. & Jakobsen, P. J. Size dependent male reproductive tactic in the two-spotted goby (Gobiusculus flavescens). PLoS ONE 10, 1–23 (2015).
Article  CAS  Google Scholar 

8.
Donelson, J., Munday, P., McCormick, M., Pankhurst, N. & Pankhurst, P. Effects of elevated water temperature and food availability on the reproductive performance of a coral reef fish. Mar. Ecol. Prog. Ser. 401, 233–243 (2010).
ADS  Article  Google Scholar 

9.
Veilleux, H. D., Donelson, J. M. & Munday, P. L. Reproductive gene expression in a coral reef fish exposed to increasing temperature across generations. Conserv. Physiol. 6, 1–12 (2018).
Article  CAS  Google Scholar 

10.
IPCC. Climate Change 2014: Impacts, Adaptation, and Vulnerability. Summaries, Frequently Asked Questions, and Cross-Chapter Boxes. Climate Change 2014: Impacts, Adaptation, and vulnerability. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (2014). https://doi.org/10.1016/j.renene.2009.11.012.

11.
Fabry, V. J., Seibel, B. A., Feely, R. A. & Orr, J. C. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J. Mar. Sci. 65, 414–432 (2008).
CAS  Article  Google Scholar 

12.
Cai, W.-J. et al. Acidification of subsurface coastal waters enhanced by eutrophication. Nat. Geosci. 4, 766–770 (2011).
ADS  CAS  Article  Google Scholar 

13.
Moser, S. C. et al. Coastal zone development and ecosystems. Clim. Chang. Impacts United States Third Natl. Clim. Assess. 579–618 (2014). https://doi.org/10.7930/J0MS3QNW.On.

14.
Donelson, J. M., Wong, M., Booth, D. J. & Munday, P. L. Transgenerational plasticity of reproduction depends on rate of warming across generations. Evol. Appl. 9, 1072–1081 (2016).
PubMed  PubMed Central  Article  Google Scholar 

15.
Philippart, C. J. M. et al. Climate-related changes in recruitment of the Bivalve Macoma balthica Bos Gerhard C. Cadée and Rob Dekker. 48, 2171–2185 (2003).
Google Scholar 

16.
Miller, L. P., Matassa, C. M. & Trussell, G. C. Climate change enhances the negative effects of predation risk on an intermediate consumer. Glob. Change Biol. 20, 3834–3844 (2014).
ADS  Article  Google Scholar 

17.
Pistevos, J. C. A., Nagelkerken, I., Rossi, T., Olmos, M. & Connell, S. D. Ocean acidification and global warming impair shark hunting behaviour and growth. Sci. Rep. 5, 1–10 (2015).
Article  CAS  Google Scholar 

18.
Goldenberg, S. U. et al. Ecological complexity buffers the impacts of future climate on marine consumers. Nat. Clim. Change 8, 229–233 (2018).
ADS  Article  Google Scholar 

19.
Welch, M. J. & Munday, P. L. Contrasting effects of ocean acidification on reproduction in reef fishes. Coral Reefs 35, 485–493 (2016).
ADS  Article  Google Scholar 

20.
Miller, G. M., Watson, S.-A., McCormick, M. I. & Munday, P. L. Increased CO2 stimulates reproduction in a coral reef fish. Glob. Change Biol. 19, 3037–3045 (2013).
ADS  Article  Google Scholar 

21.
Forsgren, E., Dupont, S., Jutfelt, F. & Amundsen, T. Elevated CO2 affects embryonic development and larval phototaxis in a temperate marine fish. Ecol. Evol. 3, 3637–3646 (2013).
PubMed  PubMed Central  Article  Google Scholar 

22.
Ishimatsu, A., Hayashi, M. & Kikkawa, T. Fishes in high-CO2, acidified oceans. Mar. Ecol. Prog. Ser. 373, 295–302 (2008).
ADS  CAS  Article  Google Scholar 

23.
Melzner, F. et al. Physiological basis for high CO2 tolerance in marine ectothermic animals: Pre-adaptation through lifestyle and ontogeny?. Biogeosciences 6, 2313–2331 (2009).
ADS  CAS  Article  Google Scholar 

24.
Gianguzza, P. et al. Temperature modulates the response of the thermophilous sea urchin Arbacia lixula early life stages to CO2 -driven acidi fi cation. Mar. Environ. Res. 93, 70–77 (2014).
CAS  PubMed  Article  PubMed Central  Google Scholar 

25.
Domenici, P., Allan, B. J. M., Watson, S.-A., McCormick, M. I. & Munday, P. L. Shifting from right to left: the combined effect of elevated CO2 and temperature on behavioural lateralization in a coral reef fish. PLoS ONE 9, e87969 (2014).
ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

26.
Schram, J. B., Schoenrock, K. M., McClintock, J. B., Amsler, C. D. & Angus, R. A. Multiple stressor effects of near-future elevated seawater temperature and decreased pH on righting and escape behaviors of two common Antarctic gastropods. J. Exp. Mar. Biol. Ecol. 457, 90–96 (2014).
Article  Google Scholar 

27.
Garzke, J., Hansen, T., Ismar, S. M. H. & Sommer, U. Combined effects of ocean warming and acidification on copepod abundance, body size and fatty acid content. PLoS ONE 11, e0155952 (2016).
PubMed  PubMed Central  Article  CAS  Google Scholar 

28.
Gobler, C. J., Merlo, L. R., Morrell, B. K. & Griffith, A. W. Temperature, acidification, and food supply interact to negatively affect the growth and survival of the forage fish, Menidia beryllina (Inland Silverside), and Cyprinodon variegatus (Sheepshead Minnow). Front. Mar. Sci. 5, 1–12 (2018).
Article  Google Scholar 

29.
Sswat, M., Stiasny, M. H., Jutfelt, F., Riebesell, U. & Clemmesen, C. Growth performance and survival of larval Atlantic herring, under the combined effects of elevated temperatures and CO2. PLoS ONE https://doi.org/10.1371/journal.pone.0191947 (2018).
Article  PubMed  PubMed Central  Google Scholar 

30.
Miller, G. M., Kroon, F. J., Metcalfe, S. & Munday, P. L. Temperature is the evil twin: effects of increased temperature and ocean acidification on reproduction in a reef fish. Ecol. Appl. 25, 603–620 (2015).
CAS  PubMed  Article  Google Scholar 

31.
Utne-Palm, A. C. Response of naïve two-spotted gobies Gobiusculus flavescens to visual and chemical stimuli of their natural predator, cod Gadus morhua. Mar. Ecol. Prog. Ser. 218, 267–274 (2001).
ADS  Article  Google Scholar 

32.
Leo, E., Dahlke, F. T., Storch, D., Pörtner, H.-O. & Mark, F. C. Impact of ocean acidification and warming on the bioenergetics of developing eggs of Atlantic herring Clupea harengus. Conserv. Physiol. 6, coy050 (2018).
CAS  PubMed  PubMed Central  Article  Google Scholar 

33.
Vargas, C. A. et al. Species-specific responses to ocean acidification should account for local adaptation and adaptive plasticity. Nat. Ecol. Evol. 1, 1–7 (2017).
CAS  Article  Google Scholar 

34.
Dorey, N., Lançon, P., Thorndyke, M. & Dupont, S. Assessing physiological tipping point of sea urchin larvae exposed to a broad range of pH. Glob. Change Biol. 19, 3355–3367 (2013).
Google Scholar 

35.
Magnhagen, C. et al. Context consistency and seasonal variation in boldness of male two-spotted gobies. PLoS ONE 9, e93354 (2014).
ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

36.
Torricelli, P., Lugli, M. & Gandolfi, G. A quantitative analysis of the fanning activity in the male Padogobius martensi (Pisces: Gobiidae). Behaviour 92, 288–301 (1985).
Google Scholar 

37.
Kraak, S. B. M. Female preference and filial cannibalism in Aidablennius sphynx (Teleostei, Blenniidae); a combined field and laboratory study. Behav. Processes 36, 85–97 (1996).
CAS  PubMed  Article  Google Scholar 

38.
Jan, M., Jan, U. & Shah, G. M. Studies on fecundity and Gonadosomatic index of Schizothorax plagiostomus (Cypriniformes: Cyprinidae). J. Threat. Taxa 6, 5375–5379 (2014).
Article  Google Scholar 

39.
Forsgren, E., Amundsen, T., Borg, Å. A. & Bjelvenmark, J. Unusually dynamic sex roles in a fish. Nature 429, 551–554 (2004).
ADS  CAS  PubMed  Article  Google Scholar 

40.
Donelson, J. M., Munday, P. L., McCormick, M. I. & Pitcher, C. R. Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat. Clim. Change 2, 30–32 (2012).
ADS  Article  Google Scholar 

41.
Bernal, M. A. et al. Phenotypic and molecular consequences of step-wise temperature increase across generations in a coral reef fish. Mol. Ecol. https://doi.org/10.1111/mec.14884 (2018).
Article  PubMed  PubMed Central  Google Scholar 

42.
Hopkins, K., Moss, B. R. & Gill, A. B. Increased ambient temperature alters the parental care behaviour and reproductive success of the three-spined stickleback (Gasterosteus aculeatus). Environ. Biol. Fishes 90, 121–129 (2011).
Article  Google Scholar 

43.
Stillman, J. H. Acclimation capacity underlies susceptibility to climate change. Science 301, 65 (2003).
CAS  PubMed  Article  PubMed Central  Google Scholar 

44.
Laubenstein, T. D., Rummer, J. L., McCormick, M. I. & Munday, P. L. A negative correlation between behavioural and physiological performance under ocean acidification and warming. Sci. Rep. 9, 1–10 (2019).
CAS  Article  Google Scholar 

45.
Dickson, A. G., Sabine, C. L. & Christian, J. R. Guide to Best Practices for Ocean CO2 measurements. PICES Special Publication. Guide to Best Practices for Ocean CO2 measurements. PICES Special Publication 3, (2007).

46.
Lewis, E. & Wallace, D. Program developed for CO2 system calculations. Ornl/Cdiac 105, 1–21 (1998).
Google Scholar 

47.
Lissåker, M. & Kvarnemo, C. Ventilation or nest defense—parental care trade-offs in a fish with male care. Behav. Ecol. Sociobiol. 60, 864–873 (2006).
Article  Google Scholar 

48.
Baklow, G. W. Ethology of the Asian Teleost Badis badis. V. dynamics of fanning and other parental activities, with comments on the behavior of the larvae and Postlarvae 2, 3. Z. Tierpsychol. 21, 99–123 (1964).
Google Scholar 

49.
Blumer, L. S. Male parental care in the bony fishes. Q. Rev. Biol. 54, 149–161 (1979).
Article  Google Scholar  More

Study area
We conducted our study at Nopporo Forest Park in Hokkaido, Japan (43° 03′ N, 141° 32′ E) (Fig. 1). This forest is a semi-isolated 2,053 ha area surrounded by residential areas and farmland. There have been concerns about raccoon impacts on this ecosystem since they were first detected in 199234.
Animals
We captured raccoons using box traps (Havahart Large Collapsible Pro Cage Model 1089, Woodstream Corp., Lititz, PA, USA) from May to July in 2018 and April to August in 2019. Traps were placed at 86 sites (Fig. 1). Trapping points within 250 m of the forest boundary line facing the farmland were defined as ‘around the farmland’ (31 points), and other points were defined as ‘in the forest’ (55 points) using QGIS version 3.1023. Captured raccoons were anesthetised with butorphanol tartrate (Vetorphale 5 mg, 1.2 mg/kg; Meiji Seika, Tokyo, Japan), medetomidine hydrochloride (Dolbene, 40 µg/kg; Kyoritsu, Tokyo, Japan), and midazolam (Dormicum injection 10 mg, 0.2 mg/kg; Astellas, Tokyo, Japan) by intramuscular injection and euthanised by potassium chloride injection into the heart. We captured 48 raccoons (34 around the farmland, 14 in the forest) in 2018, and 27 (12 around the farmland, 15 in the forest) in 2019 (Fig. 1). We collected thigh muscle samples, rectal faeces, and gastric contents from captured raccoons. Samples were stored at − 20 °C until analysis.
DNA metabarcoding
Sample preparation
Rectal faeces and gastric contents that were dominated by plant materials and groomed hair were excluded from analyses. In total, 18 rectal faeces and six gastric content samples that contained animal materials or whose contents were unknown were selected. Rapidly digested food resources such as amphibians cannot be confirmed visually in gastrointestinal contents, and even DNA may not be detected. Therefore, multiple samples were pooled and analysed because the target DNA may not be detected otherwise. The rectal faeces and gastric contents were divided into five (S1–S5) and two groups (G1–G2), respectively, based on the capture site and date of raccoons (Table 1). Each group was mixed and stored at − 20 °C until DNA extraction. Subsequent DNA analyses were performed at Bioengineering Lab. Co., Ltd. (Kanagawa, Japan).
DNA extraction
Samples (about 100 mg each) were lyophilised using a VD-250R lyophiliser freeze dryer (TAITEC, Saitama, Japan) and ground using a ShakeMaster NEO homogeniser (Bio Medical Science, Tokyo, Japan). Crude DNA was extracted from each group; then, DNA was purified using the MPure-12 Automated Nucleic Acid Purification System (MP Biomedicals, California, USA) with a MPure Bacterial DNA Extraction Kit (MP Biomedicals).
Library preparation and sequencing
Each library was prepared using two-step tailed PCR. We used the gSalamander primer, which amplifies salamander and newt 12S rRNA, as a specific primer to detect Hokkaido salamander, and the gInsect primer, which amplifies arthropod 16S rRNA, to detect Japanese crayfish (Table 5). All primers were designed by Bioengineering Lab. Co., Ltd.
Table 5 Primer sets used in this study.
Full size table

The first PCR amplified the target region using gSalamander and gInsect. These reactions were conducted in a final volume of 10 μl, comprising 2 μl DNA template, 0.5 μl each primer (10 μM), 0.1 μl Ex Taq HS (5 U/µl) (Takara Bio Inc., Shiga, Japan), 1.0 μl 10 × Ex Taq buffer, 0.8 μl dNTP mixture (2.5 mM), and 5.1 μl sterile distilled water. The PCR conditions were: first denaturation for 2 min at 94 °C, followed by 35 cycles of 30 s at 94 °C, 30 s at 50 °C, and 30 s at 72 °C, and final extension for 5 min at 72 °C.
The second PCR used the first PCR products as the template with index primers (2ndF and 2ndR). These reactions were conducted in a final volume of 10 μl, as described for the first PCR. The PCR conditions were: first denaturation for 2 min at 94 °C, followed by 12 cycles of 30 s at 94 °C, 30 s at 60 °C, and 30 s at 72 °C, and final extension for 5 min at 72 °C. At each step, PCR products were purified using the Agencourt AMPure XP system (Beckman Coulter, Inc., California, USA). The library concentrations were measured with a Synergy H1 microplate reader (BioTek) and a QuantiFluor dsDNA System (Promega). Library quality was assessed using a Fragment Analyser (Advanced Analytical Technologies, Iowa, USA) with a dsDNA 915 Reagent Kit (Agilent, California, USA). Paired-end sequencing (2 × 300 bp) was conducted on the Illumina MiSeq platform (Illumina, California, USA).
Data analysis
Reads that began with a sequence that completely matched the primer used were extracted using the fastq_barcode_splitter tool in the FASTX-Toolkit; then, the primer sequence was trimmed. The reads were trimmed and filtered using the Sickle tool with a quality value of 20; then, trimmed and paired-end reads with fewer than 150 bases were discarded. The remaining reads were merged using the FLASH paired-end merge script35 under the following conditions: fragment length after merge, 300 bases; read fragment length, 230 bases; and minimum overlap length, 10 bases. The UCHIME2 algorithm within USEARCH was used to check all filtered sequences for chimeric sequences36. All sequences that were not judged to be chimeras were used for further analysis. The UPARSE algorithm within USEARCH was used for OTU creation and taxonomic assignments. The constructed OTUs were subjected to Basic Local Alignment Search Tool (BLASTN) searches. More than 100 reads and the top BLAST hit with a sequence identity of ≥ 97% were used to assign species (target length: about 300 bp) to each representative sequence37.
Additional analyses of COI region
S–2, S–3, G–1, and G–2 sample group DNA was successfully extracted using gSalamander or gInsect primers (Table 1) and analysed by PCR using COI and blocking primers for raccoon (Table 5). The library was prepared using two-step tailed PCR. The first PCR amplification using the primer set 1st-IntF and 1st-HCOmR was conducted in a final volume of 10 μl, comprising 2 μl DNA template, 5 μl of each primer (10 μM) (forward primer 0.5 µl, reverse primer 0.5 µl, blocking primer 4 µl), 0.08 μl Ex Taq HS (5 U/µl), 1.0 μl 10 × Ex Taq buffer, 0.8 μl dNTP mixture (2.5 mM), and 1.12 μl DDW. The PCR conditions were as follows: first denaturation for 2 min at 94 °C, followed by 35 cycles of 30 s at 94 °C, 15 s at 67 °C, and 30 s at 52 °C and 30 s at 72 °C, and final extension for 5 min at 72 °C. Subsequent methods were as described above, except for the FLASH paired-end merge script (fragment length after merge, 310 bases; read fragment length, 225 bases).
Stable isotope analysis
Stable isotope ratios of muscle tissue reflect the diet over the previous few weeks to one month38,39. We used the muscles of raccoons captured from April to August and assumed that the stable isotope ratios in raccoon muscle samples reflected their diet from March to July, i.e. late winter to early summer, in Hokkaido.
Raccoon muscle and potential prey item samples were dried at 60 °C for  > 24 h and then ground with a mortar and pestle. Potential food items (such as amphibians and crustaceans) were collected from the forest. The raccoon muscle and potential prey item samples were rinsed with a 2:1 chloroform: methanol solution to remove lipids and then dried at 60 °C for at least 24 h40. Each sample (1.0–3.0 mg) was enclosed in a tin cup and combusted in an elemental analyser (Vario MICRO cube, Elementar Gmbh, Hanau, Germany) interfaced with an isotope ratio mass spectrometer (IsoPrime100, Elementar Gmbh). We determined the δ13C, δ15N, and δ34S values for each sample. The results are reported as parts per thousand of the isotopes relative to a standard. For δ13C, δ15N, and δ34S values, Vienna Pee Dee Belemnite, air, and Vienna Cañon Diablo Triolite were used as standards, respectively. We used L-alanine (Shoko Science Co., Ltd., Tokyo, Japan) and sulfanilamide (Elementar GmbH) as working standards. A working standard, sulfanilamide (δ34S value, − 1.92‰), was calibrated against IAEA (International Atomic Energy Agency, Vienna, Austria) silver sulfides, IAEA-S-1, IAEA-S-2, IAEA-S-3, and was used as a working standard for δ34S.
Statistical analysis
We performed two-way analysis of variance to examine the interactions between two independent variables, season (spring: April–June vs. summer: July–August) and capture site (around the farmland vs. in the forest), and their relationship with the dependent variables (stable isotope ratio; δ13C, δ15N, and δ34S). After examining interactions between two independent variables (season and capture site), a Mann–Whitney U test was conducted. Differences were considered statistically significant at P  More

1.
Schluter, D. The Ecology of Adaptive Radiations (Oxford Univ. Press, 2000).
2.
Gavrilets, S. & Losos, J. B. Adaptive radiation: contrasting theory with data. Science 323, 732–737 (2009).
CAS  PubMed  Google Scholar 

3.
Arnold, S. J., Bürger, R., Hohenlohe, P. A., Ajie, B. C. & Jones, A. G. Understanding the evolution and stability of the G-matrix. Evolution 62, 2451–2461 (2008).
PubMed  PubMed Central  Google Scholar 

4.
Losos, J. B. Adaptive radiation, ecological opportunity, and evolutionary determinism: American Society of Naturalists E. O. Wilson award address. Am. Nat. 175, 623–639 (2010).
PubMed  Google Scholar 

5.
Elmer, K. R. et al. Parallel evolution of Nicaraguan crater lake cichlid fishes via non-parallel routes. Nat. Commun. 5, 5168 (2014).
CAS  PubMed  Google Scholar 

6.
Mahler, D. L., Ingram, T., Revell, L. J. & Losos, J. B. Exceptional convergence on the macroevolutionary landscape in island lizard radiations. Science 341, 292–295 (2013).
CAS  PubMed  Google Scholar 

7.
Lamichhaney, S. et al. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518, 371–375 (2015).
CAS  PubMed  Google Scholar 

8.
Gould, S. J. Wonderful Life: The Burgess Shale and the Nature of History (W. W. Norton, 1989).

9.
Schluter, D. Adaptive radiation along genetic lines of least resistance. Evolution 50, 1766–1774 (1996).
PubMed  Google Scholar 

10.
Roff, D. The evolution of the G matrix: selection or drift? Heredity 84, 135–142 (2000).
PubMed  Google Scholar 

11.
Arendt, J. & Reznick, D. Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol. Evol. 23, 26–32 (2008).
PubMed  Google Scholar 

12.
Stuart, Y. E. Divergent uses of ‘parallel evolution’ during the history of the American naturalist. Am. Nat. 193, 11–19 (2019).
PubMed  Google Scholar 

13.
Oke, K. B., Rolshausen, G., LeBlond, C. & Hendry, A. P. How parallel is parallel evolution? A comparative analysis in fishes. Am. Nat. 190, 1–16 (2017).
PubMed  Google Scholar 

14.
McGee, M. D., Neches, R. Y. & Seehausen, O. Evaluating genomic divergence and parallelism in replicate ecomorphs from young and old cichlid adaptive radiations. Mol. Ecol. 25, 260–268 (2016).
CAS  PubMed  Google Scholar 

15.
Soria-Carrasco, V. et al. Stick insect genomes reveal natural selection’s role in parallel speciation. Science 344, 738–742 (2014).
CAS  PubMed  Google Scholar 

16.
MacColl, A. D. C. The ecological causes of evolution. Trends Ecol. Evol. 26, 514–522 (2011).
PubMed  Google Scholar 

17.
Elmer, K. R. & Meyer, A. Adaptation in the age of ecological genomics: insights from parallelism and convergence. Trends Ecol. Evol. 26, 298–306 (2011).
PubMed  Google Scholar 

18.
Conte, G. L., Arnegard, M. E., Peichel, C. L. & Schluter, D. The probability of genetic parallelism and convergence in natural populations. Proc. R. Soc. B 279, 5039–5047 (2012).
PubMed  Google Scholar 

19.
Jones, F. C. et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55–61 (2012).
CAS  PubMed  PubMed Central  Google Scholar 

20.
Stuart, Y. E. et al. Contrasting effects of environment and genetics generate a continuum of parallel evolution. Nat. Ecol. Evol. 1, 0158 (2017).
Google Scholar 

21.
Jacobs, A. et al. Parallelism in eco-morphology and gene expression despite variable evolutionary and genomic backgrounds in a Holarctic fish. PLoS Genet. 16, 1008658 (2020).
Google Scholar 

22.
Muschick, M., Indermaur, A. & Salzburger, W. Convergent evolution within an adaptive radiation of cichlid fishes. Curr. Biol. 22, 2362–2368 (2012).
CAS  Google Scholar 

23.
Foster, S. & Bell, M. The Evolutionary Biology of the Threespine Stickleback (Oxford Univ. Press, 1994).

24.
Taylor, E. B. & McPhail, J. D. Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus. Proc. R. Soc. Lond. B 267, 2375–2384 (2000).
CAS  Google Scholar 

25.
Kaeuffer, R., Peichel, C. L., Bolnick, D. I. & Hendry, A. P. Parallel and nonparallel aspects of ecological, phenotypic, and genetic divergence across replicate population pairs of lake and stream stickleback. Evolution 66, 402–418 (2012).
PubMed  Google Scholar 

26.
Ravinet, M., Prodöhl, P. A. & Harrod, C. Parallel and nonparallel ecological, morphological and genetic divergence in lake-stream stickleback from a single catchment. J. Evol. Biol. 26, 186–204 (2013).
CAS  PubMed  Google Scholar 

27.
Magalhaes, I. S., D’Agostino, D., Hohenlohe, P. A. & MacColl, A. D. C. The ecology of an adaptive radiation of three-spined stickleback from North Uist, Scotland. Mol. Ecol. 25, 4319–4336 (2016).
PubMed  PubMed Central  Google Scholar 

28.
Colosimo, P. F. et al. Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307, 1928–1933 (2005).
CAS  PubMed  Google Scholar 

29.
Jones, F. C. et al. A genome-wide SNP genotyping array reveals patterns of global and repeated species-pair divergence in sticklebacks. Curr. Biol. 22, 83–90 (2012).
CAS  PubMed  Google Scholar 

30.
Raeymaekers, J. A. M. et al. Adaptive and non-adaptive divergence in a common landscape. Nat. Commun. 8, 267 (2017).
PubMed  PubMed Central  Google Scholar 

31.
Rennison, D. J., Stuart, Y. E., Bolnick, D. I. & Peichel, C. L. Ecological factors and morphological traits are associated with repeated genomic differentiation between lake and stream stickleback. Phil. Trans. R. Soc. B 374, 20180241 (2019).
CAS  PubMed  Google Scholar 

32.
MacColl, A. D. C. & Aucott, B. Inappropriate analysis does not reveal the ecological causes of evolution of stickleback armour: a critique of Spence et al. 2013. Ecol. Evol. 4, 3509–3513 (2014).
PubMed  PubMed Central  Google Scholar 

33.
Spoljaric, M. A. & Reimchen, T. E. 10,000 years later: evolution of body shape in Haida Gwaii three-spined stickleback. J. Fish Biol. 70, 1484–1503 (2007).
Google Scholar 

34.
De Schamphelaere, K. A. C. et al. Reproductive toxicity of dietary zinc to Daphnia magna. Aquat. Toxicol. 70, 233–244 (2004).
PubMed  Google Scholar 

35.
Martins, C., Jesus, F. T. & Nogueira, A. J. A. The effects of copper and zinc on survival, growth and reproduction of the cladoceran Daphnia longispina: introducing new data in an ‘old’ issue. Ecotoxicology 26, 1157–1169 (2017).
CAS  PubMed  Google Scholar 

36.
Miller, C. T. et al. Modular skeletal evolution in sticklebacks is controlled by additive and clustered quantitative trait loci. Genetics 197, 405–420 (2014).
PubMed  PubMed Central  Google Scholar 

37.
Chan, Y. F. et al. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327, 302–305 (2010).
CAS  PubMed  Google Scholar 

38.
Thompson, K. A., Osmond, M. M. & Schluter, D. Parallel genetic evolution and speciation from standing variation. Evol. Lett. 3, 129–141 (2019).
PubMed  PubMed Central  Google Scholar 

39.
Nelson, T. C. & Cresko, W. A. Ancient genomic variation underlies repeated ecological adaptation in young stickleback populations. Evol. Lett. 2, 9–21 (2018).
PubMed  PubMed Central  Google Scholar 

40.
Paccard, A. et al. Repeatability of adaptive radiation depends on spatial scale: regional versus global replicates of stickleback in lake versus stream habitats. J. Hered. 111, 43–56 (2019).
Google Scholar 

41.
Baldo, L., Riera, J. L., Salzburger, W. & Barluenga, M. Phylogeography and ecological niche shape the cichlid fish gut microbiota in Central American and African lakes. Front. Microbiol. 10, 2372 (2019).
PubMed  PubMed Central  Google Scholar 

42.
Fang, B., Kemppainen, P., Momigliano, P. & Merilä, J. On the causes of geographically heterogeneous parallel evolution in sticklebacks. Nat. Ecol. Evol. 4, 1105–1115 (2020).
PubMed  Google Scholar 

43.
Mäkinen, H. S. & Merilä, J. Mitochondrial DNA phylogeography of the three-spined stickleback (Gasterosteus aculeatus) in Europe—evidence for multiple glacial refugia. Mol. Phylogenet. Evol. 46, 167–182 (2008).
PubMed  Google Scholar 

44.
Liu, S., Hansen, M. M. & Jacobsen, M. W. Region-wide and ecotype-specific differences in demographic histories of threespine stickleback populations, estimated from whole genome sequences. Mol. Ecol. 25, 5187–5202 (2016).
CAS  PubMed  Google Scholar 

45.
Fang, B., Merilä, J., Ribeiro, F., Alexandre, C. M. & Momigliano, P. Worldwide phylogeny of three-spined sticklebacks. Mol. Phylogenet. Evol. 127, 613–625 (2018).
PubMed  Google Scholar 

46.
Garduno-Paz, M. V., Couderc, S. & Adams, C. E. Habitat complexity modulates phenotype expression through developmental plasticity in the threespine stickleback. Biol. J. Linn. Soc. 100, 407–413 (2010).
Google Scholar 

47.
Coop, G., Witonsky, D., Di Rienzo, A. & Pritchard, J. K. Using environmental correlations to identify loci underlying local adaptation. Genetics 185, 1411–1423 (2010).
CAS  PubMed  PubMed Central  Google Scholar 

48.
Hohenlohe, P. A. et al. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 6, e1000862 (2010).
PubMed  PubMed Central  Google Scholar 

49.
Guo, B., DeFaveri, J., Sotelo, G., Nair, A. & Merilä, J. Population genomic evidence for adaptive differentiation in Baltic Sea three-spined sticklebacks. BMC Biol. 13, 19 (2015).
PubMed  PubMed Central  Google Scholar 

50.
Glazer, A. M., Cleves, P. A., Erickson, P. A., Lam, A. Y. & Miller, C. T. Parallel developmental genetic features underlie stickleback gill raker evolution. EvoDevo 5, 19 (2014).
PubMed  PubMed Central  Google Scholar 

51.
Day, T., Pritchard, J. & Schluter, D. A comparison of two sticklebacks. Evolution 48, 1723–1734 (1994).
PubMed  Google Scholar 

52.
Franchini, P. et al. Genomic architecture of ecologically divergent body shape in a pair of sympatric crater lake cichlid fishes. Mol. Ecol. 23, 1828–1845 (2014).
PubMed  Google Scholar 

53.
McCairns, R. J. S. & Bernatchez, L. Plasticity and heritability of morphological variation within and between parapatric stickleback demes. J. Evol. Biol. 25, 1097–1112 (2012).
CAS  PubMed  Google Scholar 

54.
Peichel, C. L. & Marques, D. A. The genetic and molecular architecture of phenotypic diversity in sticklebacks. Phil. Trans. R. Soc. B 372, 20150486 (2017).
PubMed  Google Scholar 

55.
Marques, D. A. et al. Genomics of rapid incipient speciation in sympatric threespine stickleback. PLoS Genet. 12, e1005887 (2016).
PubMed  PubMed Central  Google Scholar 

56.
Burke, M. K., Liti, G. & Long, A. D. Standing genetic variation drives repeatable experimental evolution in outcrossing populations of Saccharomyces cerevisiae. Mol. Biol. Evol. 31, 3228–3239 (2014).
CAS  PubMed  PubMed Central  Google Scholar 

57.
Kang, L., Aggarwal, D. D., Rashkovetsky, E., Korol, A. B. & Michalak, P. Rapid genomic changes in Drosophila melanogaster adapting to desiccation stress in an experimental evolution system. BMC Genom. 17, 233 (2016).
Google Scholar 

58.
Gompert, Z. & Messina, F. J. Genomic evidence that resource‐based trade‐offs limit host‐range expansion in a seed beetle. Evolution 70, 1249–1264 (2016).
CAS  PubMed  Google Scholar 

59.
Berner, D., Moser, D., Roesti, M., Buescher, H. & Salzburger, W. Genetic architecture of skeletal evolution in European lake and stream stickleback. Evolution 68, 1792–1805 (2014).
CAS  PubMed  Google Scholar 

60.
Pease, J. B., Haak, D. C., Hahn, M. W. & Moyle, L. C. Phylogenomics reveals three sources of adaptive variation during a rapid radiation. PLoS Biol. 14, e1002379 (2016).
PubMed  PubMed Central  Google Scholar 

61.
Lowry, D. B. et al. Breaking RAD: an evaluation of the utility of restriction site-associated DNA sequencing for genome scans of adaptation. Mol. Ecol. Resour. 17, 142–152 (2017).
CAS  Google Scholar 

62.
McKinney, G. J., Larson, W. A., Seeb, L. W. & Seeb, J. E. RADseq provides unprecedented insights into molecular ecology and evolutionary genetics: comment on Breaking RAD by Lowry et al. (2016). Mol. Ecol. Resour. 17, 356–361 (2017).
CAS  PubMed  Google Scholar 

63.
Roesti, M., Kueng, B., Moser, D. & Berner, D. The genomics of ecological vicariance in threespine stickleback fish. Nat. Commun. 6, 8767 (2015).
CAS  PubMed  PubMed Central  Google Scholar 

64.
Catchen, J. M. et al. Unbroken: RADseq remains a powerful tool for understanding the genetics of adaptation in natural populations. Mol. Ecol. Resour. 17, 362–365 (2017).
CAS  PubMed  Google Scholar 

65.
Roesti, M., Moser, D. & Berner, D. Recombination in the threespine stickleback genome—patterns and consequences. Mol. Ecol. 22, 3014–3027 (2013).
CAS  PubMed  Google Scholar 

66.
Samuk, K. et al. Gene flow and selection interact to promote adaptive divergence in regions of low recombination. Mol. Ecol. 26, 4378–4390 (2017).
PubMed  Google Scholar 

67.
Meier, J. I., Marques, D. A., Wagner, C. E., Excoffier, L. & Seehausen, O. Genomics of parallel ecological speciation in Lake Victoria cichlids. Mol. Biol. Evol. 35, 1489–1506 (2018).
CAS  PubMed  Google Scholar 

68.
Cruickshank, T. E. & Hahn, M. W. Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol. Ecol. 23, 3133–3157 (2014).
PubMed  Google Scholar 

69.
Terekhanova, N. V. et al. Fast evolution from precast bricks: genomics of young freshwater populations of threespine stickleback Gasterosteus aculeatus. PLoS Genet. 10, e1004696 (2014).
PubMed  PubMed Central  Google Scholar 

70.
Westram, A. M. et al. Clines on the seashore: the genomic architecture underlying rapid divergence in the face of gene flow. Evol. Lett. 2, 297–309 (2018).
PubMed  PubMed Central  Google Scholar 

71.
Shimada, Y., Shikano, T. & Merilä, J. A high incidence of selection on physiologically important genes in the three-spined stickleback, Gasterosteus aculeatus. Mol. Biol. Evol. 28, 181–193 (2011).
CAS  PubMed  Google Scholar 

72.
Xie, K. T. et al. DNA fragility in the parallel evolution of pelvic reduction in stickleback fish. Science 363, 81–84 (2019).
CAS  PubMed  PubMed Central  Google Scholar 

73.
Henning, F. & Meyer, A. The evolutionary genomics of cichlid fishes: explosive speciation and adaptation in the postgenomic era. Annu. Rev. Genomics Hum. Genet. 15, 417–441 (2014).
CAS  PubMed  Google Scholar 

74.
Kess, T., Galindo, J. & Boulding, E. G. Genomic divergence between Spanish Littorina saxatilis ecotypes unravels limited admixture and extensive parallelism associated with population history. Int. J. Bus. Innov. Res. 17, 8311–8327 (2018).
Google Scholar 

75.
Bohutínská, M. et al. Genomic basis of parallel adaptation varies with divergence in Arabidopsis and its relatives. Preprint at BioRxiv https://doi.org/10.1101/2020.03.24.005397 (2020).

76.
Rennison, D. J., Samuk, K., Owens, G. L. & Miller, S. E. Shared patterns of genome-wide differentiation are more strongly predicted by geography than by ecology. Am. Nat. 195, 192–200 (2019).
PubMed  Google Scholar 

77.
Lucek, K., Sivasundar, A., Roy, D. & Seehausen, O. Repeated and predictable patterns of ecotypic differentiation during a biological invasion: lake–stream divergence in parapatric Swiss stickleback. J. Evol. Biol. 26, 2691–2709 (2013).
CAS  PubMed  Google Scholar 

78.
Berner, D., Roesti, M., Hendry, A. P. & Salzburger, W. Constraints on speciation suggested by comparing lake–stream stickleback divergence across two continents. Mol. Ecol. 19, 4963–4978 (2010).
PubMed  Google Scholar 

79.
Giles, N. Behavioural effects of the parasite Schistocephalus solidus (Cestoda) on an intermediate host, the three-spined stickleback, Gasterosteus aculeatus L. Anim. Behav. 31, 1192–1194 (1983).
Google Scholar 

80.
Spence, R., Wootton, R. J., Barber, I., Przybylski, M. & Smith, C. Ecological causes of morphological evolution in the three-spined stickleback. Ecol. Evol. 3, 1717–1726 (2013).
PubMed  PubMed Central  Google Scholar 

81.
Reimchen, T. E. Incidence and intensity of Cyathocephalus truncatus and Schistocephalus solidus infection in Gasterosteus aculeatus. Can. J. Zool. 60, 1091–1095 (1982).
Google Scholar 

82.
MacColl, A. D. C. Parasite burdens differ between sympatric three-spined stickleback species. Ecography 32, 153–160 (2009).
Google Scholar 

83.
Stutz, W. E., Lau, O. L. & Bolnick, D. I. Contrasting patterns of phenotype-dependent parasitism within and among populations of threespine stickleback. Am. Nat. 183, 810–825 (2014).
PubMed  Google Scholar 

84.
Bassham, S., Catchen, J., Lescak, E., von Hippel, F. A. & Cresko, W. A. Repeated selection of alternatively adapted haplotypes creates sweeping genomic remodeling in stickleback. Genetics 209, 921–939 (2018).
PubMed  PubMed Central  Google Scholar 

85.
Etter, P. D., Preston, J. L., Bassham, S., Cresko, W. A. & Johnson, E. A. Local de novo assembly of RAD paired-end contigs using short sequencing reads. PLoS ONE 6, e18561 (2011).
CAS  PubMed  PubMed Central  Google Scholar 

86.
Ali, O. A. et al. Rad capture (Rapture): flexible and efficient sequence-based genotyping. Genetics 202, 389–400 (2016).
CAS  PubMed  Google Scholar 

87.
Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A. & Cresko, W. A. Stacks: an analysis tool set for population genomics. Mol. Ecol. 22, 3124–3140 (2013).
PubMed  PubMed Central  Google Scholar 

88.
Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).
CAS  Google Scholar 

89.
Chang, C. C. et al. Second-generation PLINK: rising to the challenge of larger and richer datasets. GigaScience 4, 7 (2015).
PubMed  PubMed Central  Google Scholar 

90.
R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017); https://www.R-project.org/

91.
Günther, T. & Coop, G. Robust identification of local adaptation from allele frequencies. Genetics 195, 205–220 (2013).
PubMed  PubMed Central  Google Scholar 

92.
Yeaman, S. et al. Convergent local adaptation to climate in distantly related conifers. Science 353, 1431–1433 (2016).
CAS  PubMed  Google Scholar 

93.
Storey, J. qvalue: Q-value estimation for false discovery rate control. R package version 2.0.0 (2015).

94.
Pfeifer, B., Wittelsbürger, U., Ramos-Onsins, S. E. & Lercher, M. J. PopGenome: an efficient Swiss Army knife for population genomic analyses in R. Mol. Biol. Evol. 31, 1929–1936 (2014).
CAS  PubMed  PubMed Central  Google Scholar  More

1.
Jackson, J., Donovan, M., Cramer, K. & Lam, V. Status and Trends of Caribbean Coral Reefs: 1970–2012. Glob. Coral Reef Monit. Network, Int. Union for Conserv. Nat. Glob. Mar. Polar Program, Washington, DC (2014).
2.
Baird, A. H., Babcock, R. C. & Mundy, C. P. Habitat selection by larvae influences the depth distribution of six common coral species. Mar. Ecol. Prog. Ser. 252, 289–293 (2003).
ADS  Article  Google Scholar 

3.
Harrington, L., Fabricius, K., De’ath, G. & Negri, A. Recognition and selection of settlement substrata determine post-settlement survival in corals. Ecol. 85, 3428–3437 (2004).
Article  Google Scholar 

4.
Roff, G. & Mumby, P. J. Global disparity in the resilience of coral reefs. Trends Ecol. & Evol. 27, 404–413 (2012).
PubMed  Article  PubMed Central  Google Scholar 

5.
Lessios, H. A. Mass mortality of Diadema antillarum in the Caribbean: What Have We Learned? Annu. Rev. Ecol. Syst. 19, 371–393 (1988).
Article  Google Scholar 

6.
Patterson, K. L. et al. The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata. Proc. Natl. Acad. Sci. 99, 8725–8730 (2002).

7.
Eakin, C. M. et al. Caribbean Corals in Crisis: Record Thermal Stress, Bleaching, and Mortality in 2005. PLoS ONE 5, 1–9 (2010).
Article  CAS  Google Scholar 

8.
Wilkinson, C. R. In Status of Coral Reefs of the World: 2004 (Townsville: Australian Institute of Marine Science, 2004).
Google Scholar 

9.
Miller, J., Waara, R., Muller, E. & Rogers, C. Coral bleaching and disease combine to cause extensive mortality on reefs in US Virgin Islands. Coral Reefs 25, 418 (2006).
Article  Google Scholar 

10.
Donner, S. D., Knutson, T. R. & Oppenheimer, M. Model-based assessment of the role of human-induced climate change in the 2005 Caribbean coral bleaching event. Proc. Natl. Acad. Sci. 104, 5483–5488 (2007).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

11.
Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nat. 543, 373–377 (2017).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

12.
Gardner, T. A., Côté, I. M., Gill, J. A., Grant, A. & Watkinson, A. R. Hurricanes and Caribbean coral reefs: impacts, recovery patterns, and role in long-term decline. Ecol. 86, 174–184 (2005).
Article  Google Scholar 

13.
Smith, S. R. Patterns of Coral Recruitment and Post-Settlement Mortality on Bermuda’s Reefs: Comparisons to Caribbean and Pacific Reefs. Am. Zool. 32, 663–673 (1992).
Article  Google Scholar 

14.
Arnold, S. N. & Steneck, R. S. Settling into an Increasingly Hostile World: The Rapidly Closing “Recruitment Window” for Corals. PLoS ONE 6, e28681 (2011).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

15.
Edmunds, P. J. et al. Geographic variation in long-term trajectories of change in coral recruitment: a global-to-local perspective. Mar. Freshw. Res. 66, 609–622 (2015).
Article  Google Scholar 

16.
Glassom, D., Zakai, D. & Chadwick-Furman, N. Coral recruitment: a spatio-temporal analysis along the coastline of Eilat, northern Red Sea. Mar. Biol. 144, 641–651 (2004).
Article  Google Scholar 

17.
Edmunds, P. J. et al. Why more comparative approaches are required in time-series analyses of coral reef ecosystems. Mar. Ecol. Prog. Ser. 608, 297–306 (2019).
ADS  Article  Google Scholar 

18.
Hughes, T. P. Catastrophes, Phase Shifts, and Large-Scale Degradation of a Caribbean Coral Reef. Sci. 265, 1547–1551 (1994).
ADS  CAS  PubMed  Article  Google Scholar 

19.
Jackson, J. B. C. et al. Historical Overfishing and the Recent Collapse of Coastal Ecosystems. Sci. 293, 629–637 (2001).
CAS  PubMed  Article  PubMed Central  Google Scholar 

20.
McCook, L. Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18, 357–367 (1999).
Article  Google Scholar 

21.
Loh, T., McMurray, S. E., Henkel, T. P., Vicente, J. & Pawlik, J. R. Indirect effects of overfishing on Caribbean reefs: sponges overgrow reef-building corals. PeerJ 3, e901 (2015).
PubMed  PubMed Central  Article  Google Scholar 

22.
Lenz, E., Bramanti, L., Lasker, H. & Edmunds, P. J. Long-term variation of octocoral populations in St. John, US Virgin Islands. Coral Reefs 34, 1099–1109 (2015).
ADS  Article  Google Scholar 

23.
Gleason, D. F. & Hofmann, D. K. Coral larvae: From gametes to recruits. J. Exp. Mar. Biol. Ecol. 408, 42–57 (2011).
Article  Google Scholar 

24.
Siboni, N. et al. Using Bacterial Extract along with Differential Gene Expression in Acropora millepora Larvae to Decouple the Processes of Attachment and Metamorphosis. PLoS ONE 7, e37774 (2012).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

25.
Doropoulos, C. et al. Characterizing the ecological trade-offs throughout the early ontogeny of coral recruitment. Ecol. Monogr. 86, 20–44 (2016).
Google Scholar 

26.
Ritson-Williams, R., Arnold, S. N., Paul, V. J. & Steneck, R. S. Larval settlement preferences of Acropora palmata and Montastraea faveolata in response to diverse red algae. Coral Reefs 33, 59–66 (2014).
ADS  Article  Google Scholar 

27.
Ritson-Williams, R., Paul, V. J., Arnold, S. N. & Steneck, R. S. Larval settlement preferences and post-settlement survival of the threatened caribbean corals Acropora palmata and A. cervicornis. Coral Reefs 29, 71–81 (2010).
ADS  Article  Google Scholar 

28.
Johnson, C. R., Muir, D. G. & Reysenbach, A. L. Characteristic bacteria associated with surfaces of coralline algae: a hypothesis for bacterial induction of marine invertebrate larvae. Mar. Ecol. Prog. Ser. 74, 281–294 (1991).
ADS  Article  Google Scholar 

29.
Heyward, A. J. & Negri, A. P. Natural inducers for coral larval metamorphosis. Coral Reefs 18, 273–279 (1999).
Article  Google Scholar 

30.
Webster, N. S. et al. Metamorphosis of a Scleractinian Coral in Response to Microbial Biofilms. Appl. Environ. Microbiol. 70, 1213–1221 (2004).
CAS  PubMed  PubMed Central  Article  Google Scholar 

31.
Hadfield, M. G. Biofilms and Marine Invertebrate Larvae: What Bacteria Produce that Larvae Use to Choose Settlement Sites. Annu. Rev. Mar. Sci. 3, 453–470 (2011).
ADS  Article  Google Scholar 

32.
Sneed, J. M., Ritson-Williams, R. & Paul, V. J. Crustose coralline algal species host distinct bacterial assemblages on their surfaces. ISME J. 9, 2527–2536 (2015).
PubMed  PubMed Central  Article  Google Scholar 

33.
Negri, A. P., Webster, N. S., Hill, R. T. & Heyward, A. J. Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae. Mar. Ecol. Prog. Ser. 223, 121–131 (2001).
ADS  Article  Google Scholar 

34.
Sneed, J. M., Sharp, K. H., Ritchie, K. B. & Paul, V. J. The chemical cue tetrabromopyrrole from a biofilm bacterium induces settlement of multiple Caribbean corals. Proc. Royal Soc. B 281, 20133086 (2014).
PubMed  Article  CAS  PubMed Central  Google Scholar 

35.
Tebben, J. et al. Induction of Larval Metamorphosis of the Coral Acropora millepora by Tetrabromopyrrole Isolated from a Pseudoalteromonas Bacterium. PLoS ONE 6, e19082 (2011).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

36.
Tebben, J. et al. Chemical mediation of coral larval settlement by crustose coralline algae. Sci. Reports 5, 10803 (2015).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

37.
Morse, D. E., Morse, A. N. C., Raimondi, P. T. & Hooker, N. Morphogen-Based Chemical Flypaper for Agaricia humilis Coral Larvae. The Biol. Bull. 186, 172–181 (1994).
CAS  PubMed  Article  Google Scholar 

38.
Raimondi, P. T. & Morse, A. N. C. The consequences of complex larval behavior in a coral. Ecol. 81, 3193–3211 (2000).
Article  Google Scholar 

39.
Antonius, A. & Ballesteros, E. Epizoism: a new threat to coral health in Caribbean reefs. Revista de Biol. Trop. 46, 145–156 (1998).
Google Scholar 

40.
Verlaque, M., Ballesteros, E. & Antonius, A. Metapeyssonnelia corallepida sp. nov. (Peyssonneliaceae, Rhodophyta), an Atlantic Encrusting Red Alga Overgrowing Corals. Bot. Mar. 43, 191–200 (2000).

41.
Pueschel, C. M. & Saunders, G. W. Ramicrusta textilis sp. nov. (Peyssonneliaceae, Rhodophyta), an anatomically complex Caribbean alga that overgrows corals. Phycol. 48, 480–491 (2009).
Article  Google Scholar 

42.
Eckrich, C. E., Engel, M. S. & Peachey, R. B. J. Crustose, calcareous algal bloom (Ramicrusta sp.) overgrowing scleractinian corals, gorgonians, a hydrocoral, sponges, and other algae in Lac Bay, Bonaire, Dutch Caribbean. Coral Reefs 30, 131–131 (2011)

43.
Eckrich, C. E. & Engel, M. S. Coral overgrowth by an encrusting red alga (Ramicrusta sp.): a threat to Caribbean reefs?. Coral Reefs 32, 81–84 (2013).

44.
Ballantine, D. & Ruiz, H. Metapeyssonnelia milleporoides, a new species of coral-killing red alga (Peyssonneliaceae) from Puerto Rico, Caribbean Sea. Bot. Mar. 54, 47–51 (2011).

45.
Edmunds, P. J., Zimmerman, S. A. & Bramanti, L. A spatially aggressive peyssonnelid algal crust (PAC) threatens shallow coral reefs in St. John, US Virgin Islands. Coral Reefs 38, 1329–1341 (2019).

46.
Basso, D. Carbonate production by calcareous red algae and global change. Geodiversitas 34, 13–33 (2012).

47.
Taylor, W. & Arndt, C. The marine algae of the southwestern Peninsula of Hispaniola. Am. J. Bot. 16, 651–662 (1929).

48.
Van Den Hoek, C., Cortel-Breeman, A. & Wanders, J. Algal zonation in the fringing coral reef of Curaçao, Netherlands Antilles, in relation to zonation of corals and gorgonians. Aquatic. Bot. 1, 269–308 (1975).

49.
Sammarco, P. W. Effects of grazing by Diadema antillarum Philippi (Echinodermata: Echinoidea) on algal diversity and community structure. J. Exp. Mar. Biol. Ecol. 65, 83–105 (1982).

50.
Littler, M. M., Taylor, P. R., Littler, D. S., Sims, R. H. & Norris, J. N. Dominant macrophyte standing stocks, productivity and community structure on a Belizean barrier-reef. Atoll Res. Bull. 302, 1–24 (1987).

51.
Ballantine, D. & Ruiz, H. A unique red algal reef formation in Puerto Rico. Coral Reefs 32, 411–411 (2013).

52.
Ballantine, D., Ruiz, H., Lozada-Troche, C. & Norris, J. N. The genus Ramicrusta (Peyssonneliales, Rhodophyta) in the Caribbean Sea, including Ramicrusta bonairensis sp. nov. and Ramicrusta monensis sp. nov. Bot. Mar. 59, 417–431 (2016).

53.
Zhang, D. & Zhou, J. Ramicrusta, a new genus of Peyssonneliaceae (Cryptonemiales, Rhodophyta). Oceanol. et Limnol. Sinica 12, 538–544 (1981).

54.
Bramanti, L., Lasker, H. R. & Edmunds, P. J. An encrusting peyssonnellid preempts vacant space and overgrows corals in St. John, US Virgin Islands. Reef Encount. 32, 68–70 (2017).

55.
Tran, C. & Hadfield, M. G. Larvae of Pocillopora damicornis (Anthozoa) settle and metamorphose in response to surface-biofilm bacteria. Mar. Ecol. Prog. Ser. 433, 85–96 (2011).

56.
Golbuu, Y. & Richmond, R. H. Substratum preferences in planula larvae of two species of scleractinian corals, Goniastrea retiformis and Stylaraea punctata. Mar. Biol. 152, 639–644 (2007).

57.
Longford, S. R. et al. Comparisons of diversity of bacterial communities associated with three sessile marine eukaryotes. Aquatic. Microb. Ecol. 48, 217–229 (2007).

58.
Shade, A. & Handelsman, J. Beyond the Venn diagram: the hunt for a core microbiome. Environ. Microbiol. 14, 4–12 (2011).

59.
Edmunds, P. J. The hidden dynamics of low coral cover communities. Hydrobiol. 818, 193–209 (2018).

60.
Green, D. H., Edmunds, P. J., Pochon, X. & Gates, R. D. The effects of substratum type on the growth, mortality, and photophysiology of juvenile corals in St. John, US Virgin Islands. J. Exp. Mar. Biol. Ecol. 384, 18–29 (2010).

61.
Holmström, C. & Kjelleberg, S. Marine Pseudoalteromonas species are associated with higher organisms and produce biologically active extracellular agents. FEMS Microbiol. Ecol. 30, 285–293 (1999).

62.
Offret, C. et al. Spotlight on Antimicrobial Metabolites from the Marine Bacteria Pseudoalteromonas: Chemodiversity and Ecological Significance. Mar. Drugs 14, 129 (2016).

63.
Huang, Y.-L., Dobretsov, S., Xiong, H. & Qian, P.-Y. Effect of Biofilm Formation by Pseudoalteromonas spongiae on Induction of Larval Settlement of the Polychaete Hydroides elegans. Appl. Environ. Microbiol. 73, 6284–6288 (2007).

64.
Wolfaardt, G. M., Lawrence, J. R. & Korber, D. R. Function of EPS. In Wingender, J., Neu, T. R. & Flemming, H. (eds.) Microbial extracellular polymeric substances: characterization, structure, and function, 186–190 (Springer, New York, NY, 1999).
Google Scholar 

65.
Huggett, M. J., Williamson, J. E., de Nys, R., Kjelleberg, S. & Steinberg, P. D. Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae. Oecologia 149, 604–619 (2006).
ADS  PubMed  Article  Google Scholar 

66.
Shikuma, N. J., Antoshechkin, I., Medeiros, J. M., Pilhofer, M. & Newman, D. K. Stepwise metamorphosis of the tubeworm Hydroides elegans is mediated by a bacterial inducer and MAPK signaling. Proc. Natl. Acad. Sci. 113, 10097–10102 (2016).
CAS  PubMed  Article  Google Scholar 

67.
Freckleton, M. L., Nedved, B. T. & Hadfield, M. G. Induction of Invertebrate Larval Settlement; Different Bacteria, Different Mechanisms? Sci. Reports 7, 42557 (2017).

68.
Kato, A., Baba, M., Kawai, H. & Masuda, M. Reassessment of the little-known crustose red algal genus Polystrata (Gigartinales), based on morphology and SSU rDNA sequences. J. Phycol. 42, 922–933 (2006).

69.
Dixon, K. R. & Saunders, G. W. DNA barcoding and phylogenetics of Ramicrusta and Incendia gen. nov., two early diverging lineages of the Peyssonneliaceae (Rhodophyta). Phycol. 52, 82–108 (2013).

70.
Nieder, C., Chen, P.-C., Chen, C. A. & Liu, S.-L. New record of the encrusting alga Ramicrusta textilis overgrowing corals in the lagoon of Dongsha Atoll, South China Sea. Bull. Mar. Sci. 95, 459–462 (2019).

71.
Smith, T. B., Ennis, R., Kadison, E., Nemeth, R. S. & Henderson, L. The United States Virgin Islands Territorial Coral Reef Monitoring Program. 2016 Annu. Report, Univ. Virgin Islands, United States Virgin Islands 1–286 (2016).

72.
Adey, W. H. A survey of red algal biology and ecology with reference to carbonate geology, and the role of reds in algal ridge and reef construction. In Recent Advances in Carbonate Studies, vol. 6, 3–6 (West Indies Laboratory, St. Croix, USVI, 1974).

73.
Woelkerling, W. J. South Florida benthic marine algae. In Sedimenta V (University of Miami, 1976).

74.
Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Sci. 318, 1737–1742 (2007).

75.
Hay, M. E. Marine Chemical Ecology: Chemical Signals and Cues Structure Marine Populations, Communities, and Ecosystems. Annu. Rev. Mar. Sci. 1, 193–212 (2009).

76.
Schupp, P. J. & Paul, V. J. Calcium Carbonate and Secondary Metabolites in Tropical Seaweeds: Variable Effects on Herbivorous Fishes. Ecol. 75, 1172–1185 (1994).

77.
Pennings, S. C., Puglisi, M. P., Pitlik, T. J., Himaya, A. C. & Paul, V. J. Effects of secondary metabolites and CaCO(_{3}) on feeding by surgeonfishes and parrotfishes: within-plant comparisons. Mar. Ecol. Prog. Ser. 134, 49–58 (1996).

78.
Blunt, J. W. et al. Marine natural products. Nat. Prod. Reports 24, 31–86 (2007).

79.
Blunt, J. W. et al. Marine natural products. Nat. Prod. Reports 25, 35–94 (2008).

80.
Lane, A. L. et al. Ecological leads for natural product discovery: novel sesquiterpene hydroquinones from the red macroalga Peyssonnelia sp. Tetrahedron 66, 455–461 (2010).

81.
Sawabe, T. et al. Pseudoalteromonas bacteriolytica sp. nov., a marine bacterium that is the causative agent of red spot disease of Laminaria japonica. Int. J. Syst. Evol. Microbiol. 48, 769–774 (1998).

82.
Steneck, R. & Dethier, M. A Functional Group Approach to the Structure of Algal-Dominated Communities. Oikos 69, 476–498 (1994).

83.
Edmunds, P. J. Decadal-scale changes in the community structure of coral reefs of St. John, US Virgin Islands. Mar. Ecol. Prog. Ser. 489, 107–123 (2013).

84.
Wilson, B. et al. Changes in Marine Prokaryote Composition with Season and Depth Over an Arctic Polar Year. Front. Mar. Sci. 4, 95 (2017).

85.
Øvreås, L., Forney, L., Daae, F. L. & Torsvik, V. Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl. Environ. Microbiol. 63, 3367–3373 (1997).

86.
Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. 108, 4516–4522 (2011).

87.
Freshwater, D., Fredericq, S. & Bailey, J. Characteristics and utility of nuclear-encoded large-subunit ribosomal gene sequences in phylogenetic studies of red algae. Phycol. Res. 47, 33–38 (1999).

88.
Krayesky, D. M., Norris, J. N., Gabrielson, P. W., Gabriel, D. & Fredericq, S. A new order of red algae based on the Peyssonneliaceae, with an evaluation of the ordinal classification of the Florideophyceae (Rhodophyta). Proc. Biol. Soc. Wash. 122, 364–391 (2009).

89.
Yoon, H. S., Hackett, J. D. & Bhattacharya, D. A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc. Natl. Acad. Sci. 99, 11724–11729 (2002).

90.
Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–6 (2010).

91.
Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinforma. 26, 2460–2461 (2010).

92.
Haas, B. J. et al. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 21, 494–504 (2011).

93.
Caporaso, J. G. et al. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinforma. 26, 266–267 (2009).

94.
DeSantis, T. Z. et al. Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB. Appl. Environ. Microbiol. 72, 5069–5072 (2006).

95.
Joshi, N. A. & Fass, J. N. Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ files (Version 1.33) (2011). Available at https://github.com/najoshi/sickle. Accessed 6 Nov 2020.

96.
Rice, P., Longden, I. & Bleasby, A. EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet. 16, 276–277 (2000).

97.
Altschul, S., Gish, W., Miller, W., Myers, E. & Lipman, D. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

98.
GNU General Public License. URL http://www.gnu.org/licenses/gpl.html. Accessed 6 Nov 2020. More

1.
Herring, P. J. The Biology of the Deep Ocean (Oxford University Press, Oxford, 2007).
Google Scholar 
2.
Chapman, G. Transparency in organisms. Experientia 32, 123–125 (1976).
Article  Google Scholar 

3.
Bagge, L. E. Not as clear as it may appear: Challenges associated with transparent camouflage in the ocean. Integr. Comp. Biol. 59, 1653–1663 (2019).
Article  Google Scholar 

4.
Johnsen, S. Hide and seek in the open sea: Pelagic camouflage and visual countermeasures. Ann. Rev. Mar. Sci. 6, 369–392 (2014).
Article  Google Scholar 

5.
Kakiuchida, H., Sakai, D., Nishikawa, J. & Hirose, E. Measurement of refractive indices of tunicates’ tunics: Light reflection of the transparent integuments in an ascidian Rhopalaea sp. and a salp Thetys vagina. Zool. Lett. 3, 7 (2017).
Article  Google Scholar 

6.
Sakai, D., Kakiuchida, H., Nishikawa, J. & Hirose, E. Physical properties of the tunic in the pinkish-brown salp Pegea confoederata (Tunicata: Thaliacea). Zool. Lett. 4, 1–9 (2018).
Article  Google Scholar 

7.
Giguère, L. A. & Northcote, T. G. Ingested prey increase risks of visual predation in transparent Chaoborus larvae. Oecologia 73, 48–52 (1987).
ADS  Article  Google Scholar 

8.
Cronin, T. W. Camouflage: Being invisible in the open ocean. Curr. Biol. 26, R1179–R1181 (2016).
CAS  Article  Google Scholar 

9.
Hansson, L. A. Induced pigmentation in zooplankton: A trade-off between threats from predation and ultraviolet radiation. Proc. R. Soc. B Biol. Sci. 267, 2327–2331 (2000).
CAS  Article  Google Scholar 

10.
Johnsen, S. Hidden in plain sight: The ecology and physiology of organismal transparency. Biol. Bull. 201, 301–318 (2001).
CAS  Article  Google Scholar 

11.
Yasuo, H. & McDougall, A. Practical guide for ascidian microinjection: Phallusia mammillata. Adv. Exp. Med. Biol. 1029, 15–24 (2018).
CAS  Article  Google Scholar 

12.
Piliszek, A., Kwon, G. S. & Hadjantonakis, A.-K. Embryological methods in ascidians: The Villefranche-sur-Mer protocols. In Methods in Molecular Biology (Clifton, N.J.) Vol. 770 (ed. Pelegri, F. J.) 243–257 (Humana Press, Totowa, 2011).
Google Scholar 

13.
Burighel, P. & Cloney, R. A. Urochordata: Ascidiacea. Microscopic Anatomy of Invertebrates 221–347 (1997).

14.
Conklin, E. G. Mosaic development in ascidian eggs. J. Exp. Zool. 2, 145–223 (1905).
Article  Google Scholar 

15.
Jeffery, W. R. Identification of proteins and mRNAs in isolated yellow crescents of ascidian eggs. J. Embryol. Exp. Morphol. 89, 275–287 (1985).
CAS  PubMed  Google Scholar 

16.
Arai, M. N. Biological interactions. in A Functional Biology of Scyphozoa 203–223 (Springer Netherlands, 1997). https://doi.org/10.1007/978-94-009-1497-1_9

17.
Nishikawa, T. et al. Molecular and morphological discrimination between an invasive ascidian, Ascidiella aspersa, and its congener A. scabra (Urochordata: Ascidiacea). Zool. Sci. 31, 180–185 (2014).
CAS  Article  Google Scholar 

18.
Passamaneck, Y. J. & Di Gregorio, A. Ciona intestinalis: Chordate development made simple. Dev. Dyn. https://doi.org/10.1002/dvdy.20300 (2005).
Article  PubMed  Google Scholar 

19.
Dehal, P. et al. The draft genome of Ciona intestinalis: Insights into chordate and vertebrate origins. Science 298, 2157–2167 (2002).
ADS  CAS  Article  Google Scholar 

20.
Tassy, O. et al. The ANISEED database: Digital representation, formalization, and elucidation of a chordate developmental program. Genome Res. 20, 1459–1468 (2010).
CAS  Article  Google Scholar 

21.
Brozovic, M. et al. ANISEED 2017: Extending the integrated ascidian database to the exploration and evolutionary comparison of genome-scale datasets. Nucleic Acids Res. https://doi.org/10.1093/nar/gkx1108 (2017).
Article  PubMed Central  Google Scholar 

22.
Delsuc, F. F. et al. A phylogenomic framework and timescale for comparative studies of tunicates. BMC Biol. 16, 1–14 (2018).
Article  Google Scholar 

23.
Epel, D., Hemela, K., Shick, M. & Patton, C. Development in the floating world: Defenses of eggs and embryos against damage from UV radiation. Am. Zool. 39, 271–278 (1999).
Article  Google Scholar 

24.
Eaton, T. H. & Cott, H. B. Adaptive coloration in animals. Am. Midl. Nat. https://doi.org/10.2307/2420875 (1940).
Article  Google Scholar 

25.
Lindquist, N., Hay, M. E. & Fenical, W. Defense of ascidians and their conspicuous larvae: Adult vs larval chemical defenses. Ecol. Monogr. 62, 547–568 (1992).
Article  Google Scholar 

26.
Hirose, E., Ohtake, S.-I. & Azumi, K. Morphological characterization of the tunic in the edible ascidian, Halocynthia roretzi (Drasche), with remarks on ‘soft tunic syndrome’ in aquaculture. J. Fish Dis. 32, 433–445 (2009).
CAS  Article  Google Scholar 

27.
Jacobs, G. H. Ultraviolet vision in vertebrates. Am. Zool. 32, 544–554 (1992).
Article  Google Scholar 

28.
Karentz, D., Bosch, I. & Mitchell, D. M. Limited effects of Antarctic ozone depletion on sea urchin development. Mar. Biol. 145, 277–292 (2004).
CAS  Article  Google Scholar 

29.
Winckler, K. & Fidhiany, L. Combined effects of constant sublethal UVA irradiation and elevated temperature on the survival and general metabolism of the convict-cichlid fish, Cichlasoma nigrofasciatum. Photochem. Photobiol. 63, 487–491 (1996).
CAS  Article  Google Scholar 

30.
Bingham, B. L. & Reitzel, A. M. Solar damage to the solitary ascidian, Corella inflata. J. Mar. Biol. Assoc. UK 80, 515–521 (2000).
Article  Google Scholar 

31.
Hirose, E. Pigmentation and acid storage in the tunic: Protective functions of the tunic cells in the tropical ascidian Phallusia nigra. Invertebr. Biol. 118, 414 (1999).
Article  Google Scholar 

32.
Hirose, E., Hirabayashi, S., Hori, K., Kasai, F. & Watanabe, M. M. UV protection in the photosymbiotic ascidian Didemnum molle inhabiting different depths. Zool. Sci. 23, 57–63 (2006).
CAS  Article  Google Scholar 

33.
Olson, R. R. Ascidian-prochloron symbiosis: The role of larval photoadaptations in midday larval release and settlement. Biol. Bull. 165, 221–240 (1983).
Article  Google Scholar 

34.
Sensui, N. & Hirose, E. Cytoplasmic UV-R absorption in an integumentary matrix (Tunic) of photosymbiotic ascidian colonies. Zool. Stud. 57, 1–11 (2018).
Google Scholar 

35.
Hirose, E., Ohtsuka, K., Ishikura, M. & Maruyama, T. Ultraviolet absorption in ascidian tunic and ascidian-Prochloron symbiosis. J. Mar. Biol. Assoc. UK 84, 789–794 (2004).
CAS  Article  Google Scholar 

36.
Hansson, L. A. & Hylander, S. Effects of ultraviolet radiation on pigmentation, photoenzymatic repair, behavior, and community ecology of zooplankton. Photochem. Photobiol. Sci. 8, 1266–1275 (2009).
CAS  Article  Google Scholar 

37.
Hansson, L. A., Hylander, S. & Sommaruga, R. Escape from UV threats in zooplankton: A cocktail of behavior and protective pigmentation. Ecology 88, 1932–1939 (2007).
Article  Google Scholar 

38.
Pineda, M. C., Lorente, B., López-Legentil, S., Palacín, C. & Turon, X. Stochasticity in space, persistence in time: Genetic heterogeneity in harbour populations of the introduced ascidian Styela plicata. PeerJ 4, e2158 (2016).
Article  Google Scholar 

39.
Zaniolo, G., Burighel, P. & Martinucci, G. Ovulation and placentation in Botryllus schlosseri (Ascidiacea): An ultrastructural study. Can. J. Zool. 65, 1181–1190 (1987).
Article  Google Scholar 

40.
Mukai, H., Saito, Y. & Watanabe, H. Viviparous development in Botrylloides (compound ascidians). J. Morphol. 193, 263–276 (1987).
Article  Google Scholar 

41.
Burighel, P., Cloney, R. A. & Cloney, B. Microscopic anatomy of invertebrates. Microsc. Anat. Invertebr. 15, 221–347 (1997).
Google Scholar 

42.
Sardet, C. et al. Chapter 14 Embryological methods in ascidians: The Villefranche-sur-Mer protocols. Vertebr. Embryog. Methods Mol. Biol. 770, (2011).

43.
Chatterjee, A. et al. Cephalopod-inspired optical engineering of human cells. Nat. Commun. 11, 2708 (2020).
ADS  CAS  Article  Google Scholar 

44.
Tsagkogeorga, G. et al. An updated 18S rRNA phylogeny of tunicates based on mixture and secondary structure models. BMC Evol. Biol. 9, 187 (2009).
Article  Google Scholar 

45.
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. https://doi.org/10.1071/ZO9660275 (1994).
Article  PubMed  Google Scholar 

46.
Hasegawa, N. & Kajihara, H. A redescription of syncarpa composita (Ascidiacea, stolidobranchia) with an inference of its phylogenetic position within styelidae. Zookeys 2019, 1–15 (2019).
CAS  Article  Google Scholar 

47.
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. https://doi.org/10.1093/molbev/mst010 (2013).
Article  PubMed  PubMed Central  Google Scholar 

48.
Castresana, J. Estimation of genetic distances from human and mouse introns. Genome Biol. https://doi.org/10.1186/gb-2002-3-6-research0028 (2002).
Article  PubMed  PubMed Central  Google Scholar 

49.
Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. https://doi.org/10.1093/molbev/msw054 (2016).
Article  PubMed  PubMed Central  Google Scholar 

50.
Stamatakis, A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. https://doi.org/10.1093/bioinformatics/btu033 (2014).
Article  PubMed  PubMed Central  Google Scholar 

51.
Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics https://doi.org/10.1093/bioinformatics/17.8.754 (2001).
Article  PubMed  Google Scholar 

52.
Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics https://doi.org/10.1093/bioinformatics/btg180 (2003).
Article  PubMed  Google Scholar 

53.
Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T. & Calcott, B. Partitionfinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. https://doi.org/10.1093/molbev/msw260 (2017).
Article  PubMed  Google Scholar 

54.
Rambaut, A., Drummond, A. J., Xie, D., Baele, G. & Suchard, M. A. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67, 901–904 (2018).
CAS  Article  Google Scholar  More

To the Editor — A wildlife consumption ban, which China enacted in February as a response to the COVID-19 pandemic, has been welcomed by most conservationists as a step towards avoiding a future outbreak of zoonotic diseases1. There are dissenting voices against this ban, arguing that wildlife generates multiple benefits for people who co-exist with wild species2. While both schools of thought have their own valid arguments, neither has yet to actively lobby for the free, prior and informed consent or consultation of the people who will be directly affected by conservation decisions related to COVID-19.

Throughout the years, indigenous peoples and local communities (IPLCs) have been seen as either culprits of biodiversity decline or as ‘unseen sentinels’ effectively managing and monitoring their territories, which are often highly biodiverse3. This polarized view of IPLCs signals a prevailing lack of understanding of their way of life, where most of their dependence on nature is on a subsistence level. Wildlife consumption is often an essential part of their diets. A blanket ban on wildlife consumption may, therefore, exacerbate food insecurity in these communities. In other cases, IPLC wildlife consumption is more than just for subsistence. It may also have cultural roots and should be respected in that regard. Calling for education campaigns to ‘discredit engrained cultural beliefs’ that lead to wildlife consumption ignores the dynamics of cultural development and would most likely fail to conserve wildlife or fail to prevent another zoonotic disease outbreak4. What is needed is to craft bottom-up solutions together with the IPLCs directly depending on wildlife and to learn from their nuanced understanding of nature.

Through creating opportunities and spaces for dialogue, governments and institutions can involve IPLCs in setting guidelines for wildlife consumption. They can adopt the dialogue approach employed by the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES), where IPLCs engage in knowledge exchange with technical experts and government representatives5. The dialogue, through parallel contributions of indigenous, local, scientific and practical knowledge, can enhance the understanding of wildlife consumption6. Governments and institutions can tap into the network of non-governmental organizations (NGOs) that closely collaborate with IPLCs and have them facilitate these dialogues. They need to listen carefully to IPLCs, learn from their customary protocols on wildlife use and consumption, and draft laws that could potentially prevent another zoonotic disease outbreak without jeopardizing the livelihoods and well-being of IPLCs. Likewise, IPLCs and civil society can continue to build on processes of self-strengthening and assert themselves in spaces where they can proactively engage in efforts to raise awareness and understanding of traditional wildlife consumption practices. These multiple stakeholders must work together to co-craft potential solutions to this global yet also very local concern of wildlife consumption and its connection to zoonotic diseases.

References

1.
Butler, R. A. Conservationists welcome China’s wildlife trade ban. Mongabay (26 January 2020); https://go.nature.com/3pohgzZ

2.
Roe, D. Despite COVID-19, using wild species may still be the best way to save them. International Institute for Environment and Development (1 April 2020); https://go.nature.com/3pjRNYt

3.
Sheil, D., Boissière, M. & Beaudoin, G. Ecol. Soc. 20, 39 (2015).
Article  Google Scholar 

4.
Ribeiro, J., Bingre, P., Strubbe, D. & Reino, L. Nature 578, 217 (2020).
CAS  Article  Google Scholar 

5.
Hill, R. et al. Curr. Opin. Environ. Sustain. 43, 8–20 (2020).
Article  Google Scholar 

6.
Tengö, M., Brondizio, E. S., Elmqvist, T., Malmer, P. & Spierenburg, M. AMBIO 43, 579–591 (2014).
Article  Google Scholar 

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Author information

Affiliations

Center for Development Research (ZEF) Bonn, University of Bonn, Bonn, Germany
Denise Margaret S. Matias

Institute for Social-Ecological Research (ISOE), Frankfurt am Main, Germany
Denise Margaret S. Matias

Non-Timber Forest Products Exchange Programme (NTFP-EP) Asia, Quezon City, Philippines
Eufemia Felisa Pinto & Diana San Jose

Non-Timber Forest Products Exchange Programme (NTFP-EP) India, c/o Keystone Foundation, Kotagiri, India
Madhu Ramnath

Authors
Denise Margaret S. Matias

Eufemia Felisa Pinto

Madhu Ramnath

Diana San Jose

Contributions
D.M.S.M. conceptualized and drafted the Correspondence. E.F.P. and D.S.J. provided input. M.R. reviewed the Correspondence.
Corresponding author
Correspondence to Denise Margaret S. Matias.

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Competing interests
The authors declare no competing interests.

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Matias, D.M.S., Pinto, E.F., Ramnath, M. et al. Local communities and wildlife consumption bans. Nat Sustain (2020). https://doi.org/10.1038/s41893-020-00662-7
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