More stories

  • in

    Functional traits explain crayfish invasive success in the Netherlands

    1.
    Keller, R. P., Geist, J., Jeschke, J. M. & Kühn, I. Invasive species in Europe: ecology, status, and policy. Environ. Sci. Eur. 23, 1–17 (2011).
    Article  Google Scholar 
    2.
    Parker, M., Thompson, J. N. & Weller, S. G. The population biology of invasive species. Annu. Rev. Ecol. Syst. 32, 305–332 (2001).
    Article  Google Scholar 

    3.
    Allendorf, F. W. & Lundquist, L. L. Introduction: population biology, evolution, and control of invasive species. Conserv. Biol. 17, 24–30 (2003).
    Article  Google Scholar 

    4.
    Crowl, T. A., Crist, T. O., Parmenter, R. R., Belovsky, G. & Lugo, A. E. The spread of invasive species and infectious disease as drivers of ecosystem change. Front. Ecol. Environ. 6, 238–246 (2008).
    Article  Google Scholar 

    5.
    van der Veer, G. & Nentwig, W. Environmental and economic impact assessment of alien and invasive fish species in Europe using the generic impact scoring system. Ecol. Freshw. Fish 24, 646–656 (2015).
    Article  Google Scholar 

    6.
    Clavero, M. & García-Berthou, E. Invasive species are a leading cause of animal extinctions. Trends Ecol. Evol. 20, 110 (2005).
    PubMed  Article  PubMed Central  Google Scholar 

    7.
    Scalera, R. How much is Europe spending on invasive alien species?. Biol. Invasions 12, 173–177 (2010).
    Article  Google Scholar 

    8.
    Sala, O. E. et al. Global biodiversity scenarios for the year 2100. Science 287, 1770–1774 (2000).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    9.
    McLellan, R., Iyengar, L., Jeffries, B. & Oerlemans, N. Living Planet Report 2014: Species and Spaces, People and Places (WWF International, Gland, 2014).
    Google Scholar 

    10.
    García-Berthou, E. et al. Introduction pathways and establishment rates of invasive aquatic species in Europe. Can. J. Fish. Aquat. Sci. 62, 453–463 (2005).
    Article  Google Scholar 

    11.
    Karatayev, A. Y., Burlakova, L. E., Padilla, D. K., Mastitsky, S. E., & Olenin, S. Invaders are not a random selection of species. Biol. Invasions, 11, 2009. https://doi.org/10.1007/s10530-009-9498-0 (2009).
    Article  Google Scholar 

    12.
    Verdonschot, R. C. M., Vos, J. H., & Verdonschot, P. F. M. Exotische macrofauna en macrofyten in de Nederlandse zoete wateren: voorkomen en beleid in 2012. (WOt-werkdocument 334) (Wettelijke Onderzoekstaken Natuur & Milieu, 2013).

    13.
    Holdich, D. M., Reynolds, J. D., Souty-Grosset, C. & Sibley, P. J. A review of the ever increasing threat to European crayfish from non-indigenous crayfish species. Knowl. Manag. Aquat. Ecosyst. 394–395, 11 (2009).
    Article  Google Scholar 

    14.
    Chucholl, C. Invaders for sale: trade and determinants of introduction of ornamental freshwater crayfish. Biol. Invasions 15, 125–141 (2013).
    Article  Google Scholar 

    15.
    Barbaresi, S. & Gherardi, F. The invasion of the alien crayfish Procambarus clarkii in Europe, with particular reference to Italy. Biol. Invasions 2, 259–264 (2000).
    Article  Google Scholar 

    16.
    Gherardi, F. Crayfish invading Europe: the case study of Procambarus clarkii. Mar. Freshw. Behav. Physiol. 39, 175–191 (2006).
    Article  Google Scholar 

    17.
    Kouba, A., Petrusek, A. & Kozák, P. Continental-wide distribution of crayfish species in Europe: update and maps. Knowl. Manag. Aquat. Ecosyst. 413, 5 (2014).
    Article  Google Scholar 

    18.
    Lowe, S., Browne, M., Boudjelas, S., & De Poorter, M. 100 of the world’s worst invasive alien species: a selection from the global invasive species database in Aliens vol. 12 (Invasive Species Specialist Group, 2000).

    19.
    Padilla, D. K. & Williams, S. L. Beyond ballast water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Front. Ecol. Environ. 2, 131–138 (2004).
    Article  Google Scholar 

    20.
    Faulkes, Z. The global trade in crayfish as pets. Crustacean Res. 44, 75–92 (2015).
    Article  Google Scholar 

    21.
    Soes, D. M., & Koese, B. Invasive Crayfish in the Netherlands: A Preliminary Risk Analysis. (Bureau Waardenburg bv, Stichting EIS-Nederland, Invasive Alien Species Team, 2010).

    22.
    Chucholl, C. & Wendler, F. Positive selection of beautiful invaders: long-term persistence and bio-invasion risk of freshwater crayfish in the pet trade. Biol. Invasions 19, 197–208 (2017).
    Article  Google Scholar 

    23.
    Zeng, Y., Chong, K. Y., Grey, E. K., Lodge, D. M. & Yeo, D. C. Disregarding human pre-introduction selection can confound invasive crayfish risk assessments. Biol. Invasions 17, 2373–2385 (2015).
    Article  Google Scholar 

    24.
    Blackburn, T. M. et al. A proposed unified framework for biological invasions. Trends Ecol. Evol. 26, 333–339 (2011).
    PubMed  Article  Google Scholar 

    25.
    Statzner, B., Bonada, N. & Dolédec, S. Biological attributes discriminating invasive from native European stream macroinvertebrates. Biol. Invasions 10, 517–530 (2008).
    Article  Google Scholar 

    26.
    Whitney, K. D. & Gabler, C. A. Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Divers. Distrib. 14, 569–580 (2008).
    Article  Google Scholar 

    27.
    Kolar, C. S. & Lodge, D. M. Progress in invasion biology: predicting invaders. Trends Ecol. Evol. 16, 199–204 (2001).
    PubMed  Article  Google Scholar 

    28.
    Marchetti, M. P., Moyle, P. B. & Levine, R. Invasive species profiling? Exploring the characteristics of non-native fishes across invasion stages in California. Freshw. Biol. 49, 646–661 (2004).
    Article  Google Scholar 

    29.
    Grabowski, M., Bacela, K. & Konopacka, A. How to be an invasive gammarid (Amphipoda: Gammaroidea)-comparison of life history traits. Hydrobiologia 590, 75–84 (2007).
    Article  Google Scholar 

    30.
    Thiébaut, G. Invasion success of non-indigenous aquatic and semi-aquatic plants in their native and introduced ranges. A comparison between their invasiveness in North America and in France. Biol. Invasions 9, 1–12 (2007).
    Article  Google Scholar 

    31.
    Swart, C., Visser, V. & Robinson, T. B. Patterns and traits associated with invasions by predatory marine crabs. NeoBiota 39, 79 (2018).
    Article  Google Scholar 

    32.
    Larson, E. R. & Olden, J. D. Latent extinction and invasion risk of crayfishes in the southeastern United States. Conserv. Biol. 24, 1099–1110 (2010).
    PubMed  Article  PubMed Central  Google Scholar 

    33.
    Tricarico, E., Vilizzi, L., Gherardi, F. & Copp, G. H. Calibration of FI-ISK, an invasiveness screening tool for nonnative freshwater invertebrates. Risk Anal. Int. J. 30, 285–292 (2010).
    Article  Google Scholar 

    34.
    Larson, E. R. & Olden, J. D. Using avatar species to model the potential distribution of emerging invaders. Glob Ecol. Biogeogr. 21, 1114–1125 (2012).
    Article  Google Scholar 

    35.
    Veselý, L., Buřič, M. & Kouba, A. Hardy exotics species in temperate zone: can “warm water” crayfish invaders establish regardless of low temperatures?. Sci. Rep. 5, 16340 (2015).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    36.
    Jaklič, M. & Vrezec, A. The first tropical alien crayfish species in European waters: the redclaw Cherax quadricarinatus (Von Martens, 1868) (Decapoda, Parastacidae). Crustaceana 84, 651–665 (2011).
    Article  Google Scholar 

    37.
    Colautti, R. I., Grigorovich, I. A. & MacIsaac, H. J. Propagule pressure: a null model for biological invasions. Biol. Invasions 8, 1023–1037 (2006).
    Article  Google Scholar 

    38.
    Marchetti, M. P., Moyle, P. B. & Levine, R. Alien fishes in California watersheds: characteristics of successful and failed invaders. Ecol. Appl. 14, 587–596 (2004).
    Article  Google Scholar 

    39.
    Bennett, S. N., Olson, J. R., Kershner, J. L. & Corbett, P. Propagule pressure and stream characteristics influence introgression: cutthroat and rainbow trout in British Columbia. Ecol. Appl. 20, 263–277 (2010).
    PubMed  Article  PubMed Central  Google Scholar 

    40.
    Cruz, M. J. & Rebelo, R. Colonization of freshwater habitats by an introduced crayfish, Procambarus clarkii Southwest Iberian Peninsula. Hydrobiologia 575, 191–201 (2007).
    Article  Google Scholar 

    41.
    Lynas, J., Storey, A. W. & Knott, B. Aggressive interactions between three species of freshwater crayfish of the genus Cherax (Decapoda: Parastacidae). Mar. Freshw. Behav. Physiol. 40, 105–116 (2007).
    Article  Google Scholar 

    42.
    Corey, S. Comparative fecundity of four species of crayfish in southwestern Ontario, Canada (Decapoda, Astacidea). Crustaceana 52(3), 276–286 (1987).
    Article  Google Scholar 

    43.
    Somers, K. M. Characterizing size-specific fecundity in crustaceans. Crustacean Egg Prod. 7, 357–378 (1991).
    Google Scholar 

    44.
    Maguire, I., Klobučar, G. I. V. & Erben, R. The relationship between female size and egg size in the freshwater crayfish Austropotamobius torrentium. Bulletin Français de la Pêche et de la Pisciculture 376–377, 777–785 (2005).
    Article  Google Scholar 

    45.
    Pilotto, F. et al. The invasive crayfish Faxonius limosus in Lake Varese: estimating abundance and population size structure in the context of habitat and methodological constraints. J. Crustacean Biol. 28, 633–640 (2008).
    Article  Google Scholar 

    46.
    Hobbs Jr, H. H. A checklist of the North and Middle American crayfishes (Decapoda: Astacidae and Cambaridae). Smithsonian Contrib. Zool. 166, 1–161 (1974).
    Google Scholar 

    47.
    Mrugała, A. et al. Trade of ornamental crayfish in Europe as a possible introduction pathway for important crustacean diseases: crayfish plague and white spot syndrome. Biol. Invasions 17, 1313–1326 (2015).
    Article  Google Scholar 

    48.
    Svoboda, J., Mrugała, A., Kozubíková-Balcarová, E. & Petrusek, A. Hosts and transmission of the crayfish plague pathogen Aphanomyces astaci: a review. J. Fish Dis. 40, 127–140 (2017).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    49.
    Grandjean, F. et al. Status of Pacifastacus leniusculus and its role in recent crayfish plague outbreaks in France: improving distribution and crayfish plague infection patterns. Aquat. Invasions, 12, 541–549 (2017).
    Article  Google Scholar 

    50.
    Crandall, K. A. & De Grave, S. An updated classification of the freshwater crayfishes (Decapoda: Astacidea) of the world, with a complete species list. J. Crustacean Biol. 37, 615–653 (2017).
    Article  Google Scholar 

    51.
    Freshwater Crayfish: A Global Overview. (ed. Kawai, T., Faulkes, Z., & Scholtz, G.) (CRC Press, Boca Raton, 2015).

    52.
    Buřič, M., Kouba, A. & Kozak, P. Reproductive plasticity in freshwater invader: from long-term sperm storage to parthenogenesis. PLoS ONE 8, e77597. https://doi.org/10.1371/journal.pone.0077597 (2013).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    53.
    Kaldre, K., Meženin, A., Paaver, T., & Kawai, T. A preliminary study on the tolerance of marble crayfish Procambarus fallax f. virginalis to low temperature in Nordic climate in Freshwater crayfish: global overview, 54–62 (2016).

    54.
    Vogt, G. Marmorkrebs: natural crayfish clone as emerging model for various biological disciplines. J. Biosci. 36, 377–382 (2011).
    PubMed  Article  Google Scholar 

    55.
    Chucholl, C. Predicting the risk of introduction and establishment of an exotic aquarium animal in Europe: insights from one decade of Marmorkrebs (Crustacea, Astacida, Cambaridae) releases. Biol. Invasions 5, 309–318 (2014).
    Article  Google Scholar 

    56.
    Chucholl, C., Morawetz, K. & Groß, H. The clones are coming–strong increase in Marmorkrebs [Procambarus fallax (Hagen, 1870) f. virginalis] records from Europe. Aquat. Invasions 7, 511–519 (2012).
    Article  Google Scholar 

    57.
    Soes, D. M. & van Eekelen, R. Rivierkreeften, een oprukkend probleem?. De Levende Natuur 107, 56–59 (2006).
    Google Scholar 

    58.
    Mauvisseau, Q., Tönges, S., Andriantsoa, R., Lyko, F. & Sweet, M. Early detection of an emerging invasive species: eDNA monitoring of a parthenogenetic crayfish in freshwater systems. Manag. Biol. Invasions 10, 461 (2019).
    Article  Google Scholar 

    59.
    Strand, D. A. et al. Monitoring a Norwegian freshwater crayfish tragedy: eDNA snapshots of invasion, infection and extinction. J. Appl. Ecol. 56, 1661–1673 (2019).
    CAS  Article  Google Scholar 

    60.
    Beentjes, K. K., Speksnijder, A. G., Schilthuizen, M., Schaub, B. E. & van der Hoorn, B. B. The influence of macroinvertebrate abundance on the assessment of freshwater quality in The Netherlands. Metabarcoding Metagenom. 2, e26744 (2018).
    Article  Google Scholar 

    61.
    Melo-Merino, S. M., Reyes-Bonilla, H. & Lira-Noriega, A. Ecological niche models and species distribution models in marine environments: a literature review and spatial analysis of evidence. Ecol. Model. 415, 108837 (2020).
    Article  Google Scholar 

    62.
    Zhang, Z. et al. Impacts of climate change on the global potential distribution of two notorious invasive crayfishes. Freshw. Biol. 65, 353–365 (2020).
    Article  Google Scholar 

    63.
    Capinha, C., Leung, B. & Anastácio, P. Predicting worldwide invasiveness for four major problematic decapods: an evaluation of using different calibration sets. Ecography 34, 448–459 (2011).
    Article  Google Scholar 

    64.
    Havel, J. E., Kovalenko, K. E., Thomaz, S. M., Amalfitano, S. & Kats, L. B. Aquatic invasive species: challenges for the future. Hydrobiologia 750, 147–170 (2015).
    PubMed  PubMed Central  Article  Google Scholar 

    65.
    Früh, D., Stoll, S. & Haase, P. Physicochemical and morphological degradation of stream and river habitats increases invasion risk. Biol. Invasions 14, 2243–2253 (2012).
    Article  Google Scholar 

    66.
    Ghalambor, C. K., McKay, J. K., Carroll, S. P. & Reznick, D. N. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21, 394–407 (2007).
    Article  Google Scholar 

    67.
    Scalici, M. et al. The new threat to Italian inland waters from the alien crayfish “gang”: the Australian Cherax destructor Clark, 1936. Hydrobiologia 632, 341–345 (2009).
    Article  Google Scholar 

    68.
    Koese, B. & Evers, C. H. M. A National Inventory of Invasive Freshwater Crayfish in the Netherlands in 2010 (EIS, Stichting European Invertebrate Survey Nederland, 2011).
    Google Scholar 

    69.
    Clement, J., & van Puijenbroek, P. Basiskaart Aquatisch: de Watertypenkaart Het oppervlaktewater in de TOP10NL geclassificeerd naar watertype (No. 500067004). (Planbureau voor de Leefomgeving 2010).

    70.
    Peel, M. C., Finlayson, B. L. & McMahon, T. A. Updated world map of the Köppen-Geiger climate classification. Hydrol. Earth Syst. Sci. Discuss. 4, 439–473 (2007).
    ADS  Google Scholar 

    71.
    Lyko, F. The marbled crayfish (Decapoda: Cambaridae) represents an independent new species. Zootaxa 4363(4), 544–552 (2017).
    PubMed  Article  PubMed Central  Google Scholar 

    72.
    Usseglio-Polatera, P. & Tachet, H. Theoretical habitat templets, species traits, and species richness: Plecoptera and Ephemeroptera in the Upper Rhône River and its floodplain. Freshw. Biol. 31, 357–375 (1994).
    Article  Google Scholar 

    73.
    Poff, N. L. et al. Functional trait niches of North American lotic insects: traits-based ecological applications in light of phylogenetic relationships. J. North Am. Benthological. Soc. 25, 730–755 (2006).
    Article  Google Scholar 

    74.
    Wyse, S. V. et al. A quantitative assessment of shoot flammability for 60 tree and shrub species supports rankings based on expert opinion. Int. J. Wildland Fire 25, 466–477 (2016).
    Article  Google Scholar 

    75.
    Hill, M. O. TWINSPAN. A FORTRAN program for arranging multivariate data in an ordered two-way table by classification of the individuals and attributes. (Ecology and Systematics, Cornell University, 1979).

    76.
    Hu, G. et al. Regeneration of different plant functional types in a Masson pine forest following pine wilt disease. PLoS ONE 7, e36432. https://doi.org/10.1371/journal.pone.0036432 (2012).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    77.
    Agir, S. U., Kutbay, H. G. & Surmen, B. Plant diversity along coastal dunes of the Black Sea (North of Turkey). Rendiconti Lincei 27, 443–453 (2016).
    Article  Google Scholar 

    78.
    Andrej, P. & Andraž, Č. Functional response traits and plant community strategy indicate the stage of secondary succession. Hacquetia 11, 209–225 (2012).
    Article  Google Scholar 

    79.
    Hill, M.O. & Šmilauer, P. TWINSPAN for Windows version 2.3. (Centre for Ecology and Hydrology & University of South Bohemia, Huntingdon & Ceske Budejovice, 2005).

    80.
    Roleček, J., Tichý, L., Zelený, D. & Chytrý, M. Modified TWINSPAN classification in which the hierarchy respects cluster heterogeneity. J. Veg. Sci. 20, 596–602 (2009).
    Article  Google Scholar  More

  • in

    Extreme temperatures compromise male and female fertility in a large desert bird

    1.
    Angilletta, M. J. Thermal Adaptation: A Theoretical And Empirical Analysis (Oxford University Press, 2009).
    2.
    Chown, S. L., Sinclair, B. J., Leinaas, H. P. & Gaston, K. J. Hemispheric asymmetries in biodiversity—a serious matter for ecology. PLoS Biol. 2, e406 (2004).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    3.
    Sunday, J. M., Bates, A. E. & Dulvy, N. K. Thermal tolerance and the global redistribution of animals. Nat. Clim. Change 2, 686–690 (2012).
    ADS  Article  Google Scholar 

    4.
    Kellermann, V., van Heerwaarden, B., Sgrò, C. M. & Hoffmann, A. A. Fundamental evolutionary limits in ecological traits drive Drosophila species distributions. Science 325, 1244–1246 (2009).
    ADS  CAS  PubMed  Article  Google Scholar 

    5.
    Araújo, M. B. et al. Heat freezes niche evolution. Ecol. Lett. 16, 1206–1219 (2013).
    PubMed  Article  Google Scholar 

    6.
    García-Robledo, C., Kuprewicz, E. K., Staines, C. L., Erwin, T. L. & Kress, W. J. Limited tolerance by insects to high temperatures across tropical elevational gradients and the implications of global warming for extinction. Proc. Natl Acad. Sci. USA 113, 680–685 (2016).
    ADS  PubMed  Article  CAS  Google Scholar 

    7.
    Geerts, A. N. et al. Rapid evolution of thermal tolerance in the water flea, Daphnia. Nat. Clim. Change 5, 665–668 (2015).
    ADS  Article  Google Scholar 

    8.
    Iossa, G. Sex-specific differences in thermal fertility limits. Trends Ecol. Evol. 34, 490–492 (2019).
    PubMed  Article  Google Scholar 

    9.
    Walsh, B. S. et al. The impact of climate change on fertility. Trends Ecol. Evol. 34, 249–259 (2019).
    PubMed  Article  Google Scholar 

    10.
    Vasudeva, R. et al. Adaptive thermal plasticity enhances sperm and egg performance in a model insect. eLife 8, e49452 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    11.
    Hurley, L. L., McDiarmid, C. S., Friesen, C. R., Griffith, S. C. & Rowe, M. Experimental heatwaves negatively impact sperm quality in the zebra finch. Proc. R. Soc. B 285, 20172547 (2018).
    PubMed  Article  Google Scholar 

    12.
    Dahlke, F., Wohlrab, S., Butzin, M. & Pörtner, H. Thermal bottlenecks in the lifecycle define climate vulnerability of fish. Science 369, 65–70 (2020).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    13.
    Bathiany, S., Dakos, V., Scheffer, M. & Lenton, T. M. Climate models predict increasing temperature variability in poor countries. Sci. Adv. 4, 1–11 (2018).
    Article  Google Scholar 

    14.
    Vázquez, D. P., Gianoli, E., Morris, W. F. & Bozinovic, F. Ecological and evolutionary impacts of changing climatic variability. Biol. Rev. 92, 22–42 (2017).
    PubMed  Article  Google Scholar 

    15.
    Chevin, L.-M., Lande, R. & Mace, G. M. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol. 8, e1000357 (2010).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    16.
    Sgrò, C. M. & Hoffmann, A. A. Genetic correlations, tradeoffs and environmental variation. Heredity 93, 241–248 (2004).
    PubMed  Article  Google Scholar 

    17.
    Wood, C. W. & Brodie, E. D. Environmental effects on the structure of the G-matrix. Evolution 69, 2927–2940 (2015).
    PubMed  Article  Google Scholar 

    18.
    Brommer, J. E., Merila, J., Sheldon, B. C. & Gustavsson, L. Natural selection and genetic variation for reproductive reaction norms in a wild bird population. Evolution 59, 1362–1371 (2005).
    PubMed  Article  Google Scholar 

    19.
    Brommer, J. E., Rattiste, K. & Wilson, A. J. Exploring plasticity in the wild: laying date–temperature reaction norms in the common gull Larus canus. Proc. R. Soc. B 275, 687–693 (2008).
    PubMed  Article  Google Scholar 

    20.
    Nussey, D. H., Postma, E., Gienapp, P., Visser, M. E. & Gienapp, P. Selection on heritable phenotypic plasticity in a wild bird population. Science 310, 304–306 (2005).
    ADS  CAS  PubMed  Article  Google Scholar 

    21.
    Charmantier, A. et al. Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320, 800–803 (2008).
    ADS  CAS  PubMed  Article  Google Scholar 

    22.
    Matthysen, E., Adriaensen, F. & Dhondt, A. A. Multiple responses to increasing spring temperatures in the breeding cycle of blue and great tits (Cyanistes caeruleus, Parus major). Glob. Change Biol. 17, 1–16 (2011).
    ADS  Article  Google Scholar 

    23.
    Both, C. & Visser, M. E. Adjustment to climate change is constrained by arrival date in a long-distance migrant bird. Nature 411, 296–298 (2001).
    ADS  CAS  PubMed  Article  Google Scholar 

    24.
    Schiegg, K., Pasinelli, G., Walters, J. R. & Daniels, S. J. Inbreeding and experience affect response to climate change by endangered woodpeckers. Proc. R. Soc. B 269, 1153–1159 (2002).
    PubMed  Article  Google Scholar 

    25.
    Wilson, S., Norris, D. R., Wilson, A. G. & Arcese, P. Breeding experience and population density affect the ability of a songbird to respond to future climate variation. Proc. R. Soc. B 274, 2539–2545 (2007).
    PubMed  Article  Google Scholar 

    26.
    Dunn, P. O. & Winkler, D. W. Climate change has affected the breeding date of tree swallows throughout North America. Proc. R. Soc. B 266, 2487–2490 (1999).
    CAS  Article  Google Scholar 

    27.
    Hällfors, M. H. et al. Shifts in timing and duration of breeding for 73 boreal bird species over four decades. Proc. Natl Acad. Sci. USA 117, 18557–18565 (2020).
    PubMed  Article  CAS  Google Scholar 

    28.
    Gienapp, P., Postma, E. & Visser, M. E. Why breeding time has not responded to selection for earlier breeding in a songbird population. Evolution 60, 2381 (2006).
    PubMed  Article  Google Scholar 

    29.
    Jàrvinen, A. Global warming and egg size of birds. Ecography 17, 108–110 (1994).
    Article  Google Scholar 

    30.
    Kitaysky, A. S. & Golubova, E. G. Climate change causes contrasting trends in reproductive performance of planktivorous and piscivorous alcids. J. Anim. Ecol. 69, 248–262 (2000).
    Article  Google Scholar 

    31.
    Julliard, R., Clavel, J., Devictor, V., Jiguet, F. & Couvet, D. Spatial segregation of specialists and generalists in bird communities. Ecol. Lett. 9, 1237–1244 (2006).
    PubMed  Article  Google Scholar 

    32.
    Weatherhead, P. J. Effects of climate variation on timing of nesting, reproductive success, and offspring sex ratios of red-winged blackbirds. Oecologia 144, 168–175 (2005).
    ADS  PubMed  Article  Google Scholar 

    33.
    Auer, S. K. & Martin, T. E. Climate change has indirect effects on resource use and overlap among coexisting bird species with negative consequences for their reproductive success. Glob. Change Biol. 19, 411–419 (2013).
    ADS  Article  Google Scholar 

    34.
    Riddell, E. A., Iknayan, K. J., Wolf, B. O., Sinervo, B. & Beissinger, S. R. Cooling requirements fueled the collapse of a desert bird community from climate change. Proc. Natl Acad. Sci. USA116, 21609–21615 (2019).
    CAS  PubMed  Article  Google Scholar 

    35.
    Visser, M. E., Van Noordwijk, A. J., Tinbergen, J. M. & Lessells, C. M. Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc. R. Soc. B 265, 1867–1870 (1998).
    Article  Google Scholar 

    36.
    Both, C., Bouwhuis, S., Lessells, C. M. & Visser, M. E. Climate change and population declines in a long-distance migratory bird. Nature 441, 81–83 (2006).
    ADS  CAS  PubMed  Article  Google Scholar 

    37.
    Magige, F. J., Stokke, B. G., Sortland, R. & Røskaft, E. Breeding biology of ostriches (Struthio camelus) in the Serengeti ecosystem, Tanzania. Afr. J. Ecol. 47, 400–408 (2009).
    Article  Google Scholar 

    38.
    Bertram, B. C. R. The Ostrich Communal Nesting System (Princeton University Press, New Jersey, 1992).

    39.
    Kimwele, C. N. & Graves, J. A. A molecular genetic analysis of the communal nesting of the ostrich (Struthio camelus). Mol. Ecol. 12, 229–236 (2003).
    CAS  PubMed  Article  Google Scholar 

    40.
    Maloney, S. K. Thermoregulation in ratites: a review. Aust. J. Exp. Agric. 48, 1293–1301 (2008).
    Article  Google Scholar 

    41.
    Hassan, S. M., Siam, A. A., Mady, M. E. & Cartwright, A. L. Egg storage period and weight effects on hatchability of ostrich (Struthio camelus) eggs. Poult. Sci. 84, 1908–1912 (2005).
    CAS  PubMed  Article  Google Scholar 

    42.
    Gonzalez, A., Satterlee, D. G., Moharer, F. & Cadd, G. G. Factors affecting ostrich egg hatchability. Poult. Sci. 78, 1257–1262 (1999).
    CAS  PubMed  Article  Google Scholar 

    43.
    Roff, D. A. & Wilson, A. J. Quantifying genotype-by-environment interactions in laboratory systems. In Genotype‐by‐Environment Interactions and Sexual Selection (eds. Hunt, J. & Hosken, D.) 100–136 (John Wiley & Sons, Ltd, 2014).

    44.
    Christians, J. K. Avian egg size: variation within species and inflexibility within individuals. Biol. Rev. Camb. Philos. Soc. 77, 1–26 (2002).
    PubMed  Article  Google Scholar 

    45.
    Lack, D. The Natural Regulation of Animal Numbers (Clarendon Press, 1954).

    46.
    Perrins, C. M. The timing of birds‘ breeding seasons. Ibis 112, 242–255 (1970).
    Article  Google Scholar 

    47.
    Sales, K. et al. Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect. Nat. Commun. 9, 1–11 (2018).
    ADS  CAS  Article  Google Scholar 

    48.
    McAfee, A. et al. Vulnerability of honey bee queens to heat-induced loss of fertility. Nat. Sustain 3, 367–376 (2020).
    Article  Google Scholar 

    49.
    Pérez-Crespo, M., Pintado, B. & Gutiérrez-Adán, A. Scrotal heat stress effects on sperm viability, sperm DNA integrity, and the offspring sex ratio in mice. Mol. Reprod. Dev. 75, 40–47 (2008).
    PubMed  Article  CAS  Google Scholar 

    50.
    Hansen, P. J. Effects of heat stress on mammalian reproduction. Philos. Trans. R. Soc. B 364, 3341–3350 (2009).
    Article  Google Scholar 

    51.
    Moreno, R. D., Lagos-Cabre, R., Bunay, J., Urzua, N. & Bustamante-Marin, X. Molecular basis of heat stress damage in mammalian testis. In Testis: Anatomy, Physiology and Pathology (eds. Nemoto, Y. & Inaba, N.) 127–155 (Nova Science, 2012).

    52.
    Karaca, A. G., Parker, H. M., Yeatman, J. B. & McDaniel, C. D. The effects of heat stress and sperm quality classification on broiler breeder male fertility and semen ion concentrations. Br. Poult. Sci. 43, 621–628 (2002).
    CAS  PubMed  Article  Google Scholar 

    53.
    Mita, P., Hinton, B. T. & Dufour, J. M. The blood–testis and blood–epididymis barriers are more than just their tight junctions. Biol. Reprod. 84, 851–858 (2011).
    Article  CAS  Google Scholar 

    54.
    Smith, C. C. & Fretwell, S. D. The optimal balance between size and number of offspring. Am. Nat. 108, 499–506 (1974).
    Article  Google Scholar 

    55.
    Ojanen, M. Composition of the eggs of the great tit (Parus major) and pied flycatcher (Ficedula hypoleuca). Ann. Zool. Fenn. 20, 57–63 (1983).
    Google Scholar 

    56.
    Krist, M. Egg size and offspring quality: a meta-analysis in birds. Biol. Rev. 86, 692–716 (2011).
    PubMed  Article  Google Scholar 

    57.
    Falconer, D. S. & Mackay, T. F. C. Introduction to Quantitative Genetics (Pearson, 1996).

    58.
    Lynch, M. & Gabriel, W. Environmental tolerance. Am. Nat. 129, 283–303 (1987).
    Article  Google Scholar 

    59.
    Gilchrist, G. W. Specialists and generalists in changing environments. I. Fitness landscapes of thermal sensitivity. Am. Nat. 146, 252–270 (1995).
    Article  Google Scholar 

    60.
    Whitlock, M. C. The red queen beats the jack-of-all-trades: the limitations on the evolution of phenotypic plasticity and niche breadth. Am. Nat. 148, S65 (1996).
    Article  Google Scholar 

    61.
    Pen, I. & Weissing, F. J. Towards a unified theory of cooperative breeding: the role of ecology and life history re-examined. Proc. R. Soc. B 267, 2411–2418 (2000).
    Article  Google Scholar 

    62.
    Emlen, S. T. The evolution of helping. I. An ecological constraints model. Am. Nat. 119, 29–39 (1982).
    Article  Google Scholar 

    63.
    Rubenstein, D. R. Spatiotemporal environmental variation, risk aversion, and the evolution of cooperative breeding as a bet-hedging strategy. Proc. Natl Acad. Sci. USA 108, 10816–10822 (2011).
    ADS  CAS  PubMed  Article  Google Scholar 

    64.
    Cornwallis, C. K. et al. Cooperation facilitates the colonization of harsh environments. Nat. Ecol. Evol. 1, 0057 (2017).
    Article  Google Scholar 

    65.
    Rubenstein, D. R. & Lovette, I. J. Temporal environmental variability drives the evolution of cooperative breeding in birds. Curr. Biol. 17, 1414–1419 (2007).
    CAS  PubMed  Article  Google Scholar 

    66.
    Albright, T. P. et al. Mapping evaporative water loss in desert passerines reveals an expanding threat of lethal dehydration. Proc. Natl Acad. Sci. USA 114, 201613625 (2017).
    Google Scholar 

    67.
    Vincze, O. et al. Parental cooperation in a changing climate: fluctuating environments predict shifts in care division. Glob. Ecol. Biogeogr. 26, 347–358 (2017).
    Article  Google Scholar 

    68.
    Nord, A. & Nilsson, J. Å. Heat dissipation rate constrains reproductive investment in a wild bird. Funct. Ecol. 33, 250–259 (2019).
    Article  Google Scholar 

    69.
    Cloete, S. W. P. et al. Variance components for live weight, body measurements and reproductive traits of pair-mated ostrich females. Br. Poult. Sci. 47, 147–158 (2006).
    CAS  PubMed  Article  Google Scholar 

    70.
    Rybnik, P. K., Horbanczuk, J. O., Naranowicz, H., Lukaszewicz, E. & Malecki, I. A. Semen collection in the ostrich (Struthio camelus) using a dummy or a teaser female. Br. Poult. Sci. 48, 635–643 (2007).
    CAS  PubMed  Article  Google Scholar 

    71.
    Brand, T. S., Olivier, T. R. & Gous, R. M. The response in food intake and reproductive parameters of breeding ostriches to increasing dietary energy. South Afr. J. Anim. Sci. 40, 434–437 (2010).
    Google Scholar 

    72.
    Brand, T. S., Olivier, T. R. & Gous, R. M. The reproductive response of female ostriches to dietary protein. Br. Poult. Sci. 56, 232–238 (2015).
    CAS  PubMed  Article  Google Scholar 

    73.
    Martin, P. A., Reimers, T. J., Lodge, J. R. & Dziuk, P. J. The effect of ratios and numbers of spermatozoa mixed from two males on proportions of offspring. J. Reprod. Fertil. 39, 251–258 (1974).
    CAS  PubMed  Article  Google Scholar 

    74.
    Birkhead, T. R. & Møller, A. P. Sperm Competition and Sexual Selection (Academic Press, 1998).

    75.
    Birkhead, T. R. & Biggins, J. D. Sperm competition mechanisms in birds: models and data. Behav. Ecol. 9, 253–260 (1998).
    Article  Google Scholar 

    76.
    Soley, J. T. & Roberts, J. C. Ultrastructure of ostrich (Struthio camelus) spermatozoa. II. Scanning electron microscopy. Onderstepoort J. Vet. Res. 61, 239–246 (1994).
    CAS  PubMed  Google Scholar 

    77.
    Lake, P. E. & Stewart, J. M. Artificial Insemination in Poultry. Ministry of Agriculture Fisheries and Food, Bulletin 213 (Her Majesty’s Stationery Office, 1978).

    78.
    Bonato, M., Malecki, I. A., Rybnik-Trzaskowska, P. K., Cornwallis, C. K. & Cloete, S. W. P. Predicting ejaculate quality and libido in male ostriches: effect of season and age. Anim. Reprod. Sci. 151, 49–55 (2014).
    PubMed  Article  Google Scholar 

    79.
    Bonato, M., Rybnik, P. K., Malecki, I. A., Cornwallis, C. K. & Cloete, S. W. P. Twice daily collection yields greater semen output and does not affect male libido in the ostrich. Anim. Reprod. Sci. 123, 258–264 (2011).
    PubMed  Article  Google Scholar 

    80.
    Muvhali, P. T. et al. Ostrich ejaculate characteristics and male libido around equinox and solstice dates. Trop. Anim. Health and Prod. 52, 2609–2619 (2020).
    CAS  Article  Google Scholar 

    81.
    Brand, Z., Cloete, S. W. P., Brown, C. R. & Malecki, I. A. Systematic factors that affect ostrich egg incubation traits. South Afr. J. Anim. Sci. 38, 315–325 (2008).
    Google Scholar 

    82.
    Bronneberg, R. G. G. et al. The relation between ultrasonographic observations in the oviduct and plasma progesterone, luteinizing hormone and estradiol during the egg laying cycle in ostriches. Domest. Anim. Endocrinol. 32, 15–28 (2007).
    CAS  PubMed  Article  Google Scholar 

    83.
    Van Schalkwyk, S. J., Cloete, S. W. P. & De Kock, J. A. Repeatability and phenotypic correlations for body weight and reproduction in commercial ostrich breeding pairs. Br. Poult. Sci. 37, 953–962 (1996).
    PubMed  Article  Google Scholar 

    84.
    Jones, R. C. & Lin, M. Spermatogenesis in birds. In Oxford Reviews of Reproductive Biology, Vol. 15 (ed. Milligan, S. R.) (Oxford University Press, 1993).

    85.
    R Core Team. R: A Language and Environment for Statistical Computing (R Core Team, 2020).

    86.
    Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).
    Article  Google Scholar 

    87.
    Araya-Ajoy, Y. G. & Dingemanse, N. J. Repeatability, heritability, and age-dependence of seasonal plasticity in aggressiveness in a wild passerine bird. J. Anim. Ecol. 86, 227–238 (2017).
    PubMed  Article  Google Scholar 

    88.
    Araya-Ajoy, Y. G., Mathot, K. J. & Dingemanse, N. J. An approach to estimate short-term, long-term and reaction norm repeatability. Methods Ecol. Evol. 6, 1462–1473 (2015).
    Article  Google Scholar 

    89.
    Scheiner, S. M. Genetics and evolution of phenotypic plasticity. Annu. Rev. Ecol. Syst. 24, 35–68 (1993).
    Article  Google Scholar 

    90.
    Wilson, A. J. Why h2 does not always equal VA/VP. J. Evol. Biol. 21, 647–650 (2008).
    CAS  PubMed  Article  Google Scholar 

    91.
    de Villemereuil, P., Morrissey, M. B., Nakagawa, S. & Schielzeth, H. Fixed-effect variance and the estimation of repeatabilities and heritabilities: Issues and solutions. J. Evol. Biol. 31, 621–632 (2018).
    PubMed  Article  Google Scholar 

    92.
    de Villemereuil, P., Schielzeth, H., Nakagawa, S. & Morrissey, M. General methods for evolutionary quantitative genetic inference from generalized mixed models. Genetics 204, 1281–1294 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    93.
    BirdLife International. BirdLife International and Handbook of the Birds of the World. Bird Species Distribution Maps of the World (BirdLife International, 2019).

    94.
    Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).
    Article  Google Scholar  More

  • in

    Genomic evidence of prevalent hybridization throughout the evolutionary history of the fig-wasp pollination mutualism

    1.
    Taylor, S. A. & Larson, E. L. Insights from genomes into the evolutionary importance and prevalence of hybridization in nature. Nat. Ecol. Evol. 3, 170–177 (2019).
    PubMed  Article  PubMed Central  Google Scholar 
    2.
    Payseur, B. A. & Rieseberg, L. H. A genomic perspective on hybridization and speciation. Mol. Ecol. 25, 2337–2360 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    3.
    Arnold, M. L. & Kunte, K. Adaptive genetic exchange: a tangled history of admixture and evolutionary innovation. Trends Ecol. Evol. 32, 601–611 (2017).
    PubMed  Article  Google Scholar 

    4.
    Mallet, J. Hybrid speciation. Nature 446, 279–283 (2007).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    5.
    Abbott, R. et al. Hybridization and speciation. J. Evol. Biol. 26, 229–246 (2013).
    CAS  PubMed  Article  Google Scholar 

    6.
    Gross, B. L. & Rieseberg, L. H. The ecological genetics of homoploid hybrid speciation. J. Hered. 96, 241–252 (2005).
    CAS  PubMed  Article  Google Scholar 

    7.
    Schumer, M., Rosenthal, G. G. & Andolfatto, P. How common is homoploid hybrid speciation? Evolution 68, 1553–1560 (2014).
    PubMed  Article  Google Scholar 

    8.
    Grant, V. Pollination systems as isolating mechanisms in angiosperms. Evolution 3, 82–97 (1949).
    CAS  PubMed  Article  Google Scholar 

    9.
    Kay, K. M. & Sargent, R. D. The role of animal pollination in plant speciation: Integrating ecology, geography, and genetics. Annu. Rev. Ecol. Evol. Syst. 40, 637–656 (2009).
    Article  Google Scholar 

    10.
    Serrano-Serrano, M. L., Rolland, J., Clark, J. L., Salamin, N. & Perret, M. Hummingbird pollination and the diversification of angiosperms: an old and successful association in Gesneriaceae. Proc. R. Soc. B Biol. Sci. 284, https://doi.org/10.1098/rspb.2016.2816 (2017).

    11.
    Thompson, J. N. Specific hypotheses on the geographic mosaic of coevolution. Am. Nat. 153, S1–S14 (1999).
    Article  Google Scholar 

    12.
    Van der Niet, T., Peakall, R. & Johnson, S. D. Pollinator-driven ecological speciation in plants: new evidence and future perspectives. Ann. Bot. 113, 199–211 (2014).
    PubMed  PubMed Central  Article  Google Scholar 

    13.
    Armbruster, W. S. The specialization continuum in pollination systems: diversity of concepts and implications for ecology, evolution and conservation. Funct. Ecol. 31, 88–100 (2017).
    Article  Google Scholar 

    14.
    Ayasse, M., Stokl, J. & Francke, W. Chemical ecology and pollinator-driven speciation in sexually deceptive orchids. Phytochemistry 72, 1667–1677 (2011).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    15.
    Machado, C. A., Robbins, N., Gilbert, M. T. P. & Herre, E. A. Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualism. Proc. Natl Acad. Sci. USA 102, 6558–6565 (2005).
    ADS  CAS  PubMed  Article  Google Scholar 

    16.
    Kawakita, A. Evolution of obligate pollination mutualism in the tribe Phyllantheae (Phyllanthaceae). Plant Species Biol. 25, 3–19 (2010).
    Article  Google Scholar 

    17.
    Ramirez, W. Host specificity of fig wasps (Agaonidae). Evolution 24, 680–691 (1970).
    Article  Google Scholar 

    18.
    Schiestl, F. P. & Schluter, P. M. Floral isolation, specialized pollination, and pollinator behavior in orchids. Annu. Rev. Entomol. 54, 425–446 (2009).
    CAS  PubMed  Article  Google Scholar 

    19.
    Ramirez, S. R. et al. Asynchronous diversification in a specialized plant-pollinator mutualism. Science 333, 1742–1746 (2011).
    ADS  CAS  PubMed  Article  Google Scholar 

    20.
    Cruaud, A. et al. An extreme case of plant-insect co-diversification: figs and fig-pollinating wasps. Syst. Biol. 61, 1029–1047 (2012).
    PubMed  PubMed Central  Article  Google Scholar 

    21.
    Berg, C. C. & Corner, E. J. H. in Flora Malesiana Series I -Seed Plants Vol. 17 (ed. Nooteboom, H. P.) 1–702 (Nationaal Herbarium, Nederland, 2005).

    22.
    Wang, G., Cannon, C. H. & Chen, J. Pollinator sharing and gene flow among closely related sympatric dioecious fig taxa. Proc. R. Soc. B Biol. Sci. 283, https://doi.org/10.1098/rspb.2015.2963 (2016).

    23.
    Machado, C. A., Jousselin, E., Kjellberg, F., Compton, S. G. & Herre, E. A. Phylogenetic relationships, historical biogeography and character evolution of fig-pollinating wasps. Proc. R. Soc. B Biol. Sci. 268, 685–694 (2001).
    CAS  Article  Google Scholar 

    24.
    Harrison, R. D. Figs and the diversity of tropical rainforests. Bioscience 55, 1053–1064 (2005).
    Article  Google Scholar 

    25.
    Grison-Pigé, L., Bessière, J. M. & Hossaert-McKey, M. Specific attraction of fig-pollinating wasps: Role of volatile compounds released by tropical figs. J. Chem. Ecol. 28, 283–295 (2002).
    PubMed  Article  PubMed Central  Google Scholar 

    26.
    Herre, E. A. et al. Molecular phylogenies of figs and their pollinator wasps. J. Biogeogr. 23, 521–530 (1996).
    Article  Google Scholar 

    27.
    Molbo, D., Machado, C. A., Sevenster, J. G., Keller, L. & Herre, E. A. Cryptic species of fig-pollinating wasps: Implications for the evolution of the fig-wasp mutualism, sex allocation, and precision of adaptation. Proc. Natl Acad. Sci. USA 100, 5867–5872 (2003).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    28.
    Rasplus, J. Y. in The Biodiversity of African Plants (eds van der Maesen, L. J. G. et al.) 639–649 (Springer, 1996).

    29.
    Yang, L.-Y. et al. The incidence and pattern of co-pollinator diversification in dioecious and monoecious figs. Evolution 69, 294–304 (2015).
    PubMed  PubMed Central  Article  Google Scholar 

    30.
    Cornille, A. et al. Floral volatiles, pollinator sharing and diversification in the fig-wasp mutualism: insights from Ficus natalensis, and its two wasp pollinators (South Africa). Proc. R. Soc. B Biol. Sci. 279, 1731–1739 (2012).
    CAS  Article  Google Scholar 

    31.
    Compton, S. G. A collapse of host specificity in some African fig wasps. S. Afr. J. Sci. 86, 39–40 (1990).
    Google Scholar 

    32.
    Renoult, J. P., Kjellberg, F., Grout, C., Santoni, S. & Khadari, B. Cyto-nuclear discordance in the phylogeny of Ficus section Galoglychia and host shifts in plant-pollinator associations. BMC Evol. Biol. 9, 248 (2009).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    33.
    Satler, J. D. et al. Inferring processes of coevolutionary diversification in a community of Panamanian strangler figs and associated pollinating wasps. Evolution 73, 2295–2311 (2019).

    34.
    Jackson, A. P., Machado, C. A., Robbins, N. & Herre, E. A. Multi-locus phylogenetic analysis of neotropical figs does not support co-speciation with the pollinators: the importance of systematic scale in fig/wasp cophylogenetic studies. Symbiosis 45, 57–72 (2008).
    CAS  Google Scholar 

    35.
    Parrish, T. L., Koelewijn, H. P., van Dijk, P. J. & Kruijt, M. Genetic evidence for natural hybridization between species of dioecious Ficus on island populations. Biotropica 35, 333–343 (2003).
    Article  Google Scholar 

    36.
    Ramirez, W. Hybridization of Ficus religiosa with F. septica and F. aurea (Moraceae). Rev. Biol. Trop. 42, 339–342 (1994).
    Google Scholar 

    37.
    Wei, Z. D., Kobmoo, N., Cruaud, A. & Kjellberg, F. Genetic structure and hybridization in the species group of Ficus auriculata: can closely related sympatric Ficus species retain their genetic identity while sharing pollinators? Mol. Ecol. 23, 3538–3550 (2014).
    PubMed  Article  PubMed Central  Google Scholar 

    38.
    Bruun-Lund, S., Clement, W. L., Kjellberg, F. & Rønsted, N. First plastid phylogenomic study reveals potential cyto-nuclear discordance in the evolutionary history of Ficus L. (Moraceae). Mol. Phylogenet. Evol. 109, 93–104 (2017).
    PubMed  Article  Google Scholar 

    39.
    Zhang, X. et al. Genomes of the Banyan tree and pollinator wasp provide insights into fig-wasp coevolution. Cell 183, 875–889 (2020).
    CAS  PubMed  Article  Google Scholar 

    40.
    Mirarab, S. & Warnow, T. ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31, 44–52 (2015).
    Article  CAS  Google Scholar 

    41.
    Rønsted, N., Weiblen, G. D., Clement, W. L., Zerega, N. J. C. & Savolainen, V. Reconstructing the phylogeny of figs (Ficus, Moraceae) to reveal the history of the fig pollination mutualism. Symbiosis 45, 45–55 (2008).
    Google Scholar 

    42.
    Ane, C., Larget, B., Baum, D. A., Smith, S. D. & Rokas, A. Bayesian estimation of concordance among gene trees. Mol. Biol. Evol. 24, 412–426 (2007).
    CAS  PubMed  Article  Google Scholar 

    43.
    Larget, B. R., Kotha, S. K., Dewey, C. N. & Ane, C. BUCKy: Gene tree/species tree reconciliation with Bayesian concordance analysis. Bioinformatics 26, 2910–2911 (2010).
    CAS  PubMed  Article  Google Scholar 

    44.
    Baum, D. A. Concordance trees, concordance factors, and the exploration of reticulate genealogy. Taxon 56, 417–426 (2007).
    Article  Google Scholar 

    45.
    Solis-Lemus, C., Bastide, P. & Ane, C. PhyloNetworks: a package for phylogenetic networks. Mol. Biol. Evol. 34, 3292–3298 (2017).
    CAS  PubMed  Article  Google Scholar 

    46.
    Soraggi, S., Wiuf, C. & Albrechtsen, A. Powerful inference with the D-statistic on low-coverage whole-genome data. G3 (Bethesda) 8, 551–566 (2018).

    47.
    Durand, E. Y., Patterson, N., Reich, D. & Slatkin, M. Testing for ancient admixture between closely related populations. Mol. Biol. Evol. 28, 2239–2252 (2011).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    48.
    Degnan, J. H. & Rosenberg, N. A. Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol. Evol. 24, 332–340 (2009).
    PubMed  Article  Google Scholar 

    49.
    Conow, C., Fielder, D., Ovadia, Y. & Libeskind-Hadas, R. Jane: a new tool for the cophylogeny reconstruction problem. Algorithms Mol. Biol. 5, https://doi.org/10.1186/1748-7188-5-16 (2010).

    50.
    Ramsey, A. J. & Mandel, J. R. When one genome is not enough: organellar heteroplasmy in plants. Annual Plant Reviews 2, 619–658 (2019).
    Article  Google Scholar 

    51.
    Zhang, Q. & Liu, Y. & Sodmergen. Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cytoplasmic inheritance in 295 angiosperm species. Plant Cell Physiol. 44, 941–951 (2003).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    52.
    Hu, Y. C., Zhang, Q. & Rao, G. Y. & Sodmergen. Occurrence of plastids in the sperm cells of Caprifoliaceae: Biparental plastid inheritance in angiosperms is unilaterally derived from maternal inheritance. Plant Cell Physiol. 49, 958–968 (2008).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    53.
    Mayr, E. Animal Species and Evolution 1–811 (Belknap Press, 1963).

    54.
    Wu, C. I. The genic view of the process of speciation. J. Evol. Biol. 14, 851–865 (2001).
    Article  Google Scholar 

    55.
    Sun, M. et al. Deep phylogenetic incongruence in the angiosperm clade Rosidae. Mol. Phylogenet. Evol. 83, 156–166 (2015).
    PubMed  Article  PubMed Central  Google Scholar 

    56.
    Folk, R. A., Soltis, P. S., Soltis, D. E. & Guralnick, R. New prospects in the detection and comparative analysis of hybridization in the tree of life. Am. J. Bot. 105, 364–375 (2018).
    PubMed  Article  PubMed Central  Google Scholar 

    57.
    Jiao, X., Flouri, T., Rannala, B. & Yang, Z. The impact of cross-species gene flow on species tree estimation. Syst. Biol. 69, 830–847 (2020).

    58.
    Jousselin, E. et al. One fig to bind them all: host conservatism in a fig wasp community unraveled by cospeciation analyses among pollinating and nonpollinating fig wasps. Evolution 62, 1777–1797 (2008).
    PubMed  Article  PubMed Central  Google Scholar 

    59.
    Moe, A. M. & Weiblen, G. D. Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae). Evolution 66, 3710–3721 (2012).
    PubMed  Article  PubMed Central  Google Scholar 

    60.
    Wang, G., Compton, S. G. & Chen, J. The mechanism of pollinator specificity between two sympatric fig varieties: a combination of olfactory signals and contact cues. Ann. Bot. 111, 173–181 (2013).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    61.
    Bronstein, J. L. Maintenance of species-specificity in a neotropical fig – pollinator wasp mutualism. Oikos 48, 39–46 (1987).
    Article  Google Scholar 

    62.
    Ware, A., Kaye, P., Compton, S. & Noort, S. Fig volatiles: their role in attracting pollinators and maintaining pollinator specificity. Plant Syst. Evol. 186, 147–156 (1993).
    Article  Google Scholar 

    63.
    Soler, C. C. L., Proffit, M., Bessière, J. M., Hossaert-McKey, M. & Schatz, B. Evidence for intersexual chemical mimicry in a dioecious plant. Ecol. Lett. 15, 978–985 (2012).
    PubMed  Article  PubMed Central  Google Scholar 

    64.
    Hossaert-McKey, M., Soler, C., Schatz, B. & Proffit, M. Floral scents: their roles in nursery pollination mutualisms. Chemoecology 20, 75–88 (2010).
    Article  Google Scholar 

    65.
    Knudsen, J. T., Eriksson, R., Gershenzon, J. & Stahl, B. Diversity and distribution of floral scent. Bot. Rev. 72, 1–120 (2006).
    Article  Google Scholar 

    66.
    Herre, E. A., Jander, K. C. & Machado, C. A. Evolutionary ecology of figs and their associates: Recent progress and outstanding puzzles. Annu. Rev. Ecol. Evol. Syst. 39, 439–458 (2008).
    Article  Google Scholar 

    67.
    Kiester, A. R., Lande, R. & Schemske, D. W. Models of coevolution and speciation in plants and their pollinators. Am. Nat. 124, 220–243 (1984).
    Article  Google Scholar 

    68.
    Vereecken, N. J., Cozzolino, S. & Schiestl, F. P. Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids. BMC Evol. Biol. 10, 103 (2010).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    69.
    Rønsted, N. et al. 60 million years of co-divergence in the fig-wasp symbiosis. Proc. R. Soc. B Biol. Sci. 272, 0962–8452 (2005). 2593-2599.
    Google Scholar 

    70.
    Wiebes, J. T. Co-evolution of figs and their insect pollinators. Annu. Rev. Ecol. Syst. 10, 1–12 (1979).
    Article  Google Scholar 

    71.
    Zhu, H. et al. Native Seed Plants in Xishuangbanna of Yunnan (eds Zhu, H. & Yan, L.) 1–565 (Science Press, 2012).

    72.
    Yang, J. B., Li, D. Z. & Li, H. T. Highly effective sequencing whole chloroplast genomes of angiosperms by nine novel universal primer pairs. Mol. Ecol. Resour. 14, 1024–1031 (2014).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    73.
    Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    74.
    Andrews, S. FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (2010).

    75.
    Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589–595 (2010).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    76.
    Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    77.
    McKenna, A. et al. The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    78.
    Jin, J.-J. et al. GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol. 21, 31 (2020).
    Article  Google Scholar 

    79.
    Wick, R. R., Schultz, M. B., Zobel, J. & Holt, K. E. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 31, 3350–3352 (2015).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    80.
    Weiß, C. L., Pais, M., Cano, L. M., Kamoun, S. & Burbano, H. A. nQuire: a statistical framework for ploidy estimation using next generation sequencing. BMC Bioinformatics 19, 122 (2018).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    81.
    Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    82.
    Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).
    PubMed  PubMed Central  Article  Google Scholar 

    83.
    Yang, Z. H. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).
    CAS  PubMed  Article  Google Scholar 

    84.
    Zhu, T. Q., Dos Reis, M. & Yang, Z. H. Characterization of the uncertainty of divergence time estimation under relaxed molecular clock models using multiple loci. Syst. Biol. 64, 267–280 (2015).
    CAS  PubMed  Article  Google Scholar 

    85.
    Gardner, E. M., Sarraf, P., Williams, E. W. & Zerega, N. J. C. Phylogeny and biogeography of Maclura (Moraceae) and the origin of an anachronistic fruit. Mol. Phylogenet. Evol. 117, 49–59 (2017).
    PubMed  Article  Google Scholar 

    86.
    dos Reis, M. & Yang, Z. Approximate likelihood calculation on a phylogeny for bayesian estimation of divergence times. Mol. Biol. Evol. 28, 2161–2172 (2011).
    PubMed  Article  CAS  Google Scholar 

    87.
    Yang, Z. & Rannala, B. Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds. Mol. Biol. Evol. 23, 212–226 (2006).
    CAS  PubMed  Article  Google Scholar 

    88.
    Matzke, N. J. Model selection in historical biogeography reveals that founder-event speciation is a crucial process in Island Clades. Syst. Biol. 63, 951–970 (2014).
    PubMed  Article  Google Scholar 

    89.
    Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    90.
    Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772–772 (2012).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    91.
    Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).

    92.
    Korneliussen, T. S., Albrechtsen, A. & Nielsen, R. ANGSD: analysis of next generation sequencing data. BMC Bioinformatics 15, 1–13 (2014).
    Article  Google Scholar 

    93.
    Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    94.
    Wang, G. et al. Data from: Genomic evidence of prevalent hybridization throughout the evolutionary history of the fig-wasp pollination mutualism. Dryad, Dataset https://doi.org/10.5061/dryad.zcrjdfn7m (2020).

    95.
    Zhang, T. & Zhang, S. C. Code from: Genomic evidence of prevalent hybridization throughout the evolutionary history of the fig-wasp pollination mutualism. Github https://doi.org/10.5281/zenodo.4308886 (2020). More

  • in

    Implications of monsoon season and UVB radiation for COVID-19 in India

    1.
    Dong, E., Du, H. & Gardner, L. An interactive web-based dashboard to track COVID-19 in real time. Lancet Infect. Dis. 20, 533–534 (2020).
    CAS  PubMed  PubMed Central  Article  Google Scholar 
    2.
    Chadha, M. S. et al. Dynamics of influenza seasonality at sub-regional levels in India and implications for vaccination timing. PLoS ONE 10, e0124122 (2015).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    3.
    Dash, N., Rose, W. & Nallasamy, K. India’s lockdown exit: Are we prepared to lock horns with COVID-19 and dengue in the rainy season?. Pediatr. Res. https://doi.org/10.1038/s41390-020-1063-7 (2020).
    Article  PubMed  PubMed Central  Google Scholar 

    4.
    Moozhipurath, R. K. & Kulkarni, P. Monsoon, Vitamin-D, COVID-19: Implications for India. Postgraduate Medical Journal Blog (accessed 20 November 2020). https://blogs.bmj.com/pmj/2020/07/08/monsoon-vitamin-d-covid-19-implications-for-india/ (2020).

    5.
    D’Avolio, A. et al. 25-Hydroxyvitamin D concentrations are lower in patients with positive PCR for SARS-CoV-2. Nutrients 12, 1359 (2020).
    PubMed Central  Article  CAS  Google Scholar 

    6.
    Meltzer, D. O. et al. Association of vitamin D status and other clinical characteristics with COVID-19 test results. JAMA Netw. Open 3, e2019722 (2020).
    PubMed  PubMed Central  Article  Google Scholar 

    7.
    Merzon, E. et al. Low plasma 25 (OH) vitamin D level is associated with increased risk of COVID-19 infection: An Israeli population-based study. FEBS J. 287, 3693–3702 (2020).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    8.
    Kaufman, H. W., Niles, J. K., Kroll, M. H., Bi, C. & Holick, M. F. SARS-CoV-2 positivity rates associated with circulating 25-hydroxyvitamin D levels. PLoS ONE 15, e0239252 (2020).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    9.
    Honardoost, M., Ghavideldarestani, M. & Khamseh, M. E. Role of vitamin D in pathogenesis and severity of COVID-19 infection. Arch. Physiol. Biochem. https://doi.org/10.1080/13813455.2020.1792505 (2020).
    Article  PubMed  PubMed Central  Google Scholar 

    10.
    Ilie, P. C., Stefanescu, S. & Smith, L. The role of vitamin D in the prevention of coronavirus disease 2019 infection and mortality. Aging Clin. Exp. Res. 32, 1195–1198 (2020).
    PubMed  Article  PubMed Central  Google Scholar 

    11.
    Maghbooli, Z. et al. Vitamin D sufficiency, a serum 25-hydroxyvitamin D at least 30 ng/mL reduced risk for adverse clinical outcomes in patients with COVID-19 infection. PLoS ONE 15, e0239799 (2020).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    12.
    Castillo, M. E. et al. Effect of calcifediol treatment and best available therapy versus best available therapy on intensive care unit admission and mortality among patients hospitalized for COVID-19: A pilot randomized clinical study. J. Steroid Biochem. Mol. Biol. 203, 105751 (2020).
    Article  CAS  Google Scholar 

    13.
    Benskin, L. L. A basic review of the preliminary evidence that COVID-19 risk and severity is increased in vitamin D deficiency. Front. Public Health 8, 513 (2020).
    PubMed  PubMed Central  Article  Google Scholar 

    14.
    Moozhipurath, R. K., Kraft, L. & Skiera, B. Evidence of protective role of ultraviolet-B (UVB) radiation in reducing COVID-19 deaths. Sci. Rep. 10, 17705 (2020).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    15.
    Engelsen, O., Brustad, M., Aksnes, L. & Lund, E. Daily duration of vitamin D synthesis in human skin with relation to latitude, total ozone, altitude, ground cover, aerosols and cloud thickness. Photochem. Photobiol. 81, 1287–1290 (2005).
    CAS  PubMed  Article  Google Scholar 

    16.
    Li, Y. et al. Global patterns in monthly activity of influenza virus, respiratory syncytial virus, parainfluenza virus, and metapneumovirus: A systematic analysis. Lancet Glob. Health 7, e1031–e1045 (2019).
    PubMed  Article  Google Scholar 

    17.
    Li, Y., Wang, X. & Nair, H. Global seasonality of human seasonal coronaviruses: A clue for postpandemic circulating season of severe acute respiratory syndrome coronavirus 2?. J. Infect. Dis. 222, 1090–1097 (2020).
    CAS  PubMed  Article  Google Scholar 

    18.
    Gupta, E., Dar, L., Kapoor, G. & Broor, S. The changing epidemiology of dengue in Delhi, India. Virol. J. 3, 1–5 (2006).
    Article  Google Scholar 

    19.
    Laneri, K. et al. Forcing versus feedback: Epidemic malaria and monsoon rains in Northwest India. PLoS Comput. Biol. 6, e1000898 (2010).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    20.
    Shaman, J., Jeon, C. Y., Giovannucci, E. & Lipsitch, M. Shortcomings of vitamin D-based model simulations of seasonal influenza. PLoS ONE 6, e20743 (2011).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    21.
    Ianevski, A. et al. Low temperature and low UV indexes correlated with peaks of influenza virus activity in Northern Europe during 2010–2018. Viruses 11, 207 (2019).
    CAS  PubMed Central  Article  Google Scholar 

    22.
    Yang, W. et al. Dynamics of influenza in tropical Africa: Temperature, humidity, and co-circulating (sub)types. Influenza Other Respir. Viruses 12, 446–456 (2018).
    PubMed  PubMed Central  Article  Google Scholar 

    23.
    Sajadi, M. M. et al. Temperature, humidity, and latitude analysis to estimate potential spread and seasonality of coronavirus disease 2019 (COVID-19). JAMA Netw. Open 3, e2011834 (2020).
    PubMed  PubMed Central  Article  Google Scholar 

    24.
    Dhara, V. R., Schramm, P. J. & Luber, G. Climate change & infectious diseases in India: Implications for health care providers. Indian J. Med. Res. 138, 847–852 (2013).
    PubMed  PubMed Central  Google Scholar 

    25.
    Nimitphong, H., Chanprasertyothin, S., Jongjaroenprasert, W. & Ongphiphadhanakul, B. The association between vitamin D status and circulating adiponectin independent of adiposity in subjects with abnormal glucose tolerance. Endocrine 36, 205–210 (2009).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    26.
    Sagripanti, J.-L. & Lytle, C. D. Inactivation of influenza virus by solar radiation. Photochem. Photobiol. 83, 1278–1282 (2007).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    27.
    Hart, P. H., Gorman, S. & Finlay-Jones, J. J. Modulation of the immune system by UV radiation: More than just the effects of vitamin D?. Nat. Rev. Immunol. 11, 584–596 (2011).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    28.
    Bodiwala, D. et al. Prostate cancer risk and exposure to ultraviolet radiation: Further support for the protective effect of sunlight. Cancer Lett. 192, 145–149 (2003).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    29.
    Grant, W. B. An estimate of premature cancer mortality in the US due to inadequate doses of solar ultraviolet-B radiation. Cancer 94, 1867–1875 (2002).
    PubMed  Article  PubMed Central  Google Scholar 

    30.
    Grant, W. B. An ecologic study of the role of solar UV-B radiation in reducing the risk of cancer using cancer mortality data, dietary supply data, and latitude for European countries. In Biologic Effects of Light 2001 (ed. Holick, M. F.) 267–276 (Springer, Berlin, 2002).
    Google Scholar 

    31.
    Rostand, S. G. Ultraviolet light may contribute to geographic and racial blood pressure differences. Hypertension 30, 150–156 (1997).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    32.
    Holick, M. F. Vitamin D deficiency. N. Engl. J. Med. 357, 266–281 (2007).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    33.
    Ritu, G. & Gupta, A. Vitamin D deficiency in India: Prevalence, causalities and interventions. Nutrients 6, 729–775 (2014).
    MathSciNet  Article  CAS  Google Scholar 

    34.
    Zittermann, A. Vitamin D in preventive medicine: Are we ignoring the evidence?. Br. J. Nutr. 89, 552–572 (2003).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    35.
    Tangpricha, V., Pearce, E. N., Chen, T. C. & Holick, M. F. Vitamin D insufficiency among free-living healthy young adults. Am. J. Med. 112, 659–662 (2002).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    36.
    Crowe, F. L. et al. Plasma concentrations of 25-hydroxyvitamin D in meat eaters, fish eaters, vegetarians and vegans: Results from the EPIC–Oxford study. Public Health Nutr. 14, 340–346 (2011).
    PubMed  Article  PubMed Central  Google Scholar 

    37.
    Harinarayan, C. V., Holick, M. F., Prasad, U. V., Vani, P. S. & Himabindu, G. Vitamin D status and sun exposure in India. Dermato-endocrinology 5, 130–141 (2013).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    38.
    Grant, W. B. et al. Evidence that vitamin D supplementation could reduce risk of influenza and COVID-19 infections and deaths. Nutrients 12, 988 (2020).
    CAS  PubMed Central  Article  PubMed  Google Scholar 

    39.
    Charoenngam, N. & Holick, M. F. Immunologic effects of vitamin D on human health and disease. Nutrients 12, 2097 (2020).
    CAS  PubMed Central  Article  PubMed  Google Scholar 

    40.
    Cui, C. et al. Vitamin D receptor activation regulates microglia polarization and oxidative stress in spontaneously hypertensive rats and angiotensin II-exposed microglial cells: Role of renin-angiotensin system. Redox Biol. 26, 101295 (2019).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    41.
    Xu, J. et al. Vitamin D alleviates lipopolysaccharide-induced acute lung injury via regulation of the renin–angiotensin system. Mol. Med. Rep. 16, 7432–7438 (2017).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    42.
    Adams, J. S. et al. Vitamin D-directed rheostatic regulation of monocyte antibacterial responses. J. Immunol. 182, 4289–4295 (2009).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    43.
    Herr, C., Shaykhiev, R. & Bals, R. The role of cathelicidin and defensins in pulmonary inflammatory diseases. Expert Opin. Biol. Ther. 7, 1449–1461 (2007).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    44.
    Zhou, Y. et al. Effects of human mobility restrictions on the spread of COVID-19 in Shenzhen, China: A modelling study using mobile phone data. Lancet Digit. Health 2, e417–e424 (2020).
    PubMed  PubMed Central  Article  Google Scholar 

    45.
    Lytle, C. D. & Sagripanti, J.-L. Predicted inactivation of viruses of relevance to biodefense by solar radiation. J. Virol. 79, 14244–14252 (2005).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    46.
    Deliconstantinos, G., Villiotou, V. & Stravrides, J. C. Release by ultraviolet B (u.v.B.) radiation of nitric oxide (NO) from human keratinocytes: A potential role for nitric oxide in erythema production. Br. J. Pharmacol. 114, 1257–1265 (1995).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    47.
    D’Orazio, J., Jarrett, S., Amaro-Ortiz, A. & Scott, T. UV radiation and the skin. Int. J. Mol. Sci. 14, 12222–12248 (2013).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    48.
    Grant, W. B. The effect of solar UVB doses and vitamin D production, skin cancer action spectra, and smoking in explaining links between skin cancers and solid tumours. Eur. J. Cancer 44, 12–15 (2008).
    CAS  PubMed  Article  PubMed Central  Google Scholar  More