Philippa Kaur

Read, Q. D., Moorhead, L. C., Swenson, N. G., Bailey, J. K. & Sanders, N. J. Convergent effects of elevation on functional leaf traits within and among species. Funct. Ecol. 28, 37–45. https://doi.org/10.1111/1365-2435.12162 (2014).Article 

Google Scholar 
Isbell, F. et al. Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526, 574–577. https://doi.org/10.1038/nature15374 (2015).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Vellend, M. & Geber, M. A. Connections between species diversity and genetic diversity. Ecol. Lett. 8, 767–781. https://doi.org/10.1111/j.1461-0248.2005.00775.x (2005).Article 

Google Scholar 
Hart, S. P., Schreiber, S. J. & Levine, J. M. How variation between individuals affects species coexistence. Ecol. Lett. 19, 825–838. https://doi.org/10.1111/ele.12618 (2016).Article 
PubMed 

Google Scholar 
Paschke, M. C. & Schmid, B. Relationship between population size, allozyme variation, and plant performance in the narrow endemic Cochlearia bavarica. Conserv. Genet. 3, 131–144 (2002).Article 
CAS 

Google Scholar 
Soleimani, V., Baum, B. & Johnson, D. A. AFLP and pedigree-based genetic diversity estimates in modern cultivars of durum wheat [Triticum turgidum L. subsp. durum (Desf.) Husn.]. Theor. Appl. Genet. 104, 350–357. https://doi.org/10.1007/s001220100714 (2002).Article 
CAS 
PubMed 

Google Scholar 
Hughes, A. R., Inouye, B. D., Johnson, M. T., Underwood, N. & Vellend, M. Ecological consequences of genetic diversity. Ecol. Lett. 11, 609–623. https://doi.org/10.1111/j.1461-0248.2008.01179.x (2008).Article 
PubMed 

Google Scholar 
Prati, D., Peintinger, M. & Fischer, M. Genetic composition, genetic diversity and small-scale environmental variation matter for the experimental reintroduction of a rare plant. J. Plant Ecol. https://doi.org/10.1093/jpe/rtv067 (2016).Article 

Google Scholar 
Barrett, R. D. & Schluter, D. Adaptation from standing genetic variation. Trends Ecol. Evol. 23, 38–44. https://doi.org/10.1016/j.tree.2007.09.008 (2008).Article 
PubMed 

Google Scholar 
Atwater, D. Z. & Callaway, R. M. Testing the mechanisms of diversity-dependent overyielding in a grass species. Ecology 96, 3332–3342. https://doi.org/10.1890/15-0889.1 (2015).Article 
PubMed 

Google Scholar 
Cook-Patton, S. C., McArt, S. H., Parachnowitsch, A. L., Thaler, J. S. & Agrawal, A. A. A direct comparison of the consequences of plant genotypic and species diversity on communities and ecosystem function. Ecology 92, 915–923. https://doi.org/10.1890/10-0999.1 (2011).Article 
PubMed 

Google Scholar 
Whitney, K. D. et al. Experimental drought reduces genetic diversity in the grassland foundation species Bouteloua eriopoda. Oecologia 189, 1107–1120. https://doi.org/10.1007/s00442-019-04371-7 (2019).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Violle, C. et al. Let the concept of trait be functional!. Oikos 116, 882–892. https://doi.org/10.1111/j.0030-1299.2007.15559.x (2007).Article 

Google Scholar 
Kattge, J. et al. TRY plant trait database-enhanced coverage and open access. Glob. Change Biol. 26, 119–188. https://doi.org/10.1111/gcb.14904 (2020).Article 
ADS 

Google Scholar 
König, P. et al. Advances in flowering phenology across the Northern Hemisphere are explained by functional traits. Glob. Ecol. Biogeogr. 27, 310–321 (2018).Article 

Google Scholar 
Robinson, K. M., Ingvarsson, P. K., Jansson, S. & Albrectsen, B. R. Genetic variation in functional traits influences arthropod community composition in aspen (Populus tremula L.). PLoS ONE 7, e37679. https://doi.org/10.1371/journal.pone.0037679 (2012).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Karbstein, K., Prinz, K., Hellwig, F. & Römermann, C. Plant intraspecific functional trait variation is related to within-habitat heterogeneity and genetic diversity in Trifolium montanum L. Ecol. Evol. 10, 5015–5033. https://doi.org/10.1002/ece3.6255 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Kaya, S. & Tekin, A. R. The effect of salep content on the rheological characteristics of a typical ice-cream mix. J. Food Eng. 47, 59–62. https://doi.org/10.1016/S0260-8774(00)00093-5 (2001).Article 

Google Scholar 
Ktistis, G. & Georgakopoulos, P. P. Rheology of salep mucilages. Pharmazie 46, 55–56 (1991).CAS 

Google Scholar 
Kayacier, A. & Dogan, M. Rheological properties of some gums-salep mixed solutions. J. Food Eng. 72, 261–265. https://doi.org/10.1016/j.jfoodeng.2004.12.005 (2006).Article 
CAS 

Google Scholar 
Sen, M. A., Palabiyik, I. & Kurultay, S. The effect of saleps obtained from various Orchidacease species on some physical and sensory properties of ice cream. Food Sci. Technol. 39, 82–87. https://doi.org/10.1590/fst.26017 (2019).Article 

Google Scholar 
Farhoosh, R. & Riazi, A. A compositional study on two current types of salep in Iran and their rheological properties as a function of concentration and temperature. Food Hydrocoll. 21, 660–666. https://doi.org/10.1016/j.foodhyd.2006.07.021 (2007).Article 
CAS 

Google Scholar 
Ghorbani, A., Zarre, S., Gravendeel, B. & de Boer, H. J. Illegal wild collection and international trade of CITES-listed terrestrial orchid tubers in Iran. Traffic Bullet. 26, 52–58 (2014).
Google Scholar 
Lenoir, J., Gégout, J.-C., Marquet, P., De Ruffray, P. & Brisse, H. A significant upward shift in plant species optimum elevation during the 20th century. Science 320, 1768–1771. https://doi.org/10.1126/science.1156831 (2008).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Chen, Z.-Q., Algeo, T. J. & Fraiser, M. L. Organism-environment interactions during the Permian-Triassic mass extinction and its aftermath. Palaios 28, 661–663. https://doi.org/10.2110/palo.2012.p12-102r (2013).Article 
ADS 

Google Scholar 
Ebrahimi, A. et al. Evaluation of phenotypic diversity of the endangered orchid (Orchis mascula): Emphasizing on breeding, conservation and development. S. Afr. J. Bot. 132, 304–315. https://doi.org/10.1016/j.sajb.2020.05.013 (2020).Article 

Google Scholar 
Ghorbani, A., Gravendeel, B., Naghibi, F. & de Boer, H. Wild orchid tuber collection in Iran: A wake-up call for conservation. Biodivers. Conserv. 23, 2749–2760. https://doi.org/10.1007/s10531-014-0746-y (2014).Article 

Google Scholar 
Barrett, S. C. & Kohn, J. R. The application of minimum viable population theory to plants. Genetics and conservation of rare plants 3–1 (Oxford University Press, 1991).
Google Scholar 
Yun, S. A., Son, H.-D., Im, H.-T. & Kim, S.-C. Genetic diversity and population structure of the endangered orchid Pelatantheria scolopendrifolia (Orchidaceae) in Korea. PLoS ONE 15, e0237546. https://doi.org/10.1371/journal.pone.0237546 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Gholami, S., Vafaee, Y., Nazari, F. & Ghorbani, A. Exploring genetic variations in threatened medicinal orchids using start codon targeted (SCoT) polymorphism and marker-association with seed morphometric traits. Physiol. Mol. Biol. Plants 27, 769–785. https://doi.org/10.1007/s12298-021-00978-4 (2021).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Gholami, S., Vafaee, Y., Nazari, F. & Ghorbani, A. Molecular characterization of endangered Iranian terrestrial orchids using ISSR markers and association with floral and tuber-related phenotypic traits. Physiol. Mol. Biol. Plants 27, 53–68. https://doi.org/10.1007/s12298-020-00920-0 (2021).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Kaki, A., Vafaee, Y. & Khadivi, A. Genetic variation of Anacamptis coriophora, Dactylorhiza umbrosa, Himantoglossum affine, Orchis mascula, and Ophrys schulzei in the western parts of Iran. Ind. Crops Prod. 156, 112854. https://doi.org/10.1016/j.indcrop.2020.112854 (2020).Article 
CAS 

Google Scholar 
Falk, D., & Holsinger, K. E. Genetic sampling guidelines for conservation collections of endangered plants (1991).Dempewolf, H. et al. Past and future use of wild relatives in crop breeding. Crop Sci. 57, 1070–1082. https://doi.org/10.2135/cropsci2016.10.0885 (2017).Article 

Google Scholar 
Renz, J. Flora Iranica. Part 126: Orchidaceae (1978).Shahsavari, A. Flora of Iran. Part 57: Orchidaceae (2008).Boulila, A., Béjaoui, A., Messaoud, C. & Boussaid, M. Genetic diversity and population structure of Teucrium polium (Lamiaceae) in Tunisia. Biochem. Gen. 48, 57–70. https://doi.org/10.1007/s10528-009-9295-6 (2010).Article 
CAS 

Google Scholar 
Zannou, A., Struik, P., Richards, P., Zoundjih, E. & Yam, J. (Dioscorea spp.) responses to the environmental variability in the Guinea Sudan zone of Benin. Afr. J. Agric. Res. 10, 4913–4925. https://doi.org/10.5897/AJAR2013.8099 (2015).Article 

Google Scholar 
Sujii, P. et al. Morphological and molecular characteristics do not confirm popular classification of the Brazil nut tree in Acre, Brazil. Genet. Mol. Res. https://doi.org/10.4238/2013.september.27.3 (2013).Article 
PubMed 

Google Scholar 
Nadeem, M. A. et al. DNA molecular markers in plant breeding: current status and recent advancements in genomic selection and genome editing. Biotechnol. Biotechnol. Equip. 32, 261–285. https://doi.org/10.1080/13102818.2017.1400401 (2018).Article 
CAS 

Google Scholar 
Jacquemyn, H., Brys, R., Adriaens, D., Honnay, O. & Roldán-Ruiz, I. Effects of population size and forest management on genetic diversity and structure of the tuberous orchid Orchis mascula. Conserv. Genet. 10, 161–168. https://doi.org/10.1007/s10592-008-9543-z (2009).Article 

Google Scholar 
Mitchell, P. & Woodward, F. Responses of three woodland herbs to reduced photosynthetically active radiation and low red to far-red ratio in shade. J. Ecol. https://doi.org/10.2307/2260575 (1988).Article 

Google Scholar 
Likens, G. E., Bormann, F. H., Johnson, N. M., Fisher, D. & Pierce, R. S. Effects of forest cutting and herbicide treatment on nutrient budgets in the Hubbard Brook watershed-ecosystem. Ecol. Monog. 40, 23–47. https://doi.org/10.2307/1942440 (1970).Article 

Google Scholar 
Jacquemyn, H. & Brys, R. Lack of strong selection pressures maintains wide variation in floral traits in a food-deceptive orchid. Ann. Bot. 126, 445–453. https://doi.org/10.1093/aob/mcaa080 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Olaya-Arenas, P., Meléndez-Ackerman, E. J., Pérez, M. E. & Tremblay, R. Demographic response by a small epiphytic orchid. Am. J. Bot. 98, 2040–2048. https://doi.org/10.3732/ajb.1100223 (2011).Article 
PubMed 

Google Scholar 
Primack, R. B., Miao, S. & Becker, K. R. Costs of reproduction in the pink lady’s slipper orchid (Cypripedium acaule): Defoliation, increased fruit production, and fire. Am. J. Bot. 81, 1083–1090. https://doi.org/10.2307/2446500 (1994).Article 

Google Scholar 
Whigham, D. F. & O’Neill, J. P. Dynamics of flowering and fruit production in two eastern North American terrestrial orchids. In Tipularia Discolor and Liparis Lilifolia in Population Ecology of Terrestrial Orchids (eds Wells, T. C. E. & Willems, J. H.) 89–101 (SPB Academic Publishers, 1991).
Google Scholar 
Tekinşen, K. K. & Güner, A. Chemical composition and physicochemical properties of tubera salep produced from some Orchidaceae species. Food Chem. 121, 468–471. https://doi.org/10.1016/j.foodchem.2009.12.066 (2010).Article 
CAS 

Google Scholar 
Whigham, D. F. Biomass and nutrient allocation of Tipularia discolor (Orchidaceae). Oikos https://doi.org/10.2307/3544398 (1984).Article 

Google Scholar 
Mattila, E. & Kuitunen, M. T. Nutrient versus pollination limitation in Platanthera bifolia and Dactylorhiza incarnata (Orchidaceae). Oikos 89, 360–366. https://doi.org/10.1034/j.1600-0706.2000.890217.x (2000).Article 

Google Scholar 
Xu, W. et al. Drought stress condition increases root to shoot ratio via alteration of carbohydrate partitioning and enzymatic activity in rice seedlings. Acta Physiol. Plant. 37, 9. https://doi.org/10.1007/s11738-014-1760-0 (2015).Article 
CAS 

Google Scholar 
March-Salas, M., Fandos, G. & Fitze, P. S. Effects of intrinsic environmental predictability on intra-individual and intra-population variability of plant reproductive traits and eco-evolutionary consequences. Ann. Bot. 127, 413–423. https://doi.org/10.1093/aob/mcaa096 (2021).Article 
CAS 
PubMed 

Google Scholar 
Jump, A. S., Marchant, R. & Peñuelas, J. Environmental change and the option value of genetic diversity. Trends Plant Sci. 14, 51–58. https://doi.org/10.1016/j.tplants.2008.10.002 (2009).Article 
CAS 
PubMed 

Google Scholar 
Huang, J. et al. Global semi-arid climate change over last 60 years. Clim. Dyn. 46, 1131–1150. https://doi.org/10.1007/s00382-015-2636-8 (2016).Article 

Google Scholar 
Crémieux, L., Bischoff, A., Müller-Schärer, H. & Steinger, T. Gene flow from foreign provenances into local plant populations: Fitness consequences and implications for biodiversity restoration. Am. J. Bot. 97, 94–100. https://doi.org/10.3732/ajb.0900103 (2010).Article 
PubMed 

Google Scholar 
Garant, D., Forde, S. E. & Hendry, A. P. The multifarious effects of dispersal and gene flow on contemporary adaptation. Funct. Ecol. 21, 434–443. https://doi.org/10.1111/j.1365-2435.2006.01228.x (2007).Article 

Google Scholar 
Jacquemyn, H. et al. Multigenerational analysis of spatial structure in the terrestrial, food-deceptive orchid Orchis mascula. J. Ecol. 97, 206–216. https://doi.org/10.1111/j.1365-2745.2008.01464.x (2009).Article 

Google Scholar 
Siepielski, A. M. et al. Precipitation drives global variation in natural selection. Science 355, 959–962. https://doi.org/10.1126/science.aag2773 (2017).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Ene, C. O., Ogbonna, P. E., Agbo, C. U. & Chukwudi, U. P. Studies of phenotypic and genotypic variation in sixteen cucumber genotypes. Chilean J. Agric. Res. 76, 307–313. https://doi.org/10.4067/S0718-58392016000300007 (2016).Article 

Google Scholar 
Pradhan, S. K. et al. Population structure, genetic diversity and molecular marker-trait association analysis for high temperature stress tolerance in rice. PLoS ONE 11, e0160027. https://doi.org/10.1371/journal.pone.0160027 (2016).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Swarup, S. et al. Genetic diversity is indispensable for plant breeding to improve crops. Crop Sci. 61, 839–852. https://doi.org/10.1002/csc2.20377 (2021).Article 

Google Scholar 
Patzak, A. Plantaginaceae in KH Rechinger Flora Iranica 15: 1–21 (Academische Druck und Verlagsantalt, 1965).
Google Scholar 
Mehrvarz Saeidi, S. Plantaginaceae Family Vol. 14 (Research Institute of Forests and Rangelands, 1995).
Google Scholar 
Limited, M. I. I. Glucomannan assay procedure KGLUM 10/04. Ireland (2004).Limited, M. I. I. Total starch assay procedure (amyloglucosidase/a-Amylase Method) AA/AMG 11/01. AOAC Method 996.11.Ireland (2004).Bradshaw, H., Otto, K. G., Frewen, B. E., McKay, J. K. & Schemske, D. W. Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics 149, 367–382. https://doi.org/10.1093/genetics/149.1.367 (1998).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Del Sal, G., Manfioletti, G. & Schneider, C. The CTAB-DNA precipitation method: A common mini-scale preparation of template DNA from phagemids, phages or plasmids suitable for sequencing. Biotechniques 7, 514–520 (1989).PubMed 

Google Scholar 
Vos, P. et al. AFLP: A new technique for DNA fingerprinting. Nucl. Acid Res. 23, 4407–4414. https://doi.org/10.1093/nar/23.21.4407 (1995).Article 
CAS 

Google Scholar 
Bassam, B. J., Caetano-Anollés, G. & Gresshoff, P. M. Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal. Biochem. 196, 80–83. https://doi.org/10.1016/0003-2697(91)90120-I (1991).Article 
CAS 
PubMed 

Google Scholar 
Husson, F., Josse, J., Le, S., Mazet, J. & Husson, M. F. Package ‘FactoMineR’. An R package 96, 698 (2016).
Google Scholar 
Lê, S., Josse, J. & Husson, F. FactoMineR: An R package for multivariate analysis. J. Stat. Softw. 25, 1–18 (2008).Article 

Google Scholar 
Galili, T. in The R User Conference, useR! 2017 July 4–7 2017 Brussels, Belgium. 219.Wei, T. et al. Package ‘corrplot’. 56, e24 (2017).Yeh, F. POPGENE (version 1.3. 1). Microsoft Window-Bases Freeware for Population Genetic Analysis. http://www.ualbertaca/~fyeh/ (1999).Wickham, H. & Chang, W. URL: http://CRAN.R-project.org/package=ggplot2.ggplot2: An implementation of the Grammar of Graphics. 3 (2008).Kolde, R. & Kolde, M. R. Package’ pheatmap’. R package 1, 790 (2015).
Google Scholar 
Landgraf, A. J. & Lee, Y. Dimensionality reduction for binary data through the projection of natural parameters. J. Mult. Anal. 180, 104668. https://doi.org/10.1016/j.jmva.2020.104668 (2020).Article 
MathSciNet 
MATH 

Google Scholar 
Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959. https://doi.org/10.1093/genetics/155.2.945 (2000).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Earl, D. A. & VonHoldt, B. M. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Biol. J. Linn. Soc. 4, 359–361. https://doi.org/10.1007/s12686-011-9548-7 (2012).Article 

Google Scholar 
Oksanen, J. et al. Vegan: Community Ecology Package. R package version 2.4-3 (2016).Kamvar, Z. N., Tabima, J. F. & Grünwald, N. J. Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. Peer. J. 2, e281 (2014).Article 
PubMed 
PubMed Central 

Google Scholar 
Vavrek, M. J. Fossil: Palaeoecological and palaeogeographical analysis tools. Palaeontol. Electron. 14, 16. https://doi.org/10.7717/peerj.281 (2011).Article 

Google Scholar 
Bradbury, P. J. et al. TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics 23, 2633–2635. https://doi.org/10.1093/bioinformatics/btm308 (2007).Article 
CAS 
PubMed 

Google Scholar  More

Phung, T. X., Nascimento, J. C. S., Novarro, A. J. & Wiens, J. J. Correlated and decoupled evolution of adult and larval body size in frogs. Proc. R. Soc. Lond. B 287, 20201474–10 (2020).
Google Scholar 
Hall, B. K. & Wake, M. H. The Origin and Evolution of Larval Forms (Gulf Professional Publishing, 1999).Hime, P. M. et al. Phylogenomics reveals ancient gene tree discordance in the amphibian tree of life. Syst. Biol. 70, 49–66 (2021).CAS 
PubMed 

Google Scholar 
Duellman, W. E. & Trueb, L. Biology of Amphibians (Johns Hopkins University Press, 1994).Nunes-de-Almeida, C. H., Batista Haddad, C. F. & Toledo, L. F. A revised classification of the amphibian reproductive modes. Salamandra 57, 413–427 (2021).
Google Scholar 
Vences, M. & Köhler, J. Global diversity of amphibians (Amphibia) in freshwater. Hydrobiologia 595, 569–580 (2007).
Google Scholar 
Blackburn, D. G. Evolution of vertebrate viviparity and specializations for fetal nutrition: a quantitative and qualitative analysis. J. Morphol. 276, 961–990 (2015).PubMed 

Google Scholar 
AmphibiaWeb. Electronic Database (University of California, Berkeley, CA, USA, 2019). https://amphibiaweb.org.Frost, D. R. Amphibian Species of the World: an Online Reference. Version 6.0 (date of access: 01.08.2019). Electronic Database (American Museum of Natural History, New York, USA, 2019). https://amphibiansoftheworld.amnh.org/.Bonett, R. M., Ledbetter, N. M., Hess, A. J., Herrboldt, M. A. & Denoël, M. Repeated ecological and life cycle transitions make salamanders an ideal model for evolution and development. Developmental Dynamics 251, 957–972 (2022).Salthe, S. N. Reproductive modes and the number and sizes of ova in the urodeles. Am. Midl. Naturalist 81, 467490 (1969).
Google Scholar 
Salthe, S. N. & Duellman, W. E. in Evolutionary Biology of the Anurans (ed. Vial, J. L.) 229–249 (University of Missouri Press Columbia, 1973).Haddad, C. & Prado, C. P. A. Reproductive modes in frogs and their unexpected diversity in the Atlantic Forest of Brazil. BioScience 55, 207–217 (2005).
Google Scholar 
Lutz, B. Ontogenetic evolution in frogs. Evolution 2, 29–39 (1948).CAS 
PubMed 

Google Scholar 
Crump, M. L. Anuran reproductive modes: evolving perspectives. J. Herpetol. 49, 1–16 (2015).
Google Scholar 
Schoch, R. Evolution of life cycles in early amphibians. Annu. Rev. Earth Planet. Sci. 37, 135–162 (2009).ADS 
CAS 

Google Scholar 
Meegaskumbura, M. et al. Patterns of reproductive-mode evolution in Old World tree frogs (Anura, Rhacophoridae). Zool. Scr. 44, 509–522 (2015).
Google Scholar 
Portik, D. M. & Blackburn, D. C. The evolution of reproductive diversity in Afrobatrachia: A phylogenetic comparative analysis of an extensive radiation of African frogs. Evolution 70, 2017–2032 (2016).PubMed 
PubMed Central 

Google Scholar 
San Mauro, D. et al. Life-history evolution and mitogenomic phylogeny of caecilian amphibians. Mol. Phylogenet. Evol. 73, 177–189 (2014).PubMed 

Google Scholar 
Pereira, E. B., Collevatti, R. G., de Carvalho Kokubum, M. N., de Oliveira Miranda, N. E. & Maciel, N. M. Ancestral reconstruction of reproductive traits shows no tendency toward terrestriality in leptodactyline frogs. BMC Evol. Biol. 15, 91 (2015).Gomez-Mestre, I., Pyron, R. A. & Wiens, J. J. Phylogenetic analyses reveal unexpected patterns in the evolution of reproductive modes in frogs. Evolution 66, 3687–3700 (2012).PubMed 

Google Scholar 
Wake, D. B. & Hanken, J. Direct development in the lungless salamanders: what are the consequences for developmental biology, evolution and phylogenesis? Int. J. Dev. Biol. 40, 859–869 (1996).CAS 
PubMed 

Google Scholar 
Dubois, A. Developmental pathway, speciation and supraspecific taxonomy in amphibians: 1. Why are there so many frog species in Sri Lanka? Alytes 22, 19–37 (2004).
Google Scholar 
Hedges, S. B., Duellman, W. E. & Heinicke, M. P. New World direct-developing frogs (Anura: Terrarana): molecular phylogeny, classification, biogeography, and conservation. Zootaxa 1737, 1–182 (2008).
Google Scholar 
Dugo-Cota, Á., Vilà, C., Rodríguez, A. & Gonzalez-Voyer, A. Ecomorphological convergence in Eleutherodactylus frogs: a case of replicate radiations in the Caribbean. Ecol. Lett. 22, 884–893 (2019).PubMed 

Google Scholar 
Simpson, G. G. The Major Features of Evolution (Columbia University Press, 1953).Vági, B., Végvári, Z., Liker, A., Freckleton, R. P. & Szekely, T. Parental care and the evolution of terrestriality in frogs. Proc. R. Soc. Lond. B 286, 20182737–10 (2019).
Google Scholar 
Furness, A. I. & Capellini, I. The evolution of parental care diversity in amphibians. Nat. Commun. 10, 1–12 (2019).CAS 

Google Scholar 
Furness, A. I., Venditti, C. & Capellini, I. Terrestrial reproduction and parental care drive rapid evolution in the trade-off between offspring size and number across amphibians. PLoS Biol. 20, e3001495 (2022).CAS 
PubMed 
PubMed Central 

Google Scholar 
Wollenberg, K. C., Vieites, D. R., Glaw, F. & Vences, M. Speciation in little: the role of range and body size in the diversification of Malagasy mantellid frogs. BMC Evol. Biol. 11, 217 (2011).PubMed 
PubMed Central 

Google Scholar 
Cayuela, H. et al. Determinants and consequences of dispersal in vertebrates with complex life cycles: a review of pond-breeding amphibians. Q. Rev. Biol. 95, 1–36 (2020).
Google Scholar 
Phillimore, A. B., Freckleton, R. P., Orme, C. D. L. & Owens, I. P. F. Ecology predicts large‐scale patterns of phylogenetic diversification in birds. Am. Nat. 168, 220–229 (2006).PubMed 

Google Scholar 
Chen, J.-M. et al. An integrative phylogenomic approach illuminates the evolutionary history of Old World tree frogs (Anura: Rhacophoridae). Mol. Phylogenet. Evol. 145, 106724 (2020).PubMed 

Google Scholar 
Zimkus, B. M., Lawson, L., Loader, S. P. & Hanken, J. Terrestrialization, miniaturization and rates of diversification in African Puddle Frogs (Anura: Phrynobatrachidae). PLoS ONE 7, e35118 (2012).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Moen, D. S. Improving inference and avoiding over-interpretation of hidden-state diversification models: specialized plant breeding has no effect on diversification in frogs. Evolution 76, 373–384 (2022).PubMed 

Google Scholar 
Eastman, J. M. & Storfer, A. Correlations of life-history and distributional-range variation with salamander diversification rates: evidence for species selection. Syst. Biol. 60, 503–518 (2011).PubMed 

Google Scholar 
Bonett, R. M., Steffen, M. A., Lambert, S. M., Wiens, J. J. & Chippindale, P. T. Evolution of paedomorphosis in plethodontid salamanders: ecological correlates and re-evolution of metamorphosis. Evolution 68, 466–482 (2014).PubMed 

Google Scholar 
Akaike, H. A new look at the statistical-model identification. IEEE Trans. Autom. Control 19, 716–723 (1974).ADS 
MathSciNet 
MATH 

Google Scholar 
Wagenmakers, E.-J. & Farrell, S. AIC model selection using Akaike weights. Psychon. Bull. Rev. 11, 192–196 (2004).PubMed 

Google Scholar 
Beaulieu, J. M., Oliver, J. C., O’Meara, B. & Boyko, J. R package ‘corHMM’: hidden markov models of character evolution. (2020).Pagel, M. & Meade, A. BayesTraits, version 4. University of Reading, Berkshire, UK. http://www.evolution.rdg.ac.uk (2022).Pagel, M. & Meade, A. Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am. Nat. 167, 808–825 (2006).PubMed 

Google Scholar 
Maddison, W., Midford, P. & Otto, S. Estimating a binary character’s effect on speciation and extinction. Syst. Biol. 56, 701–710 (2007).PubMed 

Google Scholar 
FitzJohn, R. G., Maddison, W. P. & Otto, S. P. Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies. Syst. Biol. 58, 595–611 (2009).PubMed 

Google Scholar 
Beaulieu, J. M. & O’Meara, B. C. Detecting hidden diversification shifts in models of trait-dependent speciation and extinction. Syst. Biol. 65, 583–601 (2016).PubMed 

Google Scholar 
Herrera-Alsina, L., van Els, P. & Etienne, R. S. Detecting the dependence of diversification on multiple traits from phylogenetic trees and trait data. Syst. Biol. 68, 317–328 (2018).
Google Scholar 
Strathmann, R. R. Hypotheses on the origins of marine larvae. Annu. Rev. Ecol. Syst. 24, 89–117 (1993).
Google Scholar 
Wray, G. A. Evolution of larvae and developmental modes. In Ecology of Marine Invertebrate Larvae. (ed. McEdward, L.) 413–447 (CRC Press, 1995).Raff, R. A. Origins of the other metazoan body plans: the evolution of larval forms. Philos. T R. Soc. B 363, 1473–1479 (2008).
Google Scholar 
Collin, R. & Moran, A. in Evolutionary Ecology of Marine Invertebrate Larvae 50–66 (Oxford University Press, 2018).Collin, R. & Miglietta, M. P. Reversing opinions on Dollo’s Law. Trends Ecol. Evol. 23, 602–609 (2008).PubMed 

Google Scholar 
Wiens, J. J. Re-evolution of lost mandibular teeth in frogs after more than 200 million years, and re-evaluating Dollo’s law. Evolution 65, 1283–1296 (2011).PubMed 

Google Scholar 
Wiens, J. J., Kuczynski, C. A., Duellman, W. E. & Reeder, T. W. Loss and re-evolution of complex life cycles in marsupial frogs: does ancestral trait reconstruction mislead? Evolution 61, 1886–1899 (2007).CAS 
PubMed 

Google Scholar 
Chippindale, P. T., Bonett, R. M., Baldwin, A. S. & Wiens, J. J. Phylogenetic evidence for a major reversal of life-history evolution in plethodontid salamanders. Evolution 58, 2809–2815 (2004).CAS 
PubMed 

Google Scholar 
Castroviejo-Fisher, S. et al. Phylogenetic systematics of egg-brooding frogs (Anura: Hemiphractidae) and the evolution of direct development. Zootaxa 4004, 1–75 (2015).PubMed 

Google Scholar 
Naumann, B., Schweiger, S., Hammel, J. U. & Müller, H. Parallel evolution of direct development in frogs—skin and thyroid gland development in African Squeaker Frogs (Anura: Arthroleptidae: Arthroleptis). Dev. Dyn. 250, 584–600 (2021).PubMed 

Google Scholar 
Goldberg, J., Taucce, P. P. G., Quinzio, S. I., Haddad, C. F. B. & Candioti, F. V. Increasing our knowledge on direct-developing frogs: the ontogeny of Ischnocnema henselii (Anura: Brachycephalidae). Zool. Anz. 284, 78–87 (2020).
Google Scholar 
Wassersug, R. J. & Duellman, W. E. Oral structures and their development in egg-brooding hylid frog embryos and larvae: evolutionary and ecological implications. J. Morphol. 182, 1–37 (1984).PubMed 

Google Scholar 
Kerney, R. R., Blackburn, D. C., Müller, H. & Hanken, J. Do larval traits re-evolve? Evidence from the embryogenesis of a direct-developing salamander, Plethodon cinereus. Evolution 66, 252–262 (2011).PubMed 

Google Scholar 
Theska, T. Musculoskeletal development of the Central African caecilian Idiocranium russeli (Amphibia: Gymnophiona: Indotyphlidae) and its bearing on the re-evolution of larvae in caecilian amphibians. Zoomorphology 138, 137–158 (2019).
Google Scholar 
Laslo, M., Denver, R. J. & Hanken, J. Evolutionary conservation of thyroid hormone receptor and deiodinase expression dynamics in ovo in a direct-developing frog, Eleutherodactylus coqui. Front. Endocrinol. 10, 307 (2019).
Google Scholar 
Gao, W. et al. Genomic and transcriptomic investigations of the evolutionary transition from oviparity to viviparity. Proc. Natl Acad. Sci. USA 116, 3646–3655 (2019).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Altig, R. & Crother, B. I. The evolution of three deviations from the biphasic anuran life cycle: alternatives to selection. Herpetol. Rev. 37, 321–356 (2006).
Google Scholar 
Venturelli, D. P., da Silva, W. R. & Giaretta, A. A. Tadpoles’ resistance to desiccation in species of Leptodactylus (Anura, Leptodactylidae). J. Herpetol. 55, 265–270 (2021).
Google Scholar 
Seymour, R. S. Respiration of aquatic and terrestrial amphibian embryos. American Zoologist 39, 261–270 (1999).Blackburn, D. G. Convergent evolution of viviparity, matrotrophy, and specializations for fetal nutrition in reptiles and other vertebrates. Am. Zool. 32, 313–321 (1992).
Google Scholar 
Buckley, D., Alcobendas, M., García-París, M. & Wake, M. H. Heterochrony, cannibalism, and the evolution of viviparity in Salamandra salamandra. Evol. Dev. 9, 105–115 (2007).PubMed 

Google Scholar 
Kusrini, M. D., Rowley, J. J. L., Khairunnisa, L. R., Shea, G. M. & Altig, R. The reproductive biology and larvae of the first tadpole-bearing frog, Limnonectes larvaepartus. PLoS ONE 10, e116154–e116159 (2015).ADS 
PubMed 
PubMed Central 

Google Scholar 
Lanza, B. & Leo, P. Sul primo caso sicuro di riproduzione vivipara nel genere Speleomantes. 1–54 (2000).Lunghi, E. et al. Comparative reproductive biology of European cave salamanders (Genus Hydromantes): nesting selection and multiple annual breeding. Salamandra 54, 101–108 (2018).
Google Scholar 
Liedtke, H. C. et al. Terrestrial reproduction as an adaptation to steep terrain in African toads. Proc. R. Soc. Lond. B 284, 20162598–20162599 (2017).
Google Scholar 
Wake, M. H. The reproductive biology of Eleutherodactylus jasperi (Amphibia, Anura, Leptodactylidae), with comments on the evolution of live-bearing systems. J. Herpetol. 12, 121–133 (1978).
Google Scholar 
Jennings, D. H. & Hanken, J. Mechanistic basis of life history evolution in anuran amphibians: thyroid gland development in the direct-developing frog, Eleutherodactylus coqui. Gen. Comp. Endocr. 111, 225–232 (1998).CAS 
PubMed 

Google Scholar 
Callery, E. M. & Elinson, R. P. Thyroid hormone-dependent metamorphosis in a direct developing frog. Proc. Natl Acad. Sci. USA 97, 2615–2620 (2000).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Callery, E. M., Hung, F. & Elinson, R. P. Frogs without polliwogs: evolution of anuran direct development. BioEssays 23, 233–241 (2001).CAS 
PubMed 

Google Scholar 
Buckley, L. B. & Jetz, W. Environmental and historical constraints on global patterns of amphibian richness. Proc. R. Soc. Lond. B 274, 1167–1173 (2007).
Google Scholar 
Pyron, R. A. & Wiens, J. J. Large-scale phylogenetic analyses reveal the causes of high tropical amphibian diversity. Proc. R. Soc. Lond. B 280, 20131622 (2013).
Google Scholar 
Gómez-Rodríguez, C., Baselga, A. & Wiens, J. J. Is diversification rate related to climatic niche width? Glob. Ecol. Biogeogr. 24, 383–395 (2015).
Google Scholar 
Moen, D. S. & Wiens, J. J. Microhabitat and climatic niche change explain patterns of diversification among frog families. Am. Nat. 190, 29–44 (2017).PubMed 

Google Scholar 
Kozak, K. H. & Wiens, J. J. Accelerated rates of climatic-niche evolution underlie rapid species diversification. Ecol. Lett. 13, 1378–1389 (2010).PubMed 

Google Scholar 
Jaramillo, A. F. et al. Vastly underestimated species richness of Amazonian salamanders (Plethodontidae: Bolitoglossa) and implications about plethodontid diversification. Mol. Phylogenet. Evol. 149, 106841 (2020).PubMed 

Google Scholar 
Jetz, W. & Pyron, R. A. The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nat. Ecol. Evol. 2, 850–858 (2018).PubMed 

Google Scholar 
Bars-Closel, M., Kohlsdorf, T., Moen, D. S. & Wiens, J. J. Diversification rates are more strongly related to microhabitat than climate in squamate reptiles (lizards and snakes). Evolution 71, 2243–2261 (2017).PubMed 

Google Scholar 
Cyriac, V. P. & Kodandaramaiah, U. Digging their own macroevolutionary grave: fossoriality as an evolutionary dead end in snakes. J. Evolution. Biol. 31, 587–598 (2018).CAS 

Google Scholar 
Zamudio, K. R., Bell, R. C., Nali, R. C., Haddad, C. F. B. & Prado, C. P. A. Polyandry, predation, and the evolution of frog reproductive modes. Am. Nat. 188, S41–S61 (2016).PubMed 

Google Scholar 
Lion, M. B. et al. Global patterns of terrestriality in amphibian reproduction. Glob. Ecol. Biogeogr. 4, 679–13 (2019).
Google Scholar 
Müller, H. et al. Forests as promoters of terrestrial life-history strategies in East African amphibians. Biol. Lett. 9, 20121146–20121146 (2013).PubMed 
PubMed Central 

Google Scholar 
Velo-Antón, G., García-París, M., Galán, P. & Cordero Rivera, A. The evolution of viviparity in Holocene islands: ecological adaptation versus phylogenetic descent along the transition from aquatic to terrestrial environments. J. Zool. Syst. Evol. Res. 45, 345–352 (2007).
Google Scholar 
Liedtke, H. C. AmphiNom: an amphibian systematics tool. Syst. Biodivers. 17, 1–6 (2019).
Google Scholar 
R Core Team. R: a language and environment for statistical computing (R Foundation for Statistical Computing, Vienna, Austria, 2020). http://www.R-project.org/.IUCN. IUCN 2020. The IUCN Red List of Threatened Species. Version 2020-2. https://www.iucnredlist.org (2019).AmphibiaChina. The database of Chinese amphibians. Electronic Database (Kunming Institute of Zoology (CAS), Kunming, Yunnan, China, 2019) http://www.amphibiachina.org/.Ron, S. R., Yanez-Muñoz, M. H., Merino-Viteri, A. & Ortiz, D. A. Anfibios del Ecuador. Version 2019.0 (Museo de Zoología, Pontificia Universidad Católica del Ecuador, 2019). https://bioweb.bio/faunaweb/amphibiaweb.Greven, H. In Reproductive Biology and Phylogeny of Urodela 447–475 (Taylor & Francis, 2003).Marks, S. B. & Collazo, A. Direct development in Desmognathus aeneus (Caudata: Plethodontidae): a staging table. Copeia 1998, 637–648 (1998).
Google Scholar 
Müller, H., Loader, S. P., Ngalason, W., Howell, K. M. & Gower, D. J. Reproduction in brevicipitid frogs (Amphibia: Anura: Brevicipitidae)—evidence from Probreviceps m. macrodactylus. Copeia 2007, 726–733 (2007).
Google Scholar 
Velo-Antón, G., Santos, X., Sanmartín-Villar, I., Cordero-Rivera, A. & Buckley, D. Intraspecific variation in clutch size and maternal investment in pueriparous and larviparous Salamandra salamandra females. Evol. Ecol. 29, 185–204 (2014).
Google Scholar 
Beaulieu, J. M., O’Meara, B. C. & Donoghue, M. J. Identifying hidden rate changes in the evolution of a binary morphological character: the evolution of plant habit in campanulid angiosperms. Systematic biology 62, 725–737 (2013).Pupko, T., Pe’er, I., Shamir, R. & Graur, D. A fast algorithm for joint reconstruction of ancestral amino acid sequences. Mol. Biol. Evol. 17, 890–896 (2000).CAS 
PubMed 

Google Scholar 
Bollback, J. P. SIMMAP: stochastic character mapping of discrete traits on phylogenies. BMC Bioinforma. 7, 88 (2006).
Google Scholar 
Plummer, M., Best, N., Cowles, K. & Vines, K. CODA: convergence diagnosis and output analysis for MCMC. R. News 6, 7–11 (2006).
Google Scholar 
Tuffley, C. & Steel, M. Modeling the covarion hypothesis of nucleotide substitution. Math. Biosci. 147, 63–91 (1998).MathSciNet 
CAS 
PubMed 
MATH 

Google Scholar 
Xie, W., Lewis, P. O., Fan, Y., Kuo, L. & Chen, M. H. Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Syst. Biol. 60, 150–160 (2011).PubMed 

Google Scholar 
Nakov, T., Beaulieu, J. M. & Alverson, A. J. Diatoms diversify and turn over faster in freshwater than marine environments. Evolution 73, 2497–2511 (2019).PubMed 

Google Scholar 
Etienne, R. S. et al. Diversity-dependence brings molecular phylogenies closer to agreement with the fossil record. Proc. R. Soc. Lond. B 279, 1300–1309 (2011).
Google Scholar  More

Kristensen, T. N. et al. A test of quantitative genetic theory using Drosophila- effects of inbreeding and rate of inbreeding on heritabilities and variance components. J. Evol. Biol. 18, 763–770 (2005).CAS 
PubMed 

Google Scholar 
Angeloni, F., Ouborg, N. J. & Leimu, R. Meta-analysis on the association of population size and life history with inbreeding depression in plants. Biol. Conserv. 144, 35–43 (2011).
Google Scholar 
Caballero, A., Bravo, I. & Wang, J. Inbreeding load and purging: implications for the short-term survival and the conservation management of small populations. Heredity 118, 177–185 (2017).CAS 
PubMed 

Google Scholar 
Park, D. S., Ellison, A. M. & Davis, C. C. Mating system does not predict niche breath. Glob. Ecol. Biogeogr. 27, 804–813 (2018).
Google Scholar 
Buckley, J., Daly, R., Cobbold, C. A., Burgess, K. & Mable, B. K. Changing environments and genetic variation: natural variation in inbreeding does not compromise short-term physiological responses. Proc. R. Soc. B Biol. Sci. 286, 20192109 (2019).
Google Scholar 
Grossenbacher, D., Briscoe Runquist, R., Goldberg, E. E. & Brandvain, Y. Geographic range size is predicted by plant mating system. Ecol. Lett. 18, 706–713 (2015).PubMed 

Google Scholar 
Wright, S. I., Lauga, B. & Charlesworth, D. Rates and patterns of molecular evolution in inbred and outbred arabidopsis. Mol. Biol. Evol. 19, 1407–1420 (2002).CAS 
PubMed 

Google Scholar 
Atwell, S. et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465, 627–631 (2010).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Platt, A. et al. The scale of population structure in Arabidopsis thaliana. PLoS Genet. 6, e1000843 (2010).PubMed 
PubMed Central 

Google Scholar 
Lynch, M., Conery, J. & Burger, R. Mutation accumulation and the extinction of small populations. Am. Nat. 146, 489–518 (1995).
Google Scholar 
Willis, J. H. The role of genes of large effect on inbreeding depression in Mimulus guttatus. Evolution 53, 1678–1691 (1999).CAS 
PubMed 

Google Scholar 
Coron, C., Méléard, S., Porcher, E. & Robert, A. Quantifying the mutational meltdown in diploid populations. Am. Nat. 181, 623–636 (2013).PubMed 

Google Scholar 
Kyriazis, C. C., Wayne, R. K. & Lohmueller, K. E. Strongly deleterious mutations are a primary determinant of extinction risk due to inbreeding depression. Evol. Lett. https://doi.org/10.1002/evl3.209 (2020).Barrett, S. C. H. & Charlesworth, D. Effects of a change in the level of inbreeding on the genetic load. Nature 352, 522–524 (1991).ADS 
CAS 
PubMed 

Google Scholar 
Hedrick, P. W. & Garcia-Dorado, A. Understanding inbreeding depression, purging, and genetic rescue. Trends Ecol. Evol. 31, 940–952 (2016).PubMed 

Google Scholar 
Robinson, J. A., Brown, C., Kim, B. Y., Lohmueller, K. E. & Wayne, R. K. Purging of strongly deleterious mutations explains long-term persistence and absence of inbreeding depression in island foxes. Curr. Biol. 28, 3487–3494.e4 (2018).CAS 
PubMed 
PubMed Central 

Google Scholar 
Khan, A. et al. Genomic evidence for inbreeding depression and purging of deleterious genetic variation in Indian tigers. Proc. Natl. Acad. Sci. USA 118, e2023018118 (2021).Byers, D. L. & Waller, D. M. Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annu. Rev. Ecol. Syst. 30, 479–513 (1999).
Google Scholar 
Goodwillie, C., Kalisz, S. & Eckert, C. G. The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annu. Rev. Ecol. Evol. Syst. 36, 47–79 (2005).
Google Scholar 
Hill, W. G. & Robertson, A. The effect of linkage on limits to artificial selection. Genet. Res. 8, 269–294 (1966).CAS 
PubMed 

Google Scholar 
Covert, A. W. III, Lenski, R. E., Wilke, C. O. & Ofria, C. Experiments on the role of deleterious mutations as stepping stones in adaptive evolution. Proc. Natl Acad. Sci. USA 110, E3171–E3178 (2013).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Castellano, D., Coronado-Zamora, M., Campos, J. L., Barbadilla, A. & Eyre-Walker, A. Adaptive evolution is substantially impeded by hill–robertson interference in Drosophila. Mol. Biol. Evol. 33, 442–455 (2016).CAS 
PubMed 

Google Scholar 
Anderson, J. T., Lee, C.-R., Rushworth, C. A., Colautti, R. I. & Mitchell-Olds, T. Genetic trade-offs and conditional neutrality contribute to local adaptation. Mol. Ecol. 22, 699–708 (2013).PubMed 

Google Scholar 
Hämälä, T. & Savolainen, O. Genomic patterns of local adaptation under gene flow in arabidopsis lyrata. Mol. Biol. Evol. 36, 2557–2571 (2019).
Google Scholar 
Taylor, M. A. et al. Large-effect flowering time mutations reveal conditionally adaptive paths through fitness landscapes in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 116, 17890–17899 (2019).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Storz, J. F. Causes of molecular convergence and parallelism in protein evolution. Nat. Rev. Genet. 17, 239–250 (2016).CAS 
PubMed 
PubMed Central 

Google Scholar 
Mimura, M. & Aitken, S. N. Local adaptation at the range peripheries of Sitka spruce. J. Evol. Biol. 23, 249–258 (2010).CAS 
PubMed 

Google Scholar 
Stanton-Geddes, J., Tiffin, P. & Shaw, R. G. Role of climate and competitors in limiting fitness across range edges of an annual plant. Ecology 93, 1604–1613 (2012).PubMed 

Google Scholar 
Vergeer, P. & Kunin, W. E. Adaptation at range margins: common garden trials and the performance of Arabidopsis lyrata across its northwestern European range. N. Phytol. 197, 989–1001 (2013).
Google Scholar 
Volis, S., Ormanbekova, D. & Shulgina, I. Role of selection and gene flow in population differentiation at the edge vs. interior of the species range differing in climatic conditions. Mol. Ecol. 25, 1449–1464 (2016).CAS 
PubMed 

Google Scholar 
Glémin, S., Bazin, E. & Charlesworth, D. Impact of mating systems on patterns of sequence polymorphism in flowering plants. Proc. R. Soc. B Biol. Sci. 273, 3011–3019 (2006).
Google Scholar 
Almeida‐Rocha, J. M., Soares, L. A. S. S., Andrade, E. R., Gaiotto, F. A. & Cazetta, E. The impact of anthropogenic disturbances on the genetic diversity of terrestrial species: A global meta‐analysis. Mol. Ecol. 29, 4812–4822 (2020).PubMed 

Google Scholar 
Schrader, L. et al. Transposable element islands facilitate adaptation to novel environments in an invasive species. Nat. Commun. 5, 5495 (2014).ADS 
CAS 
PubMed 

Google Scholar 
Lu, L. et al. Tracking the genome-wide outcomes of a transposable element burst over decades of amplification. Proc. Natl Acad. Sci. USA 114, E10550–E10559 (2017).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Schrader, L. & Schmitz, J. The impact of transposable elements in adaptive evolution. Mol. Ecol. 28, 1537–1549 (2019).PubMed 

Google Scholar 
Habig, M., Lorrain, C., Feurtey, A., Komluski, J. & Stukenbrock, E. H. Epigenetic modifications affect the rate of spontaneous mutations in a pathogenic fungus. Nat. Commun. 12, 1–13 (2021).
Google Scholar 
Wicker, T. et al. DNA transposon activity is associated with increased mutation rates in genes of rice and other grasses. Nat. Commun. 7, 1–9 (2016).
Google Scholar 
Dubin, M. J., Mittelsten Scheid, O. & Becker, C. Transposons: a blessing curse. Curr. Opin. Plant Biol. 42, 23–29 (2018).CAS 
PubMed 

Google Scholar 
Stapley, J., Santure, A. W. & Dennis, S. R. Transposable elements as agents of rapid adaptation may explain the genetic paradox of invasive species. Mol. Ecol. 24, 2241–2252 (2015).CAS 
PubMed 

Google Scholar 
Sultana, T., Zamborlini, A., Cristofari, G. & Lesage, P. Integration site selection by retroviruses and transposable elements in eukaryotes. Nat. Rev. Genet. 18, 292–308 (2017).CAS 
PubMed 

Google Scholar 
Baduel, P. et al. Genetic and environmental modulation of transposition shapes the evolutionary potential of Arabidopsis thaliana. Genome Biol. 22, 1–26 (2021).
Google Scholar 
Quesneville, H. Twenty years of transposable element analysis in the Arabidopsis thaliana genome. Mob. DNA 11, 28 (2020).PubMed 
PubMed Central 

Google Scholar 
Ossowski, S. et al. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327, 92–94 (2010).ADS 
CAS 
PubMed 

Google Scholar 
Coulondre, C., Miller, J. H., Farabaugh, P. J. & Gilbert, W. Molecular basis of base substitution hotspots in Escherichia coli. Nature 274, 775–780 (1978).ADS 
CAS 
PubMed 

Google Scholar 
Duncan, B. K. & Miller, J. H. Mutagenic deamination of cytosine residues in DNA. Nature 287, 560–561 (1980).ADS 
CAS 
PubMed 

Google Scholar 
Linquist, S. et al. Distinguishing ecological from evolutionary approaches to transposable elements. Biol. Rev. 88, 573–584 (2013).PubMed 

Google Scholar 
Dupeyron, M., Singh, K. S., Bass, C. & Hayward, A. Evolution of Mutator transposable elements across eukaryotic diversity. Mob. DNA 10, 1–14 (2019).
Google Scholar 
Batstone, R. T. Genomes within genomes: nested symbiosis and its implications for plant evolution. New Phytol. https://doi.org/10.1111/nph.17847 (2021).Pietzenuk, B. et al. Recurrent evolution of heat-responsiveness in Brassicaceae COPIA elements. Genome Biol. 17, 209 (2016).PubMed 
PubMed Central 

Google Scholar 
Horváth, V., Merenciano, M. & González, J. Revisiting the relationship between transposable elements and the eukaryotic stress response. Trends Genet. 33, 832–841 (2017).PubMed 

Google Scholar 
Liu, S. et al. Role of H1 and DNA methylation in selective regulation of transposable elements during heat stress. N. Phytol. 229, 2238–2250 (2021).CAS 

Google Scholar 
Mao, H. et al. A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat. Commun. 6, 1–13 (2015).ADS 
CAS 

Google Scholar 
Castelletti, S., Tuberosa, R., Pindo, M. & Salvi, S. A MITE transposon insertion is associated with differential methylation at the maize flowering time QTL vgt1. G3 Genes, Genomes, Genet. 4, 805–812 (2014).CAS 

Google Scholar 
Legrand, S. et al. Differential retention of transposable element-derived sequences in outcrossing Arabidopsis genomes. Mob. DNA 10, 30 (2019).PubMed 
PubMed Central 

Google Scholar 
Quadrana, L. et al. Transposition favors the generation of large effect mutations that may facilitate rapid adaption. Nat. Commun. 10, 1–10 (2019).CAS 

Google Scholar 
Teschendorf, A. E. & Relton, C. L. Statistical and integrative system-level analysis of DNA methylation data. Nat. Rev. Genet. 19, 129–147 (2019).
Google Scholar 
Bonchev, G. & Willi, Y. Accumulation of transposable elements in selfing populations of Arabidopsis lyrata supports the ectopic recombination model of transposon evolution. N. Phytol. 219, 767–778 (2018).CAS 

Google Scholar 
Lockton, S., Ross-Ibarra, J. & Gaut, B. S. Demography and weak selection drive patterns of transposable element diversity in natural populations of Arabidopsis lyrata. Proc. Natl Acad. Sci. USA 105, 13965–13970 (2008).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Lockton, S. & Gaut, B. S. The evolution of transposable elements in natural populations of self-fertilizing Arabidopsis thaliana and its outcrossing relative Arabidopsis lyrata. BMC Evol. Biol. 10, 10 (2010).PubMed 
PubMed Central 

Google Scholar 
Mable, B. K., Dart, A. V. R., Berardo, C., Di & Witham, L. Breakdown of self-incompatibility in the perennial Arabidopsis lyrata (Brassicaceae) and its genetic consequences. Evolution 59, 1437–1448 (2005).PubMed 

Google Scholar 
Foxe, J. P. et al. Reconstructing origins of loss of self-incompatibility and selfing in North American Arabidopsis lyrata: a population genetic context. Evolution 64, 3495–3510 (2010).PubMed 

Google Scholar 
Quadrana, L. et al. The Arabidopsis thaliana mobilome and its impact at the species level. Elife 5, e15716 (2016).Stuart, T. et al. Population scale mapping of transposable element diversity reveals links to gene regulation and epigenomic variation. Elife 5, e20777 (2016).Willi, Y. Mutational meltdown in selfing Arabidopsis lyrata. Evolution 67, 806–815 (2013).PubMed 

Google Scholar 
Joschinski, J., van Kleunen, M. & Stift, M. Costs associated with the evolution of selfing in North American populations of Arabidopsis lyrata? Evol. Ecol. 29, 749–764 (2015).
Google Scholar 
Koonin, E. V. & Krupovic, M. Evolution of adaptive immunity from transposable elements combined with innate immune systems. Nat. Rev. Genet. 16, 184–192 (2015).CAS 
PubMed 

Google Scholar 
Li, Z.-W. et al. Transposable elements contribute to the adaptation of Arabidopsis thaliana. Genome Biol. Evol. 10, 2140–2150 (2018).CAS 
PubMed 
PubMed Central 

Google Scholar 
Catlin, N. S. & Josephs, E. B. The important contribution of transposable elements to phenotypic variation and evolution. Curr. Opin. Plant Biol. 65, 102140 (2022).CAS 
PubMed 

Google Scholar 
Casacuberta, E. & González, J. The impact of transposable elements in environmental adaptation. Mol. Ecol. 22, 1503–1517 (2013).CAS 
PubMed 

Google Scholar 
Baduel, P., Quadrana, L., Hunter, B., Bomblies, K. & Colot, V. Relaxed purifying selection in autopolyploids drives transposable element over-accumulation which provides variants for local adaptation. Nat. Commun. 10, 1–10 (2019).
Google Scholar 
Wos, G., Choudhury, R. R., Kolář, F. & Parisod, C. Transcriptional activity of transposable elements along an elevational gradient in Arabidopsis arenosa. Mob. DNA 12, 7 (2021).CAS 
PubMed 
PubMed Central 

Google Scholar 
Stebbins, G. L. Self fertilization and population variability in the higher plants. Am. Nat. 91, 337–354 (1957).
Google Scholar 
Takebayashi, N. & Morrell, P. L. Is self-fertilization an evolutionary dead end? Revisiting an old hypothesis with genetic theories and a macroevolutionary approach. Am. J. Bot. 88, 1143–1150 (2001).CAS 
PubMed 

Google Scholar 
Igic, B. & Busch, J. W. Is self‐fertilization an evolutionary dead end? N. Phytol. 198, 386–397 (2013).
Google Scholar 
Goldberg, E. E. et al. Species selection maintains self-incompatibility. Science 330, 493–495 (2010).ADS 
CAS 
PubMed 

Google Scholar 
Abu Awad, D. & Billiard, S. The double edged sword: The demographic consequences of the evolution of self-fertilization. Evolution 71, 1178–1190 (2017).PubMed 

Google Scholar 
Fijarczyk, A. & Babik, W. Detecting balancing selection in genomes: limits and prospects. Mol. Ecol. 24, 3529–3545 (2015).CAS 
PubMed 

Google Scholar 
Wu, Q. et al. Long-term balancing selection contributes to adaptation in Arabidopsis and its relatives. Genome Biol. 18, 1–15 (2017).CAS 

Google Scholar 
Kerwin, R. et al. Natural genetic variation in Arabidopsis thaliana defense metabolism genes modulates field fitness. Elife 2015, 1–28 (2015).
Google Scholar 
Waller, D. M. Addressing Darwin’s dilemma: can pseudo-overdominance explain persistent inbreeding depression and load? Evolution 75, 779–793 (2021).CAS 
PubMed 

Google Scholar 
Gilbert, K. J., Pouyet, F., Excoffier, L. & Peischl, S. Transition from background selection to associative overdominance promotes diversity in regions of low recombination. Curr. Biol. 30, 101–107.e3 (2020).CAS 
PubMed 

Google Scholar 
Buckley, J. et al. R-gene variation across Arabidopsis lyrata subspecies: effects of population structure, selection and mating system. BMC Evol. Biol. 16, 93 (2016).PubMed 
PubMed Central 

Google Scholar 
Schmickl, R., Jørgensen, M. H., Brysting, A. K. & Koch, M. A. Phylogeographic implications for the north american boreal-arctic Arabidopsis lyrata complex. Plant Ecol. Divers. 1, 245–254 (2008).
Google Scholar 
Buckley, J., Holub, E. B., Koch, M. A., Vergeer, P. & Mable, B. K. Restriction associated DNA-genotyping at multiple spatial scales in Arabidopsis lyrata reveals signatures of pathogen-mediated selection. BMC Genomics 19, 1–21 (2018).
Google Scholar 
Flutre, T., Duprat, E., Feuillet, C. & Quesneville, H. Considering transposable element diversification in de novo annotation approaches. PLoS ONE 6, e16526 (2011).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Luu, K., Bazin, E. & Blum, M. G. B. pcadapt: an R package to perform genome scans for selection based on principal component analysis. in. Mol. Ecol. Resour. 17, 67–77 (2017).CAS 
PubMed 

Google Scholar 
Privé, F., Luu, K., Vilhjálmsson, B. J. & Blum, M. G. B. Performing highly efficient genome scans for local adaptation with R Package pcadapt Version 4. Mol. Biol. Evol. 37, 2153–2154 (2020).PubMed 

Google Scholar 
Foll, M. & Gaggiotti, O. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180, 977–993 (2008).PubMed 
PubMed Central 

Google Scholar 
Charlesworth, J. & Eyre-Walker, A. The McDonald-Kreitman test and slightly deleterious mutations. Mol. Biol. Evol. 25, 1007–1015 (2008).CAS 
PubMed 

Google Scholar 
Hernandez, R. D. et al. Ultrarare variants drive substantial cis heritability of human gene expression. Nat. Genet. 51, 1349–1355 (2019).CAS 
PubMed 
PubMed Central 

Google Scholar 
Williamson, R. J. et al. Evidence for widespread positive and negative selection in coding and conserved noncoding regions of capsella grandiflora. PLoS Genet. 10, e1004622 (2014).PubMed 
PubMed Central 

Google Scholar 
Brooks, M. E. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R. J. 9, 378–400 (2017).
Google Scholar 
Mattila, T. M., Tyrmi, J., Pyhäjärvi, T. & Savolainen, O. Genome-wide analysis of colonization history and concomitant selection in Arabidopsis lyrata. Mol. Biol. Evol. 34, 2665–2677 (2017).CAS 
PubMed 

Google Scholar  More

The Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) last month released its annual report on elephant poaching. It reveals a downward trend across African range states, based on data from its Monitoring the Illegal Killing of Elephants programme. The decline correlates with reduced ivory trading over the period, particularly in the Chinese market.
Competing Interests
The author declares no competing interests. More

Bacterial density and growth potential in the rearing water were related to the microbial carrying capacityQuantifying the bacterial density in each tank verified that we obtained a higher bacterial load in the systems with added organic material. The bacterial density was, on average, 7.8× higher in the systems with high compared to low bacterial carrying capacity. This difference was particularly evident at 2 (34.8×, Kruskal–Wallis p = 0.0008) and 9 DPH (9.1×, Kruskal–Wallis p = 0.0007) (Fig. 1). The bacterial density increased throughout the experiment for the tanks with low microbial carrying capacity (treatment group MMS−, FTS−), reflecting increased larval feeding and defecation. Contrastingly, the bacterial density was relatively stable over time in the MMS+ treatment and even decreased over time in the FTS+ treatment. When averaging the densities at 11 and 15 DPH within each rearing treatment, we observed that the ‘MMS+ to FTS+’ had a considerable difference in the bacterial density between incoming and rearing water (24.2×). In contrast, this difference was below 8.2× in all other treatment tanks. Such differences in density indicated that some communities were below the microbial carrying capacity of the systems. We thus investigated the growth potential to determine if carrying capacity was reached in the rearing water.Figure 1Bacterial density (million bacterial cells mL−1) at various days post-hatching (DPH) in incoming and rearing tank water. Note that the y-axis is log scaled. Colours indicate the rearing treatment, and shape signifies rearing (filled circle) and incoming water (filled triangle).Full size imageThe bacterial net growth potential in the intake and rearing water was quantified as the number of cell doublings after incubation for 3 days11. Generally, the FTS− and MMS− rearing water had net growth potential with an average of 0.2 and 0.1, respectively (Supplementary Fig. 2). In contrast, the rearing water of the FTS+ and MMS+ had a negative net growth potential with averages of −0.2 and −0.06, respectively. In the case of negative net growth potential, the bacterial density decreased during the incubation. A negative net growth potential suggested that the rearing water bacterial communities were at the tank’s microbial carrying capacity at the time of sampling. Thus, the bacterial communities were at the carrying capacity of the high (+) carrying capacity systems and below in the low (−) systems. To gain a deeper understanding of the bacterial community characteristics the 16S rRNA gene of the bacterial community was sequenced at 1 and 9 DPH.Initial rearing condition did not leave a legacy effect on bacterial α-diversityThe bacterial α-diversity of the rearing water was investigated at 1 and 12 DPH (Fig. 2). At 1 DPH, the richness was comparable between the FTS−, FTS+ and MMS+ treatments, but on average, 1.5× higher for the MMS− treatment (307 vs 205 ASVs, Tukey’s test p  More

Barbier, E. B. Marine ecosystem services. Curr. Biol. 27, R507–R510 (2017).CAS 
PubMed 

Google Scholar 
Liquete, C., Piroddi, C., Macías, D., Druon, J.-N. & Zulian, G. Ecosystem services sustainability in the Mediterranean Sea: Assessment of status and trends using multiple modelling approaches. Sci. Rep. 6, 34162 (2016).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Halpern, B. S. et al. Recent pace of change in human impact on the world’s ocean. Sci. Rep. 9, 1–8 (2019).CAS 

Google Scholar 
Duarte, C. M. et al. Rebuilding marine life. Nature 580, 39–51 (2020).ADS 
CAS 
PubMed 

Google Scholar 
Long, R. D., Charles, A. & Stephenson, R. L. Key principles of marine ecosystem-based management. Mar. Policy 57, 53–60 (2015).
Google Scholar 
Link, J. S. & Browman, H. I. Operationalizing and implementing ecosystem-based management. ICES J. Mar. Sci. 74, 379–381 (2017).
Google Scholar 
EC. A Farm to Fork Strategy for a Fair, Healthy and Environmentally-Friendly Food System. Brussels: European Commission. (2020).EC. Communication from the Commission to the European Parliament, the Council, the European Economic and Social Committee and the Committee of the Regions, “Pathway to a healthy planet for all” with the sub-title “EU action Plan: ’Towards zero pollution for air, water and soil, COM (2021) 400. (2021).EC. The European Green Deal. Communication from the Commission to the European Parliament, the European Council, the European Economic and Social Committee and the Committee of the Regions, COM (2019) 640. (2019).Alexander, K. & Haward, M. The human side of marine ecosystem-based management (EBM): ‘Sectoral interplay’ as a challenge to implementing EBM. Mar. Policy 101, 33–38 (2019).
Google Scholar 
EC. The EU Blue Economy Report 2021. (2021).Ostlaender, N. et al. Modelling Inventory and Knowledge Man-agement System of the European Commission (MIDAS) (Publications Office of the European Union, 2019).
Google Scholar 
Friedland, R. et al. Effects of nutrient management scenarios on marine eutrophication indicators: A Pan-European, multi-model assessment in support of the Marine Strategy Framework Directive. Front. Mar. Sci. 8, 596126 (2021).
Google Scholar 
Piroddi, C. et al. Effects of nutrient management scenarios on marine food webs: A Pan-European Assessment in support of the Marine Strategy Framework Directive. Front. Mar. Sci. 8, 179 (2021).
Google Scholar 
Corrales, X. et al. Multi-zone marine protected areas: Assessment of ecosystem and fisheries benefits using multiple ecosystem models. Ocean Coast. Manag. 193, 105232 (2020).
Google Scholar 
Bentley, J. W. et al. Refining fisheries advice with stock-specific ecosystem information. Front. Mar. Sci. 8, 602072 (2021).
Google Scholar 
Steenbeek, J. et al. Making spatial-temporal marine ecosystem modelling better—A perspective. Environ. Model. Softw. 145, 105209 (2021).PubMed 
PubMed Central 

Google Scholar 
Heymans, J. J. et al. The ocean decade: A true ecosystem modelling challenge. Front. Mar. Sci. 7, 554573 (2020).
Google Scholar 
Hernvann, P.-Y. et al. The Celtic sea through time and space: Ecosystem modeling to unravel fishing and climate change impacts on food-web structure and dynamics. Front. Mar. Sci. 7, 1018 (2020).
Google Scholar 
Christensen, V. & Walters, C. J. Ecopath with Ecosim: Methods, capabilities and limitations. Ecol. Model. 172, 109–139 (2004).
Google Scholar 
Steenbeek, J. et al. Bridging the gap between ecosystem modeling tools and geographic information systems: Driving a food web model with external spatial–temporal data. Ecol. Model. 263, 139–151 (2013).
Google Scholar 
Christensen, V. et al. Representing variable habitat quality in a spatial food web model. Ecosystems 17, 1397–1412 (2014).CAS 

Google Scholar 
de Mutsert, K., Lewis, K., Milroy, S., Buszowski, J. & Steenbeek, J. Using ecosystem modeling to evaluate trade-offs in coastal management: Effects of large-scale river diversions on fish and fisheries. Ecol. Model. 360, 14–26 (2017).
Google Scholar 
Serpetti, N. et al. Modelling small scale impacts of Multi-Purpose Platforms: An ecosystem approach. Front. Mar. Sci. 8, 778 (2021).
Google Scholar 
DFO. Technical review of Roberts Bank Terminal 2 environmental assessment: section 10.3—assessing ecosystem productivity. DFO Can. Sci. Advis. Sec. Sci. Resp. 2016/050 (2016).Coll, M., Pennino, M. G., Steenbeek, J., Solé, J. & Bellido, J. M. Predicting marine species distributions: Complementarity of food-web and Bayesian hierarchical modelling approaches. Ecol. Model. 405, 86–101 (2019).
Google Scholar 
Coll, M. et al. The biodiversity of the Mediterranean Sea: Estimates, patterns, and threats. PLoS One 5, e11842 (2010).ADS 
PubMed 
PubMed Central 

Google Scholar 
Coll, M. et al. The Mediterranean Sea under siege: Spatial overlap between marine biodiversity, cumulative threats and marine reserves. Glob. Ecol. Biogeogr. 21, 465–480 (2012).
Google Scholar 
Micheli, F. et al. Cumulative human impacts on mediterranean and black sea marine ecosystems: Assessing current pressures and opportunities. PLoS One 8, e79889 (2013).ADS 
PubMed 
PubMed Central 

Google Scholar 
Piroddi, C., Colloca, F. & Tsikliras, A. C. The living marine resources in the Mediterranean Sea large marine ecosystem. Environ. Dev. 36, 100555 (2020).PubMed 
PubMed Central 

Google Scholar 
Barale, V. & Gade, M. Remote Sensing of the European Seas. (Springer, 2008).Siokou-Frangou, I. et al. Plankton in the open Mediterranean Sea: A review. Biogeosciences 7, 1543–1586 (2010).ADS 

Google Scholar 
Spalding, M. D. et al. Marine ecoregions of the world: A bioregionalization of coastal and shelf areas. Bioscience 57, 573–583 (2007).
Google Scholar 
Bianchi, C. N. et al. In Life in the Mediterranean Sea: A Look at Habitat Changes, vol. 1 55 (2012).Danovaro, R. et al. Deep-sea biodiversity in the Mediterranean Sea: The known, the unknown, and the unknowable. PLoS One 5, e11832 (2010).ADS 
PubMed 
PubMed Central 

Google Scholar 
Moullec, F. et al. Capturing the big picture of Mediterranean marine biodiversity with an end-to-end model of climate and fishing impacts. Prog. Oceanogr. 178, 102179 (2019).
Google Scholar 
Macias, D., Garcia-Gorriz, E., Piroddi, C. & Stips, A. Biogeochemical control of marine productivity in the Mediterranean Sea during the last 50 years. Glob. Biogeochem. Cycles 28, 897–907 (2014).ADS 
CAS 

Google Scholar 
Piroddi, C. et al. Historical changes of the Mediterranean Sea ecosystem: Modelling the role and impact of primary productivity and fisheries changes over time. Sci. Rep. 7, 44491 (2017).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Lotze, H. K. et al. Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312, 1806–1809 (2006).ADS 
CAS 
PubMed 

Google Scholar 
Lotze, H. K., Coll, M. & Dunne, J. A. Historical changes in marine resources, food-web structure and ecosystem functioning in the Adriatic Sea, Mediterranean. Ecosystems 14, 198–222 (2011).
Google Scholar 
Macias, D., Huertas, I. E., Garcia-Gorriz, E. & Stips, A. Non-Redfieldian dynamics driven by phytoplankton phosphate frugality explain nutrient and chlorophyll patterns in model simulations for the Mediterranean Sea. Prog. Oceanogr. 173, 37–50 (2019).ADS 
PubMed 
PubMed Central 

Google Scholar 
Spedicato, M. T. et al. The MEDITS trawl survey specifications in an ecosystem approach to fishery management. Sci. Mar. 83, 9–20 (2019).
Google Scholar 
Corrales, X. et al. Hindcasting the dynamics of an Eastern Mediterranean marine ecosystem under the impacts of multiple stressors. Mar. Ecol. Prog. Ser. 580, 17–36 (2017).ADS 

Google Scholar 
FAO. The State of the Mediterranean and Black Sea fisheries (General Fisheries Commission for the Mediterranean (GFCM), 2020).Ferrà, C. et al. Mapping change in bottom trawling activity in the Mediterranean Sea through AIS data. Mar. Policy 94, 275–281 (2018).
Google Scholar 
Russo, T. et al. Trends in effort and yield of trawl fisheries: A case study from the Mediterranean Sea. Front. Mar. Sci. 6, 153 (2019).ADS 

Google Scholar 
Ramírez, F., Coll, M., Navarro, J., Bustamante, J. & Green, A. J. Spatial congruence between multiple stressors in the Mediterranean Sea may reduce its resilience to climate impacts. Sci. Rep. 8, 1–8 (2018).
Google Scholar 
Coll, M., Steenbeek, J., Ben Rais Lasram, F., Mouillot, D. & Cury, P. ‘Low-hanging fruit’ for conservation of marine vertebrate species at risk in the Mediterranean Sea. Glob. Ecol. Biogeogr. 24, 226–239 (2015).
Google Scholar 
Ruiz, J. et al. “Strengthening regional cooperation in the area of large pelagic fishery data collection (RECOLAPE)”, Annex III “Biological data collection for fisheries on highly migratory species” (2019).Boerder, K., Schiller, L. & Worm, B. Not all who wander are lost: Improving spatial protection for large pelagic fishes. Mar. Policy 105, 80–90 (2019).
Google Scholar 
Giakoumi, S. et al. Conserving European biodiversity across realms. Conserv. Lett. 12, e12586 (2019).
Google Scholar 
Gascuel, D. & Cheung, W. W. In Predicting Future Oceans 79–85 (Elsevier, 2019).Macias, D., Garcia-Gorriz, E. & Stips, A. Major fertilization sources and mechanisms for Mediterranean Sea coastal ecosystems. Limnol. Oceanogr. 63, 897–914 (2018).ADS 
CAS 

Google Scholar 
Alvarez-Berastegui, D., Tugores, M., Ottmann, D., Martín-Quetglas, M. & Reglero, P. Bluefin tuna larval indices in the Western Mediterranean, ecological and analytical sources of uncertainty. Collect. Vol. Sci. Pap. ICCAT. 77, 289–311 (2020).
Google Scholar 
ICCAT. 2020 SCRS Advice to the Commission (Madrid, Spain, 2020).Clavel-Henry, M., Piroddi, C., Quattrocchi, F., Macias, D. & Christensen, V. Spatial distribution and abundance of mesopelagic fish biomass in the Mediterranean Sea. Front. Mar. Sci. 7, 1136 (2020).
Google Scholar 
García-Ruiz, C. et al. Spatio-temporal patterns of macrourid fish species in the northern Mediterranean Sea. Sci. Mar. 83, 117–127 (2019).
Google Scholar 
Ainsworth, C. Quantifying species abundance trends in the Northern Gulf of California using local ecological knowledge. Mar. Coast. Fish. 3, 190–218 (2011).
Google Scholar 
Morris, E. K. et al. Choosing and using diversity indices: Insights for ecological applications from the German Biodiversity Exploratories. Ecol. Evol. 4, 3514–3524 (2014).PubMed 
PubMed Central 

Google Scholar 
Coll, M. et al. Ecological indicators to capture the effects of fishing on biodiversity and conservation status of marine ecosystems. Ecol. Ind. 60, 947–962 (2016).
Google Scholar 
Swartz, W., Sala, E., Tracey, S., Watson, R. & Pauly, D. The spatial expansion and ecological footprint of fisheries (1950 to present). PLoS One 5, e15143 (2010).ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Damasio, L. M., Peninno, M. G. & Lopes, P. F. Small changes, big impacts: Geographic expansion in small-scale fisheries. Fish. Res. 226, 105533 (2020).
Google Scholar 
Coll, M. et al. Assessing fishing and marine biodiversity changes using fishers’ perceptions: The Spanish Mediterranean and Gulf of Cadiz case study. PLoS One 9, e85670 (2014).ADS 
PubMed 
PubMed Central 

Google Scholar 
Tsikliras, A. C., Dinouli, A., Tsiros, V.-Z. & Tsalkou, E. The Mediterranean and Black Sea fisheries at risk from overexploitation. PLoS ONE 10, e0121188 (2015).PubMed 
PubMed Central 

Google Scholar 
Pittman, S. et al. Seascape ecology: Identifying research priorities for an emerging ocean sustainability science. Mar. Ecol. Prog. Ser. 663, 1–29 (2021).ADS 

Google Scholar 
Kritzer, J. P. & Liu, O. R. In Stock Identification Methods 29–57 (Elsevier, 2014).Piroddi, C., Heymans, J. J., Macias, D., Gregoire, M. & Townsend, H. Editorial: Using ecological models to support and shape environmental policy decisions. Front. Mar. Sci. https://doi.org/10.3389/fmars.2021.815313 (2021).
Google Scholar 
Macias, D. et al. JRC marine modelling framework in support of the marine strategy framework directive: Inventory of models, basin configurations and datasets. Update 2018. (2018).Piante, C. & Ody, D. Blue Growth in the Mediterranean Sea: The Challenge of Good Environmental Status. 192 (France, 2015).Borja, A. et al. Past and future grand challenges in marine ecosystem ecology. Front. Mar. Sci. 7, 362 (2020).
Google Scholar 
Claudet, J., Loiseau, C., Sostres, M. & Zupan, M. Underprotected marine protected areas in a global biodiversity hotspot. One Earth 2, 380–384 (2020).ADS 

Google Scholar 
Piroddi, C., Coll, M., Steenbeek, J., Moy, D. M. & Christensen, V. Modelling the Mediterranean marine ecosystem as a whole: Addressing the challenge of complexity. Mar. Ecol. Prog. Ser. 533, 47–65 (2015).ADS 

Google Scholar 
Walters, C., Pauly, D. & Christensen, V. Ecospace: Prediction of mesoscale spatial patterns in trophic relationships of exploited ecosystems, with emphasis on the impacts of marine protected areas. Ecosystems 2, 539–554 (1999).
Google Scholar 
Christensen, V., Walters, C., Pauly, D. & Forrest, R. Ecopath with Ecosim 6: A User’s Guide (University of British Columbia, 2008).
Google Scholar 
Kaschner, K. et al. AquaMaps: Predicted range maps for aquatic species. In World Wide Web Electronic Publication, www.aquamaps.org, Version, vol. 8, 2016 (2016).De Mutsert, K., Lewis, K. A., White, E. D. & Buszowski, J. End-to-End modeling reveals species-specific effects of large-scale coastal restoration on living resources facing climate change. Front. Mar. Sci. 8, 104 (2021).
Google Scholar 
Coll, M. et al. Advancing global ecological modeling capabilities to simulate future trajectories of change in marine ecosystems. Front. Mar. Sci. 741, 567877 (2020).
Google Scholar 
Shannon, C. & Weaver, W. (Univ. Illinois Press, 1949).Ainsworth, C. H. & Pitcher, T. J. Modifying Kempton’s species diversity index for use with ecosystem simulation models. Ecol. Ind. 6, 623–630 (2006).
Google Scholar 
Coll, M. & Steenbeek, J. Standardized ecological indicators to assess aquatic food webs: The ECOIND software plug-in for Ecopath with Ecosim models. Environ. Model. Softw. 89, 120–130 (2017).
Google Scholar 
Taconet, M., Kroodsma, D. & Fernandes, J. Global Atlas of AIS-Based Fishing Activity—Challenges and Opportunities (2021). More

.readcube-buybox { display: none !important;}
Protecting an overfished lobster species helps the crustaceans to grow big, according to an analysis of European lobsters in marine sanctuaries1.

Access options

/* style specs start */
style{display:none!important}.LiveAreaSection-193358632 *{align-content:stretch;align-items:stretch;align-self:auto;animation-delay:0s;animation-direction:normal;animation-duration:0s;animation-fill-mode:none;animation-iteration-count:1;animation-name:none;animation-play-state:running;animation-timing-function:ease;azimuth:center;backface-visibility:visible;background-attachment:scroll;background-blend-mode:normal;background-clip:borderBox;background-color:transparent;background-image:none;background-origin:paddingBox;background-position:0 0;background-repeat:repeat;background-size:auto auto;block-size:auto;border-block-end-color:currentcolor;border-block-end-style:none;border-block-end-width:medium;border-block-start-color:currentcolor;border-block-start-style:none;border-block-start-width:medium;border-bottom-color:currentcolor;border-bottom-left-radius:0;border-bottom-right-radius:0;border-bottom-style:none;border-bottom-width:medium;border-collapse:separate;border-image-outset:0s;border-image-repeat:stretch;border-image-slice:100%;border-image-source:none;border-image-width:1;border-inline-end-color:currentcolor;border-inline-end-style:none;border-inline-end-width:medium;border-inline-start-color:currentcolor;border-inline-start-style:none;border-inline-start-width:medium;border-left-color:currentcolor;border-left-style:none;border-left-width:medium;border-right-color:currentcolor;border-right-style:none;border-right-width:medium;border-spacing:0;border-top-color:currentcolor;border-top-left-radius:0;border-top-right-radius:0;border-top-style:none;border-top-width:medium;bottom:auto;box-decoration-break:slice;box-shadow:none;box-sizing:border-box;break-after:auto;break-before:auto;break-inside:auto;caption-side:top;caret-color:auto;clear:none;clip:auto;clip-path:none;color:initial;column-count:auto;column-fill:balance;column-gap:normal;column-rule-color:currentcolor;column-rule-style:none;column-rule-width:medium;column-span:none;column-width:auto;content:normal;counter-increment:none;counter-reset:none;cursor:auto;display:inline;empty-cells:show;filter:none;flex-basis:auto;flex-direction:row;flex-grow:0;flex-shrink:1;flex-wrap:nowrap;float:none;font-family:initial;font-feature-settings:normal;font-kerning:auto;font-language-override:normal;font-size:medium;font-size-adjust:none;font-stretch:normal;font-style:normal;font-synthesis:weight style;font-variant:normal;font-variant-alternates:normal;font-variant-caps:normal;font-variant-east-asian:normal;font-variant-ligatures:normal;font-variant-numeric:normal;font-variant-position:normal;font-weight:400;grid-auto-columns:auto;grid-auto-flow:row;grid-auto-rows:auto;grid-column-end:auto;grid-column-gap:0;grid-column-start:auto;grid-row-end:auto;grid-row-gap:0;grid-row-start:auto;grid-template-areas:none;grid-template-columns:none;grid-template-rows:none;height:auto;hyphens:manual;image-orientation:0deg;image-rendering:auto;image-resolution:1dppx;ime-mode:auto;inline-size:auto;isolation:auto;justify-content:flexStart;left:auto;letter-spacing:normal;line-break:auto;line-height:normal;list-style-image:none;list-style-position:outside;list-style-type:disc;margin-block-end:0;margin-block-start:0;margin-bottom:0;margin-inline-end:0;margin-inline-start:0;margin-left:0;margin-right:0;margin-top:0;mask-clip:borderBox;mask-composite:add;mask-image:none;mask-mode:matchSource;mask-origin:borderBox;mask-position:0 0;mask-repeat:repeat;mask-size:auto;mask-type:luminance;max-height:none;max-width:none;min-block-size:0;min-height:0;min-inline-size:0;min-width:0;mix-blend-mode:normal;object-fit:fill;object-position:50% 50%;offset-block-end:auto;offset-block-start:auto;offset-inline-end:auto;offset-inline-start:auto;opacity:1;order:0;orphans:2;outline-color:initial;outline-offset:0;outline-style:none;outline-width:medium;overflow:visible;overflow-wrap:normal;overflow-x:visible;overflow-y:visible;padding-block-end:0;padding-block-start:0;padding-bottom:0;padding-inline-end:0;padding-inline-start:0;padding-left:0;padding-right:0;padding-top:0;page-break-after:auto;page-break-before:auto;page-break-inside:auto;perspective:none;perspective-origin:50% 50%;pointer-events:auto;position:static;quotes:initial;resize:none;right:auto;ruby-align:spaceAround;ruby-merge:separate;ruby-position:over;scroll-behavior:auto;scroll-snap-coordinate:none;scroll-snap-destination:0 0;scroll-snap-points-x:none;scroll-snap-points-y:none;scroll-snap-type:none;shape-image-threshold:0;shape-margin:0;shape-outside:none;tab-size:8;table-layout:auto;text-align:initial;text-align-last:auto;text-combine-upright:none;text-decoration-color:currentcolor;text-decoration-line:none;text-decoration-style:solid;text-emphasis-color:currentcolor;text-emphasis-position:over right;text-emphasis-style:none;text-indent:0;text-justify:auto;text-orientation:mixed;text-overflow:clip;text-rendering:auto;text-shadow:none;text-transform:none;text-underline-position:auto;top:auto;touch-action:auto;transform:none;transform-box:borderBox;transform-origin:50% 50%0;transform-style:flat;transition-delay:0s;transition-duration:0s;transition-property:all;transition-timing-function:ease;vertical-align:baseline;visibility:visible;white-space:normal;widows:2;width:auto;will-change:auto;word-break:normal;word-spacing:normal;word-wrap:normal;writing-mode:horizontalTb;z-index:auto;-webkit-appearance:none;-moz-appearance:none;-ms-appearance:none;appearance:none;margin:0}.LiveAreaSection-193358632{width:100%}.LiveAreaSection-193358632 .login-option-buybox{display:block;width:100%;font-size:17px;line-height:30px;color:#222;padding-top:30px;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-access-options{display:block;font-weight:700;font-size:17px;line-height:30px;color:#222;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-login >li:not(:first-child)::before{transform:translateY(-50%);content:””;height:1rem;position:absolute;top:50%;left:0;border-left:2px solid #999}.LiveAreaSection-193358632 .additional-login >li:not(:first-child){padding-left:10px}.LiveAreaSection-193358632 .additional-login >li{display:inline-block;position:relative;vertical-align:middle;padding-right:10px}.BuyBoxSection-683559780{display:flex;flex-wrap:wrap;flex:1;flex-direction:row-reverse;margin:-30px -15px 0}.BuyBoxSection-683559780 .box-inner{width:100%;height:100%}.BuyBoxSection-683559780 .readcube-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:1;flex-basis:255px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .subscribe-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:4;flex-basis:300px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .subscribe-buybox-nature-plus{background-color:#f3f3f3;flex-shrink:1;flex-grow:4;flex-basis:100%;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .title-readcube{display:block;margin:0;margin-right:20%;margin-left:20%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-buybox{display:block;margin:0;margin-right:29%;margin-left:29%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .asia-link{color:#069;cursor:pointer;text-decoration:none;font-size:1.05em;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:1.05em6}.BuyBoxSection-683559780 .access-readcube{display:block;margin:0;margin-right:10%;margin-left:10%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-buybox{display:block;margin:0;margin-right:30%;margin-left:30%;font-size:14px;color:#222;opacity:.8px;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .usps-buybox{display:block;margin:0;margin-right:30%;margin-left:30%;font-size:14px;color:#222;opacity:.8px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .price-buybox{display:block;font-size:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;padding-top:30px;text-align:center}.BuyBoxSection-683559780 .price-from{font-size:14px;padding-right:10px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .issue-buybox{display:block;font-size:13px;text-align:center;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:19px}.BuyBoxSection-683559780 .no-price-buybox{display:block;font-size:13px;line-height:18px;text-align:center;padding-right:10%;padding-left:10%;padding-bottom:20px;padding-top:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif}.BuyBoxSection-683559780 .vat-buybox{display:block;margin-top:5px;margin-right:20%;margin-left:20%;font-size:11px;color:#222;padding-top:10px;padding-bottom:15px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:17px}.BuyBoxSection-683559780 .button-container{display:flex;padding-right:20px;padding-left:20px;justify-content:center}.BuyBoxSection-683559780 .button-container >*{flex:1px}.BuyBoxSection-683559780 .button-container >a:hover,.Button-505204839:hover,.Button-1078489254:hover,.Button-2808614501:hover{text-decoration:none}.BuyBoxSection-683559780 .readcube-button{background:#fff;margin-top:30px}.BuyBoxSection-683559780 .button-asia{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;margin-top:75px}.BuyBoxSection-683559780 .button-label-asia,.ButtonLabel-3869432492,.ButtonLabel-3296148077,.ButtonLabel-1566022830{display:block;color:#fff;font-size:17px;line-height:20px;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;text-align:center;text-decoration:none;cursor:pointer}.Button-505204839,.Button-1078489254,.Button-2808614501{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;max-width:320px;margin-top:10px}.Button-505204839 .readcube-label,.Button-1078489254 .readcube-label,.Button-2808614501 .readcube-label{color:#069}
/* style specs end */Subscribe to Nature+Get immediate online access to Nature and 55 other Nature journal$29.99monthlySubscribe to JournalGet full journal access for 1 year$199.00only $3.90 per issueAll prices are NET prices.VAT will be added later in the checkout.Tax calculation will be finalised during checkout.Buy articleGet time limited or full article access on ReadCube.$32.00All prices are NET prices.

Additional access options:

doi: https://doi.org/10.1038/d41586-022-03708-2

References

Subjects

Conservation biology More

Notwithstanding constraints on the amount of hard data, according to our integrated analysis, the developmental environment and ecology of reef communities have an important impact on the appearance of reefs.Analysis of environmental conditions for reef developmentSettings of reef developmentThe F/F extinction event in Late Devonian caused the complete recession of the reef-building communities based on stromatoporoid-coral assemblages7,17. The Carboniferous is generally considered to be a sub-optimal period for the development of framed reefs. After the biological mass extinction, microorganisms and algae rebuilt new reef-building ecosystems18,19. Some short-term biological frame reefs developed with low diversity, limited reef-building organisms, small sizes, and restricted distribution20. Harsh climate and marine conditions occurred in the Mississippian, including extensive marine hypoxia, repeated glacial and interglacial climate changes, and frequent changes of sea level and seawater surface temperature, potentially hindering the recovery of Early Carboniferous metazoan reefs7,21.Metazoans gradually began to participate in reef building in Early Viséan. A large number of biogenic structures formed by corals and bryozoans began to appear, including a small number of sponge reefs/mounds in the middle and late stage of Viséan. The richness and biodiversity of the Mississippian post-zoobenthic reefs flourished in the late Viséan during which corals, bryozoans, sponges, calcareous microorganisms, and some calcareous algae became the main builders3 and large-scale reefs could also be seen in some areas although most of the Viséan metazoan reefs were tabular or laminar. Thus, the metazoan skeletal reefs in the middle to late Viséan were considered to have been resurrected due to relatively warm climatic conditions and higher sea levels after a period of complete disintegration at the end of the Devonian and recession at the beginning of the Carboniferous7.Consequently, the coral reefs in the study area were the products of shallow benthic communities thriving in relatively favourable conditions of Late Viséan-Serpukhovian, which was common for reef development at that time7. Thus, it is expected that more synchronous reefs would to be identified in southern China, or even in the study area in the future.Paleogeography of reefsLangping is located in Dian-Qian-Gui Basin22 regionally (Fig. 2), in the eastern end of Tethys tectonic domain and at the interjunction of Tethys and Pacific structure globally. The Carboniferous Dian-Qian-Gui Basin is adjacent to the Tethys Basin. During the Early Carboniferous, the continent of Gondwana was close to the equator but was separated from the northern continent by the Tethys, where the tropical currents flowed freely from east to west. The benthic warm-water organisms were distributed widely with high abundance and diversity on both sides of the shallow shelf of Tethys.Figure 2Paleogeographic map of southern China in Viséan-Serpukhovian (modified from Feng23, Yao8, and Maillet24). This figure was obtained from articles by Feng23, Yao8 and Maillet24 respectively. The author modified the picture with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/). QG Qian-Gui Basin, DQGX Dian-Qian-Gui-Xiang platform.Full size imageViséan-Serpukhovian ecosystems experienced dramatic climate changes and widespread glaciation25. However, the Viséan was also a key layer for a variety of biological structures, with abundant coral reefs and a high diversity of shallow benthic communities, peaking in the late Viséan. Newly discovered post-faunal reefs in Tianlin were mainly formed in the late Viséan-Serpukhovian period, which coincided with frequent sea level fluctuations and possible glacial changes. It seems counterintuitive that tropical coral communities developed during glacial period. However, recent studies suggest that the persistent warm ocean currents on the platform helped some coral species survive from Carboniferous glacial events24. While other areas of symbiotic reefs were poorly developed, Tianlin may provide an ecological sanctuary for corals associated with ocean currents26.Sedimentation of reef developmentAccording to the regional geological structure, the slope model for Langping paleocarbonate platform was obviously different from that of steep slope platform margin, which could be directly affected by waves. Langping palaeo-platform could be regarded as one of the small blocks (block fault barrier) separated from a large platform (continental margin sea basin)13. The relative positions of these blocks were crucial for the emergence and growth of reefs.In situ development of mud-crystalline tuffs and muddy tuffs with weak hydrodynamic conditions is common in the Langping area, and evaporites are poorly developed. There were patch reefs and reef layers in different sizes in the wide intraclast beach, where obviously developed reef beach complexes were rare. The fragments of carbonate base broken by storm in the clastic beach haven’t been observed. The study area is considered to be gentle-slope open platform27,28 based on sedimentary characteristics. It suggests that the study area was far away from the margin of steep-slope platform that directly affected by waves, and more consistent with less energetic internal environments of gentle-slope platform.On the vast platform of Langping gentle slop, deep water lead to low water energy. While in the coastal area, the water energy was relatively strong, thus coarse-grained bioclastic beach and a small amount of point reef could be developed. The beaches were irregular-shaped due to long term transportation and reformation effects of waves and water flow, showing low and gentle slope angles. Dispersed reef-beach complexes at the platform margin slightly impacted inner-platform seawater and the water flows smoothly29.Therefore, it can be assumed that Langping reefs developed along the intertidal shallows of the terrace. The seawater around Langping carbonate platform in Late Viséan-Serpukhovian was relatively shallow while the water flow was strong. Remains of crinoids, brachiopods, a few foraminifera, and solitary corals were likely broken by strong currents, and deposited in situ with a small amount of gravels and lime-mud (Fig. 3). The clastic beach was unstable, suggesting large-scale wave-resistant structures could not be formed quickly30 due to insufficient cohesive and consolidating organisms. In addition, the circumferential impact of water in extensive terraces leads to mud-lime deposition, which is detrimental to most benthic organisms. However, bondstone was more likely to be formed by some binding algaes in the platform (Fig. 4). Therefore, neither the surrounding or the inner region of the platform could provide favourable living conditions for coral reefs to develop over for a long term. The gently sloping terrace environment of Lanping resulted in significant differences in growth size, wave resistance and reef-building capacity between corals in the study area and those on the edge of the steeply sloping terrace.Figure 3Clastic beaches in the Langping. Various clastic beaches developed in the study area. Diverse composition, fragmentation degree and sorting of the clast indicate different water conditions of formation. This figure is modified by the author from field photos with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageFigure 4Algal bondstone in the Langping. Bondstone formed by various algaes living in still water. Morphology of bondstone correlates water environment and deposition of mud. Vast algal bondstones indicate deep water and high deposition rate. This figure is modified by the author from field photos with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageAt the same time, the warm climate of the late Viséan-Serpukhovian, the good circulation of seawater around the Langping platform, and the abundant supply of oxygen and nutrients were a series of favourable conditions that facilitated the growth of reef-building corals, which led to uplifts being formed on clastic beach, including patch reefs and reef layers with certain sizes. These uplifts impeded waves and provided a protected nearshore environment, though they were much smaller than those developed at the steep-slope platform margin. The inhabitants on the beach could not resist strong waves. These rises were therefore known as reef-beach complexes and could only persist where waves and currents were mild28. They were essentially different from the framework coral reefs which developed on steep-slope platform margin that reflected changed hydrodynamic conditions, nutrient sources, reef sizes, and growth rates.Another potentially favourable factor in the study area could be the deeper water area in the gentle-slope sedimentary environment, which could provide more stable conditions and reduce the damaging effects of global glacial events and large scale sea level fluctuations on reef-building communities25. The frequent fault activities in Dian-Qian-Gui Basin caused the rise and fall of equivalent sea level. More influence of sea-level fluctuations and hydrodynamic conditions would be exerted on Langping platform due to its small size. Furthermore, reef growth promoted by reef-building communities would be frequently disturbed. The sediments displaying evidence of multicycle sedimentation, different components, and diversely fragile clasts in the study area provided direct evidence of frequently changing environment.Alternatively, the sedimentary environment of Langping platform provided conditions favorable for reef-building communities to develop and reefs to grow rapidly. These factors directly or indirectly determined the ecology of reef-building communities and the general appearance of reef development in the study area.Overall, the environmental factor is the primary factor affecting the overall development trend of reefs.Inferred ecological characteristics of reef communitiesResponse of reef-building corals to hydrodynamic conditionsHydrodynamic conditions are very important factors for reef development, which directly determine the abundance and distribution of each reef-building population and are key factors influencing sedimentation and reef growth, and was particularly evident at Langping. Evidence from the fossils suggested the reef-building corals were also changed in response (Table 1). The hydrodynamic condition changes during the development of reefs are inferred based on analysis of the vertical sediments and microfacies changes of coral reefs in the study area31. How these ancient reef-building corals adapted to hydrodynamic conditions was reconstructed combining the evolution of reef-building communities with the study.Table.1 General situation of reef-building coral population in Langping.Full size tableThe Xiadong coral reef started with colonization and expansion of Diphyphyllum on the bioclastic hard substrates32,33. They grew vertically into upright clusters (Fig. 5A) and were insensitive to more sediment in a relatively calm, turbid water environment34. The relatively dense clumped Siphonodendron and massive Lithostrotion (Fig. 5B) were better suited to the turbulent water environment, becoming dominant over time, with Diphyphyllum subordinate with the continuous increase of the water energy, as indicated by the characteristics of sediment particles from fine to coarse. After flourishing for a period, the Siphonodendron–Lithostrotion assemblage eventually waned, likely due to the failure to adapt to the increasing hydrodynamic conditions. Diphyphyllum had persisted combined with Syringopora, to maintain the growth of the reef. However, this assemblage subsequently declined as a result of strong hydrodynamic conditions and finally died out in response to continuous falling of sea level. Consequently, the reefs stopped developing.Figure 5Sketch of coral cluster with upright growing morphology. Most reef-building corals in Langping grow vertically into cluster colonies. This type of morphology is very favourable for corals to get more living space and is important to reef-building. (A) Cluster coral individuals grow uprightly with certain distance between each other. (B) Polygonal columnar coral individuals grow closely to resist strong water flow. This figure is made by the author with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageThe Longjiangdong multi-layer reef was composed of three relatively independent, flat reef layers, suggesting three distinct periods of reef development. Diverse species were identified in the reef, with colonial coral Diphyphyllum contributing greatly to reef growth. Diphyphyllum clusters colonized in patchy form on substrates composed of bioclasts or lithic gravels (Fig. 6A). The first reef-building process was brief, ending under high-energy water conditions after a period of growing (Fig. 6B). Subsequently the hydrodynamic conditions became weaker and favorable. Then Diphyphyllum once again flourished. Diphyphyllum clumps in the unit grew closely together in strong currents, with larger and more sparse individuals than in the lower units. A relatively low energy environment was formed between the Diphyphyllum clusters (Fig. 6C). Subsequently, Diphyphyllum could only grow in a limited area of suitability due to the disturbance of high-energy water brought about by short-term sea-level rise and fall. Afterwards, the environment became more favourable and Diphyphyllum expanded rapidly. As a result, the upper unit of Longjiangdong coral reef was formed, in which Diphyphyllum individuals were slightly larger than those in the first two units. Finally, because the kinetic energy of the water continued to weaken, the plaster deposition forced the whole coral reef to stop growing (Fig. 6D).Figure 6Micrographs of sediments in different positions of reef. (A) Calcareous bioclastic limestone, with biological particles accounting for about 70% of the debris. Abundant and diverse organisms indicate a medium-energy environment of the subtidal zone. Samples were taken from the bioclastic beach at the reef base. (B) Slightly larger bioclastics but lower biologic content than that in (A) suggest an increasing water energy. (C) Various bioclastic particles account for about 80% of the clastic particles contained in the calcareous bio-granular rock. The obviously small benthos indicate a low-energy environment in the subtidal zone barriered by the Diphyphyllum clusters. (D) Bioclastic grainstone is mainly composed of marl, with fine clastic particles (about 30%) and bedding. Low biomass indicates a low-energy environment of the subtidal zone. This figure is modified by the author with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/). Meaning of the letters in the figure: C crinoids, BF brachiopods, F foraminifera, B bryozoan, P pelletoid, MF mollusk shell fragment.Full size imageLongjiangdong patch reef started to develop in a relatively deep water environment. Diphyphyllum initially colonized and expanded in favorable conditions with the increase of water energy. Then the reef-builders transitioned from a single coral species to an assemblage of Diphyphyllum–Caninia–Lithostrotionella. These three coral species grew independently and contribute almost equally to the structure of the reef. However, the structure and function of the coral community were not yet stable enough. It was easily influenced by the weakening hydrodynamics and the increasing sedimentation, resulting in only small patch reefs.The Xinzhai layer reef was initialized by colonization and expansion of Lonsdaleia on bioclastic beach. Large coral clusters were formed in the presence of turbulent water. With the weakening of hydrodynamic conditions, an unknown branchlike organism and Antheria communities continued to develop separately in this area. Slender branchlike organisms expanded rapidly in these low-energy water environments until they were replaced by some individual corals as hydrodynamic energy increased. Each builder was short-lived in this layer reef, departing from the reef just at the beginning of colonization and expansion, due to rapidly changed hydrodynamic conditions.The evolution of reef-building corals in these four reefs indicated that both the coral assemblages and coral individuals would constantly adapt to the changing hydrodynamic conditions in Langping as sea level rose and fell. Although this was a reactive adjustment of coral populations in response to long-term environmental impacts, it was clearly positive for the building and development of coral reefs.Impact of disturbance on reef communitiesDisturbance is a relatively discontinuous event, which is ubiquitous in nature. It may indirectly affect the composition and population structure of reef communities by changing the environmental conditions, thus affect the structure and function of reef communities, even the evolution of the reef35. The major disturbances evident in these Mississippian framework reefs were associated with frequent changes of water flow, and drastic changes of climate and weather. These seem to be most obvious in the Langping platform due to its small size, with more frequent environmental influence evident on the reef communities in the study area.The most direct effect of disturbance events on coral reefs is the disruption of continuously evolving reef communities, which is common in coral reef studies. After the interruption caused by disturbances, some communities gradually recover due to the absence of continuous disturbance, or the dominant biota may be substituted by invading communities. The winner after interruption is decided by random factors to a large extent, in a ‘Competitive lottery’36. The conditions for the emergence of ‘Competitive lottery’ also include the need for species in a community to have similar abilities to invade discontinuities and to tolerate environmental conditions.Certainly, low-intensity disturbance does not necessarily produce discontinuity, but medium-intensity disturbance without discontinuity could directly impact on community species diversity. According to the ‘Moderate disturbance hypothesis’, moderate disturbance is conducive to a higher level of community diversity37. In environmental conditions with moderate intensity of disturbance, most species will not disappear entirely. The dominant pioneer species will also be restrained by disturbance to a certain extent, so large number of species can coexist, attaining the highest diversity35.The reef-builders in Langping are diverse compared with the Late Carboniferous reefs in Ziyun County10, which also developed in Dian-Qian-Gui Basin. More than 4 reef-building corals are identified in Xiadong reef, while 4 and 3 are in Xinzhai layer reef, Longjiangdong patch reef respectively. These reef-building corals, mostly Diphyphyllum, Lithostrotion, Siphonodendron and Lonsdaleia, were distributed irregularly in the reefs. Their ecological niche and function were likely similar and none of them was obviously dominant in the community (Fig. 7). This is in line with ‘Competitive lottery’ theory and the ‘Moderate disturbance hypothesis’.Figure 7Different species occupied the discontinuity surface irregularly. (A) Different reef-builders colonized and grew on the same hard substrate. (B) and (C) show detailed morphology of colony corals of (A). (D) Colony corals and a large number of individual corals grew together in a limited area, indicating equal colonization on the newly formed discontinuity surface. This figure is modified by the author from field photos with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageThe stability of a classical reef ecosystem includes the ability to withstand external disturbances and the ability to return to its original state once the disturbance is removed37,38. It is generally accepted that communities with high diversity are always more stable although ecosystem stability is not absolutely correlated to biodiversity35.There have been no reef-building corals with strong resistance and rapid recovery ability in the communities in Langping. None of these corals succeeded in developing into dominant species that can build reef shelves, which made the reefs in Langping mostly appear in the form of small patch reefs or reef layers. However, formation of the large reef in Xiadong Village, patch reef in Longjiangdong Village, and layer reef in Xinzhai Village were all related to their relatively high diversity of reef-building corals. Compared with the situation where only one reef-building organism dominated the Bianping large coral reef, Wengdao large phylloid algal reef and Ivanovia cf. manchurica patch reefs in Ziyun County10, Guizhou province, the different coral assemblages in Langping area could effectively adapt to changing hydrodynamic conditions and maintain reef growth.Species diversity increased by disturbance stabilized the ecosystemas shown during the construction of coral reefs in Langping.Effects of non-reef-builders on reef-building coralsBesides reef-building corals, there were a large number of reef-dwellers and off-reef organisms in the study area. Reef-dwellers referred to the species that didn’t directly contribute to reef growth in the community, mainly including various benthos and algaes39. Off-reef organisms are not part of the reef-building community, but also play an important role in participating in energy flow and providing organic matter to the reef ecosystem40.Common reef-dwelling organisms include crinoids, brachiopods, gastropods, various algae, foraminifera, bryozoans and individual corals. Crinoids were overwhelmingly dominant in numbers in the reef samples studied here.Carboniferous echinodermata in Guangxi Province reached its peak in Middle-to-Late Mississippian. In terms of amount and distribution, thick limestone with echinodermata debris in the carbonate platform were often dominated by crinoids41,42,43,44,45,46. The large number of crinoids in Langping excluded other metazoans and restricted the development of benthic reef-builders in Late Viséan-Serpukhovian in Langping, leading to poorly developed reef-building communities.Microorganisms and algaes had limited success in stablishing on the moving clastic beach in frequently disturbed water. There has not been obvious evidence of extensive “algal turf” in the coastal area of Langping platform. Only a few corals bonded by algal mats were observed47 (Fig. 8). In addition to their significant contribution to primary productivity, macroalgae were considered to play an important role in two aspects of coral reef ecosystems. One was to promote reef construction by its own binding and consolidation48,49. The other was to create a good condition for zoobenthos larvae to dwell and develop, thereby improving species diversity50. The limited productivity of algae in Langping constrained coral reef trophic inputs, which may then have limited populations of dependent metazoans. As a result, algaes and other metazoans were unable to achieve a variety of reef-building patterns, such as bonding, bounding, entanglement51,52. The reef framework in the study area was not stable in the presence of strong water flow, and the biological communities could not deal with frequent environmental changes, which were directly related to poor development of calcareous algae.Figure 8Micrographs of microbes and algaes. (A) Encrustations (indicated by black arrows) with distinct thickness around coral clusters formed by microbe and algal mats through bonding mud. The encrustations were formed before the clastic deposition (indicated by white arrows), showing the corals were living then. Microbes and algaes inside of the dense coral clusters had little impact on corals. (B) Single polarized micrograph showed clear and smooth boundaries of coral individuals without encrustation or drilling hole made by microbes or algaes. Few corals surrounded by bonding algaes could be observed in Langping, indicating that algaes were poorly developed between coral clusters. This figure is modified by the author from field photos with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageInfluence of coral morphology on reef developmentThe accumulation of reef structure had obvious impact on communities. Large reef structures could support abundance and diverse biota by modifying local environments and creating diverse conditions. Consequently the reef-building communities thrived between disturbances, stabilizing reef construction. In terms of large reef, the framework-building corals would play a key role in reef construction regardless of which kind of patterns was adopted. Therefore, reef-building corals with large size, rapid growth vertically, and strong resistance would become the biggest contributors to reef frame construction.The main reef-building corals in Langping were composed of Diphyphyllum, Lithostrotion, Siphonodendron, and Lonsdaleia, etc., being the dominant builders. These corals were similar in morphology such as cluster colony, thick and strong skeleton, and densely packed individuals (Fig. 9), which enabled them to resist water flow. At the same time, the upright colonies were adaptable to relatively calm water, being insensitive to mud deposition. The ecological characteristics of the Langping corals matched the gently sloping environment, the deep water environment and the rapidly changing energy of the currents. These cluster corals were able to colonize hard substrates and expand rapidly, thus altering the surrounding environment. The visible carbonate uplifts were formed with a large amount of benthos grouped into reef-building communities. These distinct uplifts constructed by coral clusters in different water conditions are composed of coral reefs of different sizes and appearance in the study area.Figure 9Main reef-building corals in the study area. (A) Diphyphyllum, (B) Lithostrotion, (C) Siphonodendron, (D) Lonsdaleia. (A) Rapidly grew clusters of main reef-building corals. The strong individuals are packed tightly when growing to support each other. This figure is modified by the author from field photos with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageThe complex and diverse local environments formed by large coral reefs can significantly increase benthic populations and improve reef species diversity. As a result, the nutrient flow in the community becomes complicated, and nutrients could be recycled effectively by reducing loss caused by water flow. Therefore, the overall productivity of large coral reef communities was always high. Complex trophic structure satisfied most of the benthos in the community with sufficient nutrients and inorganic salts.The morphology of reef-building corals in Langping enabled them to become predominant species in various water environments, which promoted the continued domed growth of coral reefs and facilitates the development of reef-building communities that form a variety of reefs. It suggests that the morphology of reef-building corals was a key prerequisite for reef development.In conclusion, coral reef communities are always constrained and influenced by environmental conditions. However, the ecology of the inhabitants is also an important factor in the formation of coral reefs. More