Abstract
Functionally and evolutionarily distinct species have traits or an evolutionary history that are shared by few others in a given set, which make them priority species for biodiversity conservation. On islands, life in isolation has led to the evolution of many distinct forms and functions as well as to a high level of endemism. The aim of this study is to assess the evolutionary and functional distinctiveness of insular monocotyledons and their distribution across 126 islands worldwide. We show that evolutionary and functional distinctiveness are decoupled but that both are higher on islands than on continental areas. Anagenesis on islands followed by extinctions and/or diversification on the mainland may have led to highly evolutionarily distinct species while functionally distinct species may have arisen from ecological niche shift or niche expansion. Insular endemic species with high evolutionary distinctiveness but not with high functional distinctiveness are significantly range-restricted compared to less distinct species, possibly indicating differences in dispersal potential. By showing that distinctiveness is high on islands and that the most distinct species are range-restricted, our study has important conservation implications. Indeed, islands are among the most threatened systems of the world, and extinctions of the most distinct species could lead to significant loss of phylogenetic and functional diversity.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.
Code availability
Analyses were performed with R (R Core Team 2020).
References
Alsos IG, Engelskjon T, Gielly L et al (2005) Impact of ice ages on circumpolar molecular diversity: insights from an ecological key species. Mol Ecol 14:2739–2753. https://doi.org/10.1111/j.1365-294X.2005.02621.x
Barton K (2009) Mu-MIn: Multi-model inference. R Package Version 0.12.0. http://R-Forge.R-project.org/projects/mumin/
Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745. https://doi.org/10.1111/j.0014-3820.2003.tb00285.x
Bouchenak-Khelladi Y, Muasya AM, Linder HP (2014) A revised evolutionary history of Poales: origins and diversification: evolutionary history of Poales. Bot J Linn Soc 175:4–16. https://doi.org/10.1111/boj.12160
Cadotte MW, Cardinale BJ, Oakley TH (2008) Evolutionary history and the effect of biodiversity on plant productivity. Proc Natl Acad Sci 105:17012–17017. https://doi.org/10.1073/pnas.0805962105
Cadotte MW, Jonathan Davies T (2010) Rarest of the rare: advances in combining evolutionary distinctiveness and scarcity to inform conservation at biogeographical scales: conservation phylo-biogeography. Divers Distrib 16:376–385. https://doi.org/10.1111/j.1472-4642.2010.00650.x
Caesar M, Grandcolas P, Pellens R (2017) Outstanding micro-endemism in New Caledonia: more than one out of ten animal species have a very restricted distribution range. PLoS ONE 12:e0181437. https://doi.org/10.1371/journal.pone.0181437
Cameron KM, Chase MW, Rudall PJ (2003) Recircumscription of the monocotyledonous family Petrosaviaceae to include Japonolirion. Brittonia 55:214–225
Cássia-Silva C, Freitas CG, Lemes LP et al (2020) Higher evolutionary rates in life-history traits in insular than in mainland palms. Sci Rep 10:21125. https://doi.org/10.1038/s41598-020-78267-5
Cooke RSC, Eigenbrod F, Bates AE (2020) Ecological distinctiveness of birds and mammals at the global scale. Global Ecology and Conservation 22:e00970. https://doi.org/10.1016/j.gecco.2020.e00970
Cornwell WK, Pearse WD, Dalrymple RL, Zanne AE (2019) What we (don’t) know about global plant diversity. Ecography 42:1819–1831. https://doi.org/10.1111/ecog.04481
Cronk QCB (1997) Islands: stability, diversity, conservation. Biodivers Conserv 6:477–493. https://doi.org/10.1023/A:1018372910025
Davies TJ, Buckley LB (2011) Phylogenetic diversity as a window into the evolutionary and biogeographic histories of present-day richness gradients for mammals. Phil Trans R Soc B 366:2414–2425. https://doi.org/10.1098/rstb.2011.0058
Diamond JM (1970) Ecological consequences of island colonization by Southwest Pacific Birds, I. Types of niche shifts. Proc Natl Acad Sci 67:529–536. https://doi.org/10.1073/pnas.67.2.529
Díaz S, Kattge J, Cornelissen JHC et al (2015) The global spectrum of plant form and function. Nature 529:167
Emerson BC, Gillespie RG (2008) Phylogenetic analysis of community assembly and structure over space and time. Trends Ecol Evol 23:619–630. https://doi.org/10.1016/j.tree.2008.07.005
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Cons 61:1–10. https://doi.org/10.1016/0006-3207(92)91201-3
Faith DP (2016) A general model for biodiversity and its value. In: Garson J, Plutynski A, Sarkar S (eds) The Routledge handbook of philosophy of biodiversity. Routledge, Milton Park, p 344
Faith DP (2018) Phylogenetic diversity and conservation evaluation: perspectives on multiple values, indices, and scales of application. In: Scherson RA, Faith DP (eds) Phylogenetic diversity: applications and challenges in biodiversity science. Springer, Cham, pp 1–26
Fajardo J, Mateo RG, Vargas P et al (2019) The role of abiotic mechanisms of long-distance dispersal in the American origin of the Galápagos flora. Global Ecol Biogeogr 28:1610–1620. https://doi.org/10.1111/geb.12977
Faurby S, Svenning J-C (2016) Resurrection of the island rule: human-driven extinctions have obscured a basic evolutionary pattern. Am Nat 187:812–820. https://doi.org/10.1086/686268
Flynn DFB, Gogol-Prokurat M, Nogeire T et al (2009) Loss of functional diversity under land use intensification across multiple taxa. Ecol Lett 12:22–33. https://doi.org/10.1111/j.1461-0248.2008.01255.x
Fonseca CR, Ganade G (2001) Species functional redundancy, random extinctions and the stability of ecosystems. J Ecol 89:118–125. https://doi.org/10.1046/j.1365-2745.2001.00528.x
Forest F, Moat J, Baloch E et al (2018) Gymnosperms on the EDGE. Sci Rep 8:6053. https://doi.org/10.1038/s41598-018-24365-4
Gavrilets S, Losos JB (2009) Adaptive radiation: contrasting theory with data. Science 323:732–737. https://doi.org/10.1126/science.1157966
Gillespie RG, Baldwin BG, Waters JM et al (2012) Long-distance dispersal: a framework for hypothesis testing. Trends Ecol Evol 27:47–56. https://doi.org/10.1016/j.tree.2011.08.009
Gillespie RG, Clague DA (2009) Encyclopedia of islands. University of California Press
Gillespie RG, Roderick GK (2002) Arthropods on islands: colonization, speciation, and conservation. Annu Rev Entomol 47:595–632. https://doi.org/10.1146/annurev.ento.47.091201.145244
Goldberg EE, Lancaster LT, Ree RH (2011) Phylogenetic inference of reciprocal effects between geographic range evolution and diversification. Syst Biol 60:451–465. https://doi.org/10.1093/sysbio/syr046
Gower JC (1971) A general coefficient of similarity and some of its properties. Biometrics 27:857. https://doi.org/10.2307/2528823
Grandcolas P, Murienne J, Robillard T et al (2008) New Caledonia: a very old Darwinian island? Phil Trans R Soc B 363:3309–3317. https://doi.org/10.1098/rstb.2008.0122
Grandcolas P, Nattier R, Trewick S (2014) Relict species: a relict concept? Trends Ecol Evol 29:655–663. https://doi.org/10.1016/j.tree.2014.10.002
Grenié M, Mouillot D, Villéger S et al (2018) Functional rarity of coral reef fishes at the global scale: hotspots and challenges for conservation. Biol Cons 226:288–299. https://doi.org/10.1016/j.biocon.2018.08.011
Gumbs R, Gray CL, Böhm M et al (2020) Global priorities for conservation of reptilian phylogenetic diversity in the face of human impacts. Nat Commun 11:2616. https://doi.org/10.1038/s41467-020-16410-6
Gumbs R, Chaudhary A, Daru BH et al (2021) The Post-2020 Global Biodiversity Framework must safeguard the Tree of Life. BioRxiv
Harnik PG (2011) Direct and indirect effects of biological factors on extinction risk in fossil bivalves. Proc Natl Acad Sci 108:13594–13599. https://doi.org/10.1073/pnas.1100572108
Harnik PG, Simpson C, Payne JL (2012) Long-term differences in extinction risk among the seven forms of rarity. Proc R Soc B 279:4969–4976. https://doi.org/10.1098/rspb.2012.1902
Heads M (2018) Metapopulation vicariance explains old endemics on young volcanic islands. Cladistics 34:292–311. https://doi.org/10.1111/cla.12204
Heleno R, Vargas P (2015) How do islands become green?: How do islands become green? Glob Ecol Biogeogr 24:518–526. https://doi.org/10.1111/geb.12273
Huang D (2012) Threatened Reef Corals of the World. PLoS ONE 7:e34459. https://doi.org/10.1371/journal.pone.0034459
IPBES (2019) Summary for policymakers of the global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. IPBES secretariat, Bonn, Germany
Isaac NJB, Turvey ST, Collen B et al (2007) Mammals on the EDGE: Conservation Priorities Based on Threat and Phylogeny. PLoS ONE 2:e296. https://doi.org/10.1371/journal.pone.0000296
Jetz W, Thomas GH, Joy JB et al (2014) Global distribution and conservation of evolutionary distinctness in birds. Curr Biol 24:919–930. https://doi.org/10.1016/j.cub.2014.03.011
Kier G, Kreft H, Lee TM et al (2009) A global assessment of endemism and species richness across island and mainland regions. Proc Natl Acad Sci 106:9322–9327. https://doi.org/10.1073/pnas.0810306106
Knope ML, Morden CW, Funk VA, Fukami T (2012) Area and the rapid radiation of Hawaiian Bidens (Asteraceae): rapid radiation of Hawaiian Bidens. J Biogeogr 39:1206–1216. https://doi.org/10.1111/j.1365-2699.2012.02687.x
Kondratyeva A, Grandcolas P, Pavoine S (2019) Reconciling the concepts and measures of diversity, rarity and originality in ecology and evolution: reconciling diversity, rarity and originality. Biol Rev 94:1317–1337. https://doi.org/10.1111/brv.12504
Leclerc C, Courchamp F, Bellard C (2018) Insular threat associations within taxa worldwide. Sci Rep 8:6393. https://doi.org/10.1038/s41598-018-24733-0
Leclerc C, Villéger S, Marino C, Bellard C (2020) Global changes threaten functional and taxonomic diversity of insular species worldwide. Divers Distrib 26:402–414. https://doi.org/10.1111/ddi.13024
Leitão RP, Zuanon J, Villéger S et al (2016) Rare species contribute disproportionately to the functional structure of species assemblages. Proc R Soc B 283:20160084. https://doi.org/10.1098/rspb.2016.0084
Loiseau N, Mouquet N, Casajus N et al (2020) Global distribution and conservation status of ecologically rare mammal and bird species. Nat Commun 11:5071. https://doi.org/10.1038/s41467-020-18779-w
Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11:995–1003. https://doi.org/10.1111/j.1461-0248.2008.01229.x
MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton
Mazel F, Mooers AO, Riva GVD, Pennell MW (2017) Conserving phylogenetic diversity can be a poor strategy for conserving functional diversity. Syst Biol 66:1019–1027. https://doi.org/10.1093/sysbio/syx054
Mouillot D, Culioli JM, Pelletier D, Tomasini JA (2008) Do we protect biological originality in protected areas? A new index and an application to the Bonifacio Strait natural reserve. Biol Cons 141:1569–1580. https://doi.org/10.1016/j.biocon.2008.04.002
Mouillot D, Graham NAJ, Villéger S et al (2013) A functional approach reveals community responses to disturbances. Trends Ecol Evol 28:167–177. https://doi.org/10.1016/j.tree.2012.10.004
Nattier R, Pellens R, Robillard T et al (2017) Updating the phylogenetic dating of New Caledonian biodiversity with a meta-analysis of the available evidence. Sci Rep 7:3705. https://doi.org/10.1038/s41598-017-02964-x
Negoita L, Fridley JD, Lomolino MV et al (2016) Isolation-driven functional assembly of plant communities on islands. Ecography 39:1066–1077. https://doi.org/10.1111/ecog.01551
Norder SJ, Proios K, Whittaker RJ et al (2019) Beyond the last glacial maximum: island endemism is best explained by long-lasting archipelago configurations. Glob Ecol Biogeogr 28:184–197. https://doi.org/10.1111/geb.12835
Oliver TH, Heard MS, Isaac NJB et al (2015) Biodiversity and resilience of ecosystem functions. Trends Ecol Evol 30:673–684. https://doi.org/10.1016/j.tree.2015.08.009
Ottaviani G, Keppel G, Götzenberger L et al (2020) Linking plant functional ecology to island biogeography. Trends Plant Sci 25:329–339. https://doi.org/10.1016/j.tplants.2019.12.022
Owen NR, Gumbs R, Gray CL, Faith DP (2019) Global conservation of phylogenetic diversity captures more than just functional diversity. Nat Commun 10:859. https://doi.org/10.1038/s41467-019-08600-8
Paradis E, Schliep K (2019) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528. https://doi.org/10.1093/bioinformatics/bty633
Patiño J, Whittaker RJ, Borges PAV et al (2017) A roadmap for island biology: 50 fundamental questions after 50 years of The Theory of Island Biogeography. J Biogeogr 44:963–983. https://doi.org/10.1111/jbi.12986
Pavoine S (2020) adiv: An r package to analyse biodiversity in ecology. Methods Ecol Evol 11:1106–1112. https://doi.org/10.1111/2041-210X.13430
Pavoine S, Ollier S, Dufour A-B (2005) Is the originality of a species measurable?: originality of a species. Ecol Lett 8:579–586. https://doi.org/10.1111/j.1461-0248.2005.00752.x
Pavoine S, Bonsall MB, Dupaix A et al (2017) From phylogenetic to functional originality: guide through indices and new developments. Ecol Ind 82:196–205. https://doi.org/10.1016/j.ecolind.2017.06.056
Penone C, Davidson AD, Shoemaker KT et al (2014) Imputation of missing data in life-history trait datasets: which approach performs the best? Methods Ecol Evol 5:961–970. https://doi.org/10.1111/2041-210X.12232
Pérez-Escobar OA, Chomicki G, Condamine FL et al (2017) Recent origin and rapid speciation of Neotropical orchids in the world’s richest plant biodiversity hotspot. New Phytol 215:891–905. https://doi.org/10.1111/nph.14629
Petchey OL, Hector A, Gaston KJ (2004) How do different measures of functional diversity perform? Ecology 85:847–857. https://doi.org/10.1890/03-0226
Qian H, Jin Y (2016) An updated megaphylogeny of plants, a tool for generating plant phylogenies and an analysis of phylogenetic community structure. Journal of Plant Ecology 9:233–239. https://doi.org/10.1093/jpe/rtv047
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Redding DW, Hartmann K, Mimoto A et al (2008) Evolutionarily distinctive species often capture more phylogenetic diversity than expected. J Theor Biol 251:606–615. https://doi.org/10.1016/j.jtbi.2007.12.006
Redding DW, Mazel F, Mooers AØ (2014) Measuring evolutionary isolation for conservation. PLoS ONE 9:e113490. https://doi.org/10.1371/journal.pone.0113490
Redding DW, Mooers Aø (2006) Incorporating evolutionary measures into conservation prioritization. Conserv Biol 20:1670–1678. https://doi.org/10.1111/j.1523-1739.2006.00555.x
Rensch B (1959) Evolution above the species level. Columbia University Press
Robuchon M, Pavoine S, Véron S et al (2021) Revisiting species and areas of interest for conserving global mammalian phylogenetic diversity. Nat Commun 12:1–11. https://doi.org/10.1038/s41467-021-23861-y
Rodrigues A, Pilgrim J, Lamoreux J et al (2006) The value of the IUCN red list for conservation. Trends Ecol Evol 21:71–76. https://doi.org/10.1016/j.tree.2005.10.010
Rosauer D, Laffan SW, Crisp MD et al (2009) Phylogenetic endemism: a new approach for identifying geographical concentrations of evolutionary history. Mol Ecol 18:4061–4072. https://doi.org/10.1111/j.1365-294X.2009.04311.x
Rosindell J, Phillimore AB (2011) A unified model of island biogeography sheds light on the zone of radiation: a unified model of island biogeography. Ecol Lett 14:552–560. https://doi.org/10.1111/j.1461-0248.2011.01617.x
Santos AMC, Cianciaruso MV, De Marco P, Ricklefs R (2016) Global patterns of functional diversity and assemblage structure of island parasitoid faunas. Glob Ecol Biogeogr 25:869–879. https://doi.org/10.1111/geb.12340
Simberloff DS (1974) equilibrium theory of island biogeography and ecology. Annu Rev Ecol Syst 5:161–182. https://doi.org/10.1146/annurev.es.05.110174.001113
Stein RW, Mull CG, Kuhn TS et al (2018) Global priorities for conserving the evolutionary history of sharks, rays and chimaeras. Nature Ecology & Evolution 2:288–298. https://doi.org/10.1038/s41559-017-0448-4
Steinbauer MJ, Field R, Grytnes J-A et al (2016) Topography-driven isolation, speciation and a global increase of endemism with elevation: topographic isolation and endemism. Glob Ecol Biogeogr 25:1097–1107. https://doi.org/10.1111/geb.12469
Stuessy TF, Jakubowsky G, Gomez RS et al (2006) Anagenetic evolution in island plants. J Biogeography 33:1259–1265. https://doi.org/10.1111/j.1365-2699.2006.01504.x
Thuiller W, Maiorano L, Mazel F et al (2015) Conserving the functional and phylogenetic trees of life of European tetrapods. Phil Trans R Soc B 370:20140005–20140005. https://doi.org/10.1098/rstb.2014.0005
Triantis KA, Economo EP, Guilhaumon F, Ricklefs RE (2015) Diversity regulation at macro-scales: species richness on oceanic archipelagos: diversity on oceanic archipelagos. Glob Ecol Biogeogr 24:594–605. https://doi.org/10.1111/geb.12301
UNEP-WCMC (2013) Global Islands Database. United Nation’s Environmental Program, Cambridge, United Kingdom
Veron S, Haevermans T, Govaerts R et al (2019) Distribution and relative age of endemism across islands worldwide. Sci Rep 9:11693. https://doi.org/10.1038/s41598-019-47951-6
Veron S, Saito V, Padilla-García N et al (2019) The use of phylogenetic diversity in conservation biology and community ecology: a common base but different approaches. Q Rev Biol 94:123–148. https://doi.org/10.1086/703580
Violle C, Reich PB, Pacala SW et al (2014) The emergence and promise of functional biogeography. Proc Natl Acad Sci 111:13690–13696. https://doi.org/10.1073/pnas.1415442111
Violle C, Thuiller W, Mouquet N et al (2017) Functional rarity: the ecology of outliers. Trends Ecol Evol 32:356–367. https://doi.org/10.1016/j.tree.2017.02.002
Vocabulary Maintenance Specification Task Group (2017) Vocabulary Maintenance Specification. Biodiversity Information Standards (TDWG). http://rs.tdwg.org/vms/doc/specification/
Warren BH, Simberloff D, Ricklefs RE et al (2015) Islands as model systems in ecology and evolution: prospects fifty years after MacArthur-Wilson. Ecol Lett 18:200–217. https://doi.org/10.1111/ele.12398
Warren BH, Hagen O, Gerber F et al (2018) Evaluating alternative explanations for an association of extinction risk and evolutionary uniqueness in multiple insular lineages: extinction and evolutionary uniqueness. Evolution 72:2005–2024. https://doi.org/10.1111/evo.13582
Weigelt P, Jetz W, Kreft H (2013) Bioclimatic and physical characterization of the world’s islands. Proc Natl Acad Sci 110:15307–15312. https://doi.org/10.1073/pnas.1306309110
Whittaker RJ, Fernández-Palacios JM (2007) Island biogeography: ecology, evolution, and conservation. Oxford University Press
Whittaker RJ, Fernández-Palacios JM, Matthews TJ et al (2017) Island biogeography: taking the long view of nature’s laboratories. Science 357:eaam8326. https://doi.org/10.1126/science.aam8326
Acknowledgements
We are grateful to Sandrine Pavoine for her valuable contribution to the study, both in the conception of the study and in bringing new ideas. We would also like to thank Nicolas Dubos for his valuable insights on the statistical analyses, Anne Clay for revising the text and Sandra Diaz for her insightful discussions.
Funding
This study has been funded by the French State through the National Reasearch Agency under the LabEx ANR-10-LABX-0003-BCDiv, within the framework of the ‘Investing for the future’ program (ANR-11-IDEX-0004-02).
Author information
Authors and Affiliations
Contributions
The authors are interested in the conservation of different biodiversity facets, especially in islands. All authors work on projects investigating phylogenetic and functional diversity on a global scale. RP, TH, MM and SV conceived the project, and obtained the research funds. All authors contributed to the manuscript and gave final approval for publication. SV, RG and TH collected the data. SV analysed the data. SV and AK prepared the figures. MM and RP are senior authors.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Daniel Sanchez Mata.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Veron, S., Kondratyeva, A., Robuchon, M. et al. High evolutionary and functional distinctiveness of endemic monocots in world islands. Biodivers Conserv 30, 3697–3715 (2021). https://doi.org/10.1007/s10531-021-02272-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-021-02272-x