Assessment of the breeding system in the Algerian narrow coastal endemism Anacyclus linearilobus (Anthemideae, Asteraceae)
DOI:
https://doi.org/10.3989/ajbm.542Keywords:
Compositae, mixed mating, reproductive assurance, selfing, western MediterraneanAbstract
The breeding system of Anacyclus linearilobus, an annual and endemic species restricted to dune ecosystems of the Algerian coast were assessed through the effect of self-fertilization and intra- and inter-population artificial crosses on the probability of producing viable seeds in 20 individuals from two populations in a common garden. The breeding system was determined for each individual by the self-incompatibility index (ISI). These results were compared with those published for other species of the genus, A. clavatus, A. homogamos and A. valentinus. Results of experimental crosses showed that there was high variation in the female reproductive success between individuals of A. linearilobus, like that found in its sister species, A. valentinus. Unlike the other species in the genus that are self-incompatible, A. linearilobus showed a mixed mating system, with a majority of self-incompatible individuals, others partially self-incompatible and some self-compatible. We argue that this strategy may be related to reproductive assurance in this endemic, annual species whose effective population size has been reduced probably due to individual mating incompatibilities.
Downloads
References
Agudo A.B., Torices R., Loureiro J., Castro S., Castro M. & Álvarez I. 2019. Genome size variation in a hybridizing diploid species complex in Anacyclus (Asteraceae: Anthemideae). International Journal of Plant Sciences 180: 374-385. https://doi.org/10.1086/703127
Alonso C., Vamosi J.C., Knight T.M., Steets J.A. & Ashman T.L. 2010. Is reproduction of endemic plant species particularly pollen limited in biodiversity hotspots? Oikos 119: 1192-1200. https://doi.org/10.1111/j.1600-0706.2009.18026.x
Álvarez I. 2019. Anacyclus L. In Benedí C., Buira A., Rico E., Crespo M.B., Quintanar A., Aedo C. (eds.), Flora iberica vol. 16(3), Compositae (partim). Real Jardín Botánico-CSIC, Madrid.
Álvarez I., Agudo A.B., Herrero A. & Torices R. 2020. The Mendelian inheritance of gynomonoecy: insights from Anacyclus hybridizing species. American Journal of Botany 107: 116-125. https://doi.org/10.1002/ajb2.1414 PMid:31903550
Angeloni F., Ouborg N.J. & Leimu R. 2011. Meta-analysis on the association of population size and life history with inbreeding depression in plants. Biological Conservation 144: 35-43. https://doi.org/10.1016/j.biocon.2010.08.016
Arista M., Berjano R., Viruel J., Ortiz M.A., Talavera M., Ortiz P.L. 2017. Uncertain pollination environment promotes the evolution of a stable mixed reproductive system in the self-incompatible Hypochaeris salzmanniana (Asteraceae). Annals of Botany 120: 447-456. https://doi.org/10.1093/aob/mcx059 PMid:28911017 PMCid:PMC5591423
Barrett S.C.H. 2014. Evolution of mating systems: outcrossing versus selfing. In Losos J.B. (ed.), The Princeton Guide to Evolution. Princeton University Press, Princeton.
Barrett S.C.H. & Harder L.D. 2017. The ecology of mating and its evolutionary consequences in seed plants. Annual Review of Ecology, Evolution and Systematics 48: 135-157. https://doi.org/10.1146/annurev-ecolsys-110316-023021
Bates D., Mächler M., Bolker B.M. & Walker S. 2015. Fitting Linear Mixed-Effects Models using lme4. Journal of Statistical Software 67: 1-48. https://doi.org/10.18637/jss.v067.i01
Bateson W. 1909. Heredity and variation in modern lights. In Seward A.C. (ed.), Darwin and modern science. Cambridge University Press, Cambridge.
Boissier P.E. & Reuter G.F. 1852. Pugillus Plantarum Novarum Africae Borealis Hispaniaeque Australis. Ferd. Ramboz et socii, Geneva.
Busch J.W. & Delph L.F. 2012. The relative importance of reproductive assurance and automatic selection as hypotheses for the evolution of self-fertilization. Annals of Botany 109: 553-562. https://doi.org/10.1093/aob/mcr219 PMid:21937484 PMCid:PMC3278291
Busch J.W. & Schoen D.J. 2008. The evolution of self-incompatibility when mates are limiting. Trends in Plant Science 13: 128-136. https://doi.org/10.1016/j.tplants.2008.01.002 PMid:18296103
Byers D.L. & Waller D.M. 1999. Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annual Review of Ecology and Systematics 30: 479-513. https://doi.org/10.1146/annurev.ecolsys.30.1.479
Charlesworth D. & Charlesworth B. 1987. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology, Evolution and Systematics 18: 237-268. https://doi.org/10.1146/annurev.es.18.110187.001321
Crawford D.J., Moura M., Borges Silva L., Mort M.E., Kerbs B., Schaefer H. & Kelly J.K. 2019. The transition to selfing in Azorean Tolpis (Asteraceae). Plant Systematics and Evolution 305: 305-317. https://doi.org/10.1007/s00606-019-01573-7
Dobzhansky T. 1936. Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21: 113-135. https://doi.org/10.1093/genetics/21.2.113 PMid:17246786 PMCid:PMC1208664
Ferrer M. & Good-Avila S. 2007. Macrophylogenetic analyses of the gain and loss of self-incompatibility in the Asteraceae. New Phytologist 173: 401-14. https://doi.org/10.1111/j.1469-8137.2006.01905.x PMid:17204086
Goldberg E.E., Kohn J.R., Lande R., Robertson K.A., Smith S.A. & Igić B. 2010. Species selection maintains self-incompatibility. Science 330: 493-495. https://doi.org/10.1126/science.1194513 PMid:20966249
Good-Avila S.V., Mena-Alí J.I. & Stephenson A.G. 2008. Evolutionary consequences of variations in self-fertility in self-incompatible species. In Franklin-Tong E. (ed.), Self-incompatibility in flowering plants-evolution, diversity, and mechanisms. Springer, Berlin. https://doi.org/10.1007/978-3-540-68486-2_2
Goodwillie C., Kalisz S. & Eckert C.G. 2005. The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annual Review of Ecology, Evolution and Systematics 36: 47-79. https://doi.org/10.1146/annurev.ecolsys.36.091704.175539
Grossenbacher D.L., Brandvain Y., Auld J.R., Burd M., Cheptou P.-O., Conner J.K., Grant A.G., Hovick S.M., Pannell J.R., Pauw A., Petanidou T., Randle A.M., Rubio de Casas R., Vamosi J., Winn A., Igic B., Busch J.W., Kalisz S. & Goldberg E.E. 2017. Self-compatibility is over-represented on islands. New Phytologist 215: 469-478. https://doi.org/10.1111/nph.14534 PMid:28382619
Humphries C.J. 1979. A revision of the genus Anacyclus L. (Compositae: Anthemideae). Bulletin of the British Museum (Natural History) Botany 7: 83-142.
Humphries C.J. 1981. Cytogenetic and cladistic studies in Anacyclus (Compositae: Anthemideae). Nordic Journal of Botany 1: 83-96. https://doi.org/10.1111/j.1756-1051.1981.tb01038.x
Igić B., Lande R. & Kohn J.R. 2008. Loss of self-incompatibility and its evolutionary consequences. International Journal of Plant Sciences 169: 93-104. https://doi.org/10.1086/523362
Kerbs B., Crawford D.J., White G., Moura M., Borges Silva L., Schaefer H., Brown K., Mort M.E. & Kelly J.K. 2020. How rapidly do self-compatible populations evolve selfing? Mating system estimation within recently evolved self-compatible populations of Azorean Tolpis succulenta (Asteraceae). Ecology and Evolution 10: 13990-13999. https://doi.org/10.1002/ece3.6992 PMid:33391697 PMCid:PMC7771160
Leins P. & Erbar C. 2006. Secondary pollen presentation syndromes of the Asterales-a phylogenetic perspective. Botanische Jahrbücher fur Systematik, Pflanzengeschichte und Pflanzengeographie 127: 83-103. https://doi.org/10.1127/0006-8152/2006/0127-0083
Levin D.A. 2003. The cytoplasmic factor in plant speciation. Systematic Botany 28: 5-11.
Lloyd D.G. 1992. Self- and cross-fertilization in plants II. The selection of self-fertilization. International Journal of Plant Sciences 153: 370-380. https://doi.org/10.1086/297041
Muller H.J. 1942. Isolating mechanisms, evolution, and temperature. Biology Symposium 6: 71-125.
Oberprieler C. 2004. On the taxonomic status and the phylogenetic relationships of some unispecific Mediterranean genera of Compositae-Anthemideae I. Brocchia, Endopappus and Heliocauta. Willdenowia 34: 39-57. https://doi.org/10.3372/wi.34.34102
Patterson H.D. & Thompson R. 1971. Recovery of inter-block information when block sizes are unequal. Biometrika 58: 545-554. https://doi.org/10.1093/biomet/58.3.545
Pérez M.E., Meléndez-Ackerman E.J. & Monsegur-Rivera O.A. 2018. Breeding system and pollination of Gesneria pauciflora (Gesneriaceae), a threatened Caribbean species. Flora 242: 8-15. https://doi.org/10.1016/j.flora.2018.02.009
Raduski A.R., Haney E.B., Igić B. 2012. The expression of self-incompatibility in angiosperms is bimodal. Evolution 66: 1275-1283. https://doi.org/10.1111/j.1558-5646.2011.01505.x PMid:22486704
Rosato M., Álvarez I., Nieto Feliner G. & Rosselló J.A. 2017. High and uneven levels of 45S rDNA site-number variation across wild populations of a diploid plant genus (Anacyclus, Asteraceae). PLoS One 12: e0187131. https://doi.org/10.1371/journal.pone.0187131 PMid:29088249 PMCid:PMC5663423
Shivanna K.R. 2014. Reproductive assurance through autogamy in some annual weed species. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences 84: 681-687. https://doi.org/10.1007/s40011-014-0307-x
Shivanna K.R. 2015. Reproductive assurance through autogamous self-pollination across diverse sexual and breeding systems. Current Science 109: 1255-1263. https://doi.org/10.18520/cs/v109/i7/1255-1263
Snoussi M. & Aoul E.H.T. 2000. Integrated coastal zone management programme northwest African region case. Ocean & Coastal Management 43: 1033-1045. https://doi.org/10.1016/S0964-5691(00)00071-5
Stebbins G.L. 1974. Flowering plants. Evolution above the species level. Belknap Press, Cambridge. https://doi.org/10.4159/harvard.9780674864856 PMCid:PMC301458
Torices R., Agudo A. & Álvarez I. 2013. Not only size matters: achene morphology affects time of seedling emergence in three heterocarpic species of Anacyclus (Anthemideae, Asteraceae). Anales del Jardín Botánico de Madrid 70: 48-55. https://doi.org/10.3989/ajbm.2351
Vitales D., Nieto Feliner G., Vallès J., Garnatje T., Firat M. & Álvarez I. 2018. A new circumscription of the Mediterranean Anacyclus (Anthemideae, Asteraceae) based on plastid and nuclear DNA markers. Phytotaxa 349: 1-17. https://doi.org/10.11646/phytotaxa.349.1.1
Vitales D., Álvarez I., Garcia S., Hidalgo O., Nieto Feliner G., Pellicer J., Vallès J. & Garnatje T. 2020. Genome size variation at constant chromosome number is not correlated with repetitive DNA dynamism in Anacyclus (Asteraceae). Annals of Botany 125: 611-623. https://doi.org/10.1093/aob/mcz183 PMid:31697800 PMCid:PMC7103019
Yates C.J. & Ladd P.G. 2004. Breeding system, pollination and demography in the rare granite endemic shrub Verticordia staminosa ssp. staminosa in south-west Western Australia. Austral Ecology 29: 189-200. https://doi.org/10.1111/j.1442-9993.2004.01336.x
Zuur A.F., Leno E.N. & Elphick C.S. 2010. A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1: 3-14. https://doi.org/10.1111/j.2041-210X.2009.00001.x
Published
How to Cite
Issue
Section
License
Copyright (c) 2022 Consejo Superior de Investigaciones Científicas (CSIC)

This work is licensed under a Creative Commons Attribution 4.0 International License.
© CSIC. Manuscripts published in both the print and online versions of this journal are the property of the Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.
All contents of this electronic edition, except where otherwise noted, are distributed under a Creative Commons Attribution 4.0 International (CC BY 4.0) licence. You may read the basic information and the legal text of the licence. The indication of the CC BY 4.0 licence must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the final version of the work produced by the publisher, is not allowed.
Funding data
European Regional Development Fund
Grant numbers CGL2010-18039;CGL2013-49097-C2-1-P
Ministerio de Ciencia e Innovación
Grant numbers CGL2010-18039
Ministerio de Economía y Competitividad
Grant numbers CGL2013-49097-C2-1-P