Abstract
Stone oaks, or Lithocarpus species of Fagaceae are ecologically important canopy trees in the tropical and subtropical forests over East Asia, and the fruits of which are important food sources for insects and vertebrates there. The great fruit morphological variation of this genus represents two fruit types, acorn and enclosed receptacle fruit types. However, the evolutionary mechanisms of differentiation into these two fruit types with contrasting morphology remain a puzzle. To reveal the morphogenetic properties of two fruit types, we observed tissue differentiation and development among 20 Lithocarpus species from fruit set to maturity. Unlike in fruits of Quercus, the endocarp differentiation in Lithocarpus fruits occurred later than exocarp and mesocarp. Cupules provided further protection of developing seeds, particularly of acorn-type fruits. Fruits of Lithocarpus and Quercus acorns share similar insect predators. At fruit set, both acorn and enclosed receptacle types were largely identical, with similar tissue morphology and the sequence of differentiation. The distinct difference between two fruit types at maturity came from varied rates and degrees of development between the pericarp and receptacle tissues. We found that heterochrony between two tissues could create substantially divergent ecological strategies for protection and dispersal of their seeds, which is essential for the evolution of two fruit types.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Borgardt SJ, Nixon KC (2003) A comparative flower and fruit anatomical study of Quercus acutissima, a biennial-fruiting oak from the Cerris group (Fagaceae). Am J Bot 90:1567–1584. https://doi.org/10.3732/ajb.90.11.1567
Branco M, Branco C, Merouani H, Almeida MH (2002) Germination success, survival and seedling vigour of Quercus suber acorns in relation to insect damage. For Ecol Manage 166:159–164. https://doi.org/10.1016/S0378-1127(01)00669-7
Brett DW (1964) The inflorescence of Fagus and Castanea, and the evolution of the cupules of the Fagaceae. New Phytol 63:96–118
Camus A (1952) Les chênes: monographie du genre Quercus. P. Lechevalier, Paris
Cannon CH (2001) Morphological and molecular diversity in Lithocarpus (Fagaceae) of Mount Kinabalu. Saban Park Nat J 4:45–69
Cannon CH, Manos PS (2003) Phylogeography of the Southeast Asian stone oaks (Lithocarpus). J Anim Ecol 30:211–226
Cannon CH, Manos PS (2001) Combining and comparing morphometric shape descriptors with a molecular phylogeny: the case of fruit type evolution in Bornean Lithocarpus (Fagaceae). Syst Biol 50:860–880
Chen X, Cannon CH, Conklin-Brittan N, Lou (2012) Evidence for a trade-off strategy in stone oak (Lithocarpus) seeds between physical and chemical defense highlights fiber as an important antifeedant. PLoS One 7:e32890. https://doi.org/10.1371/journal.pone.0032890
Chen X, Kohyama TS, Cannon CH (2018) Associated morphometric and geospatial differentiation among 98 species of stone oaks (Lithocarpus). PLoS One 13:e0199538. https://doi.org/10.1371/journal.pone.0199538
Crawley MJ, Long CR (1995) Alternate bearing, predator satiation and seedling recruitment in Quercus Robur L. J Ecol 83:683–696. https://doi.org/10.2307/2261636
Deng M, Zhou Z, Chen Y, Sun W (2008) Systematic significance of the development and anatomy of flowers and fruit of Quercus schottkyana (subgenus Cyclobalanopsis: Fagaceae). Int J Plant Sci 169:1261–1277. https://doi.org/10.1086/591976
Fey BS, Endress PK (1983) Development and morphological interpretation of the cupule in Fagaceae. Flora 173:451–468
Forman LL (1966) On the evolution of the cupules in the Fagaceae. Kew Bull 18:385–419
Fukumoto H, Kajimura H (2003) Seed-insect fauna in pre-dispersal acorns of Quercus variabilis and Q. serrata and its impact on acorn production. In: IUFRO Kanazawa 2003 Forest Insect Population Dynamics and Host Influences, pp 90–93
Fukumoto H, Kajimura H (2000) Effects of insect predation on hypocotyl survival and germination success of mature Quercus variabilis acorns. J For Res 5:31–34. https://doi.org/10.1007/BF02762760
Fukumoto H, Kajimura H (2001) Guild structures of seed insects in relation to acorn development in two oak species. Ecol Res 16:145–155. https://doi.org/10.1111/J.1440-1703.2001.00380.PP.X
Hawker JS, Buttrose MS (1980) Development of the almond nut (Prunus dulcis (Mill.) D. A. Webb). Anatomy and chemical composition of fruit parts from anthesis to maturity. Ann Bot 46:313–321
Huang CJ, Zhang YT, Bartholomew B (2000) Fagaceae. Flora of China: Cycadaceae through Fagaceae. Science Press, Missouri Botanical Garden, Beijing
Janzen DH (1971) Seed predation by animals. Annu Rev Ecol Syst 2:465–492. https://doi.org/10.1146/annurev.es.02.110171.002341
Kaul RB (1987) Reproductive structure of Lithocarpus sensu lato (Fagaceae): cymules and fruits. J Arnold Arbor 68:73–104. https://doi.org/10.1086/332616
Leiva MJ, Fernández-Alés R (2005) Holm-oak (Quercus ilex subsp. Ballota) acorns infestation by insects in Mediterranean dehesas and shrublands. For Ecol Manag 212:221–229. https://doi.org/10.1016/j.foreco.2005.03.036
Maeto K (1995) Relationships between size and mortality of Quercus mongolica var. grosseserrata acorns due to pre-dispersal infestation by frugivorous insects. J Jpn For Soc 77:213–219
Maeto K, Ozaki K (2003) Prolonged diapause of specialist seed-feeders makes predator satiation unstable in masting of Quercus crispula. Oecologia 137:392–398. https://doi.org/10.1007/s00442-003-1381-6
Maier MJ, Marco M, Maier J (2015) Package “DirichletReg”
McKinney ML, McNamara KJ (1991) Heterochrony: the evolution of ontogeny. Heterochrony. Springer , Boston, pp 1–12
McNamara KJ (2012) Heterochrony: the evolution of development. Evol Educ Outreach 5:203–218. https://doi.org/10.1007/s12052-012-0420-3
Mogensen HL (1975) Ovule abortion in Quercus (Fagaceae). Am J Bot 62:160–165
Mogensen HL (1965) A contribution to the anatomical development of the acorn in Quercus L. Iowa State J Sci 40:221–255
Nast CG (1935) Morphological development of the fruit of Juglans regia. Hilgardia 9:345–381. https://doi.org/10.3733/hilg.v09n07p345
Oh S-H, Manos PS (2008) Molecular phylogenetics and cupule evolution in Fagaceae as inferred from nuclear CRABS CLAW sequences. Taxon 57:434–451
Osborne DJ, Jackson MB (1989) Cell separation in plants: physiology, biochemistry, and molecular biology. Springer, Berlin
Östergård H, Hambäck PA, Ehrlén J (2007) Pre-dispersal seed predation: the role of fruit abortion and selective oviposition. Ecology 88:2959–2965. https://doi.org/10.1890/07-0346.1
Perea R, Venturas M, Gil L (2013) Empty seeds are not always bad: simultaneous affect of seed emptiness and masting on animal seed predation. PLoS One 8:e65573. https://doi.org/10.1371/journal.pone.0065573
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Ramos-Ordonez MF, Arizmendi MC, Marquez-Guzman J (2012) The fruit of Bursera: structure, maturation and parthenocarpy. AoB Plants 2012:pls027–pls027. https://doi.org/10.1093/aobpla/pls027
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
van Soepadmo E (1972) Fagaceae. Flora Malesiana-Series 1, Spermatophyta. Noordhoff-Kolff, Djakarta
Stephenson AG (1981) Flower and fruit abortion: proximate causes and ultimate functions. Annu Rev Ecol Syst 12:253–279
Teruya K, Shinzato T, Sasaki T, Nakao T (2010) Annual fluctuation and seasonal falling pattern of mature acorns of the beech family and a survey of their acorn-infesting insect fauna on subtropical Okinawa Island. Tropics 18:231–249
Traveset A (1993) Deceptive fruits reduce seed predation by insects in Pistacia terebinthus L. (Anacardiaceae). Evol Ecol 7:357–361. https://doi.org/10.1007/BF01237867
Ueda A (2000) Pre- and post-dispersal damage to the acorns of two oak species (Quercus serrata Thunb. and Q. mongolica Fisher) in a species-rich deciduous forest. J For Res 5:169–174. https://doi.org/10.1007/BF02762397
Vander Wall SB (2001) The evolutionary ecology of nut dispersal. Bot Rev 67:74–117
Verdú M, García-Fayos P (2001) The effect of deceptive fruits on predispersal seed predation by birds in Pistacia lentiscus. Plant Ecol 156:245–248. https://doi.org/10.1023/A:1012653002598
Warton DI, Duursma RA, Falster DS, Taskinen S (2012) Smatr 3- an R package for estimation and inference about allometric lines. Methods Ecol Evol 3:257–259
Weckerly FW, Sugg DW, Semlitsch RD (1989) Germination success of acorns (Quercus): insect predation and tannins. Can J For Res 19:811–815
Woodroof NC (1928) Development of the embryo sac and young embryo of hicoria pecan. Am J Bot 15:416. https://doi.org/10.2307/2435801
Acknowledgements
We thank the National Natural Science Foundation of China (NSFC, Grant Number 31460095), Center of Tree Science of Morton Arboretum, and School of Ecology and Environmental Sciences and Yunnan Key Laboratory for Plateau Mountain Ecology and Restoration of Degraded Environments (2019BC001) for financial support. We thank the National Herbarium Netherlands, the Harvard University Herbaria, United States National Herbarium, and the Herbarium of Kunming Institute of Botany of Chinese Academy of Sciences for providing the fruit samples. We thank Dr. Tetsuo Kohyama and Dr. Ian S. Pearse’s help with insect species identification. We thank Dr. Treasha R. Robertson and Dr. George Wang for copy-editing.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Membership of the Botanical Society of Japan: Takashi S. Kohyama.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chen, X., Kohyama, T.S. & Cannon, C.H. Fruit development of Lithocarpus (Fagaceae) and the role of heterochrony in their evolution. J Plant Res 133, 217–229 (2020). https://doi.org/10.1007/s10265-020-01168-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-020-01168-1