A pollination mutualism over the edge: growth form and fig traits respond differently during niche expansion to arid environments
DOI:
https://doi.org/10.38201/btha.abc.v54.9Keywords:
phenotype-by-environment, habitat selection, ecological niche, water stress, Karoo, phylogenetic constraints, host shiftAbstract
Background: It is unclear how climate shifts may interfere with the diversification of tightly associated species interactions. Obligate pollination mutualisms are ideal for investigating the underlying processes of niche evolution by environmental change.
Objectives: Niche evolution that corresponds with phenotype-by-environment interactions that include climate shifts is expected to affect the stability of partner associations of mutualisms. Here, we compare the evolution of fig syconium size and growth form strategies for coping with soil water stress during a range expansion by Ficus into arid environments.
Methods: Niche models of 31 Ficus taxa were used to define contemporary habitat requirements of each species, which are then incorporated into Bayesian mixed models to examine the response of each trait to the soil water variables, other environmental variables and phylogenetic dependencies.
Results: The results showed that phylogenetic constraints best explained syconium size variation, while environmental lability best characterised growth form variation. Two species adapted to arid environments that exhibited convergence in these traits had significantly different habitat requirements compared to forest and savanna species.
Conclusion: The niche expansions by Ficus ilicina and Ficus cordata involved distinct historical processes. The findings suggest selection for traits that varied at different temporal scales limit the rate of niche expansions, and potentially destabilise mutualist partnerships and promote host shifts.
Downloads
References
Ackerly, D.D., 2003, ‘Community assembly, niche conservatism, and adaptive evolution in changing environments’, International Journal of Plant Sciences, 164, S165–S184, https://doi.org/10.1086/368401.
Ackerly, D.D., Schwilk, D.W. & Webb, C.O., 2006, ‘Niche evolution and adaptive radiation: testing the order of trait divergence’, Ecology, 87, S50–S61, https://doi.org/10.1890/0012-9658(2006)87[50:NEAART]2.0.CO;2.
Amarasekare, P., 2004, ‘Spatial dynamics of mutualistic interactions’, Journal of Animal Ecology, 73, 128–142, https://doi.org/10.1046/j.0021-8790.2004.00788.x.
Anderson, B. & Johnson, S.D., 2008, ‘The geographical mosaic of coevolution in a plant-pollinator mutualism’, Evolution, 62, 220–225, https://doi.org/10.1111/j.1558-5646.2007.00275.x.
Armbruster, W.S., 2017, ‘The specialization continuum in pollination systems: diversity of concepts and implications for ecology, evolution and conservation’, Functional Ecology, 31, 88–100, https://doi.org/10.1111/1365-2435.12783.
Aung, K.M.M., Chen, H.H., Segar, S.T., Miao, B.G., Peng, Y.Q. & Liu, C., 2022, ‘Changes in temperature alter competitive interactions and overall structure of fig wasp communities’, Journal of Animal Ecology, 91, 1303–1315. https://doi.org/10.1111/1365-2656.13701.
Bazzaz, F.A., 1991, ‘Habitat selection in plants’, The American Naturalist, 137, S116–S130, https://doi.org/10.1086/285142.
Berg, C.C. & Corner, E.J.H., 2005, ‘Moraceae – Ficus’, Flora Malesiana Series I (Seed Plants) 17,2, National Herbarium of the Netherlands, Leiden.
Berg, C.C. & Wiebes, J.T., 1992, African fig trees and fig wasps. Koninklijke Nederlandse Akademie van Wetenschappen, Verhandelingen Afdeling Natuurkunde, Tweede Reeks, Amsterdam.
Bolnick, D.I., Amarasekare, P., Araújo, M.S., Bürger, R., Levine, J.M., Novak, M., … Vasseur D.A., 2011, ‘Why intraspecific trait variation matters in community ecology’, Trends in Ecology and Evolution, 26, 183–192, https://doi.org/10.1016/j.tree.2011.01.009.
Bridle, J.R. & Vines, T.H., 2007, ‘Limits to evolution at range margins: when and why does adaptation fail?’, Trends Ecology and Evolution, 22, 140–147. https://doi.org/10.1016/j.tree.2006.11.002.
Bronstein, J.L., 2001, ‘The costs of mutualism’, American Zoologist 41, 825–839, https://doi.org/10.1093/icb/41.4.825.
Burkle, L.A., Marlin, J.C. & Knight, T.M., 2013, ‘Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function’, Science, 339, 1611–1615, https://doi.org/10.1126/science.1232728.
Burrows, J. & Burrows, S., 2003, Figs of southern and south-central Africa, Umdaus Press, Hatfield, South Africa.
Calenge, C., 2006, ‘The package ‘adehabitat’ for the R software: a tool for the analysis of space and habitat use by animals’, Ecological Modelling, 197, 516–519, https://doi.org/10.1016/j.ecolmodel.2006.03.017.
Carscadden, K.A., Emery, N.C., Arnillas, C.A., Cadotte, M.W., Afkhami, M.E., Gravel, D., Livingstone, S.W. & Wiens, J.J., 2020, ‘Niche breadth: causes and consequences for ecology, evolution, and conservation’, The Quarterly Review of Biology, 95(3), 179–214, https://doi.org/10.1086/710388.
Cavender-Bares, J., Kozak, K.H., Fine, P.V. & Kembel, S.W., 2009, ‘The merging of community ecology and phylogenetic biology’, Ecology Letters, 12, 693–715, https://doi.org/10.1111/j.1461-0248.2009.01314.x.
Coelho, L.F.M., Ribeiro, M.C. & Pereira, R.A.S., 2014, ‘Water availability determines the richness and density of fig trees within Brazilian semideciduous forest landscapes’, Acta Oecologica, 57, 109–116, http://dx.doi.org/10.1016/j.actao.2013.02.002.
Compton, S.G. & Hawkins, B.A., 1992, ‘Determinants of species richness in southern African fig wasp assemblages’, Oecologia 91, 68–74, https://doi.org/10.1007/BF00317243.
Compton, S.G. & Van Noort, S., 1992, ‘Southern African fig wasps (Hymenoptera: Chalcidoidea): resource utilization and host relationships’, Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen 95, 423–435.
Cornille, A., Underhill, J.G., Cruaud, A., Hossaert-McKey, M., Johnson, S.D., Tolley, K.A., Kjellberg, F., Van Noort, S & Proffit, M., 2011, ‘Floral volatiles, pollinator sharing and diversification in the fig-wasp mutualism: insights from Ficus natalensis, and its two wasp pollinators (South Africa)’, Proceedings of the Royal Society London B: Biological Sciences, 279, https://doi.org/10.1098/rspb.2011.1972.
Cornwallis, C.K. & Uller, T., 2009, ‘Towards an evolutionary ecology of sexual traits’, Trends in Ecology and Evolution, 25, 145–152, https://doi.org/10.1016/j.tree.2009.09.008.
Cowling, R.M., Esler, K.J. & Rundel, P.W., 1999, ‘Namaqualand, South Africa–an overview of a unique winter-rainfall desert ecosystem’, Plant Ecology, 142, 3–21, https://doi.org/10.1023/A:1009831308074.
Cruaud, A., Cook, J., Da-Rong, Y., Genson, G., Jabbour-Zahab, R., Kjellberg, F. Pereira, R.A.S., Rønsted, N., Santos-Mattos, O., Savolainen, V., Ubaidillah, R., Van Noort, S., Yan-Qiong, P. & Rasplus, J.Y., 2011, ‘Fig-fig wasp mutualism, the fall of the strict cospeciation paradigm?’, pp. 68–102, in S. Patiny (ed.), Evolution of plant-pollinator relationships, Cambridge University Press, Cambridge, UK, https://doi.org/10.1017/CBO9781139014113.005.
Cruaud, A., Rønsted, N., Chantarasuwan, B., Chou, L.S., Clement, W.L., Couloux, A., … Hossaert-Mckey, M., 2012, ‘An extreme case of plant–insect codiversification: figs and fig-pollinating wasps’, Systematic Biology, 61, 1029–1047, https://doi.org/10.1093/sysbio/sys068.
Dayaram, A., Powrie, L., Rebelo, T. & Skowno, A., 2017, ‘Vegetation Map of South Africa, Lesotho and Swaziland 2009 and 2012: A description of changes from 2006’, Bothalia 47, 1–10, http://dx.doi.org/10.4102/abc.v47i1.2223.
De Vries, J.J., Selaolo, E.T. & Beekman, H.E., 2000, ‘Groundwater recharge in the Kalahari, with reference to paleo-hydrologic conditions’, Journal of Hydrology, 238, 110–123, https://doi.org/10.1016/S0022-1694(00)00325-5.
Dixon, D.J., 2003, ‘A taxonomic revision of the Australian Ficus species in the section Malvanthera (Ficus subg. Urostigma: Moraceae)’, Telopia, 10, 125–153, http://dx.doi.org/
7751/telopea20035611.
Dolédec, S., Chessel, D. & Gimaret-Carpentier, C., 2000, ‘Niche separation in community analysis: a new method’, Ecology, 81, 2914–2927, https://doi.org/10.1890/0012-9658(2000)081
:NSICAA]2.0.CO;2.
Dougill, A.J., Thomas, D.S. & Heathwaite, A.L., 2010, ‘Environmental change in the Kalahari: integrated land degradation studies for nonequilibrium dryland environments’, Annals of the Association of American Geographers, 89, 420–442, https://doi.org/10.1111/0004-5608.00156.
Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A., 2012, ‘Bayesian phylogenetics with BEAUti and the BEAST 1.7’, Molecular Biology and Evolution, 29, 1969–1973, https://doi.org/10.1093/molbev/mss075.
Dupont, L.M., Jahns, S., Marret, F., Ning, S., 2000, ‘Vegetation change in equatorial West Africa: time-slices for the last 150 ka’, Palaeogeography, Palaeoclimatology, Palaeoecology, 155, 95–122, https://doi.org/10.1016/S0031-0182(99)00095-4.
Duthie, A.B. & Nason, J.D., 2016, ‘Plant connectivity underlies plant-pollinator-exploiter distributions in Ficus petiolaris and associated pollinating and non-pollinating fig wasps’, Oikos, 125, 1597–1606, https://doi.org/10.1111/oik.02905.
Firetti, F., 2017, ‘Apomixis in Neotropical Vegetation’, in A. Sebata (ed.), Vegetation, InTech, http://dx.doi.org/10.5772/intechopen.71856.
Freckleton, R.P. & Jetz, W., 2008, ‘Space versus phylogeny: disentangling phylogenetic and spatial signals in comparative data’, Proceedings of the Royal Society London B: Biological Sciences, 276, 21–30, https://doi.org/10.1098/rspb.2008.0905.
Gilman, R.T., Fabina, N.S., Abbott, K.C. & Rafferty, N.E., 2011, ‘Evolution of plant-pollinator mutualisms in response to climate change’, Evolutionary Applications, 5, 2–16, https://doi.org/10.1111/j.1752-4571.2011.00202.x.
Gray, E.F. & Bond, W.J., 2015, ‘Soil nutrients in an African forest/savanna mosaic: drivers or driven?’, South African Journal of Botany, 101, 66–72, https://doi.org/10.1016/j.sajb.2015.06.003.
Guo, D., Desmet, P.G. & Powrie, L.W., 2017, ‘Impact of the future changing climate on the southern Africa biomes, and the importance of geology’, Journal of Geoscience and Environment and Protection, 5, 1–9, https://doi.org/10.4236/gep.2017.57001.
Hadfield, J.D. & Nakagawa, S., 2010, ‘General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters’, Journal of Evolutionary Biology, 23, 494–508, https://doi.org/10.1111/j.1420-9101.2009.01915.x.
Hao, G.Y., Goldstein, G., Sack, L., Holbrook, N.M., Liu, Z.H., Wang, A.Y., Harrison, R.D., Su, Z.H. & Cao, K.F., 2011, ‘Ecology of hemiepiphytism in fig species is based on evolutionary correlation of hydraulics and carbon economy’, Ecology, 92, 2117–2130, http://doi:10.1890/11-0269.1.
Hao, G-Y., Sack, L., Wang, A-Y., Cao, K-F. & Goldstein, G., 2010, ‘Differentiation in leaf water flux and drought tolerance traits in hemiepiphytic and non-hemiepiphytic Ficus tree species’, Functional Ecology, 24, 731–740, https://doi.org/10.1111/j.1365-2435.2010.01724.x.
Hawkins, B.A. & Compton, S.G., 1992, ‘African fig wasp communities: undersaturation and latitudinal gradients in species richness’, Journal of Animal Ecology, 6, 361–372.
Hoffmann, A.A. & Parsons, P.A., 1993, ‘Selection for adult desiccation resistance in Drosophila melanogaster: fitness components, larval resistance and stress correlations’, Biological Journal of the Linnean Society, 48, 43–54, https://doi.org/10.1111/j.1095-8312.1993.tb00875.x.
Holt, R.D., 2009, ‘Bringing the Hutchinsonian niche into the 21st century: ecological and evolutionary perspectives’, Proceedings of the National Academy of Sciences of the U.S.A., 106, 19659–19665, https://doi.org/10.1073/pnas.0905137106.
Huelsenbeck, J.P. & Ronquist, F., 2001, ‘MRBAYES: Bayesian inference of phylogenetic trees’, Bioinformatics, 17, 754–755, https://doi.org/10.1093/bioinformatics/17.8.754.
Ibanez, S., Arène, F. & Lavergne, S., 2016, ‘How phylogeny shapes the taxonomic and functional structure of plant–insect networks’, Oecologia, 180, 989–1000, https://doi.org/10.1007/s00442-016-3552-2.
Jacob, S., Bestion, E., Legrand, D., Clobert, J. & Cote, J., 2015, ‘Habitat matching and spatial heterogeneity of phenotypes: implications for metapopulation and metacommunity functioning’, Evolutionary Ecology, 29, 851–871, https://doi.org/10.1007/s10682-015-9776-5.
Jousselin, E., Rasplus, J-Y. & Kjellberg, F., 2003, ‘Convergence and coevolution in a mutualism: evidence from a molecular phylogeny of Ficus’, Evolution, 57, 1255–1269, https://doi.org/10.1111/j.0014-3820.2003.tb00334.x.
Joy, J.B., 2013, ‘Symbiosis catalyses niche expansion and diversification’, Proceedings of the Royal Society London B: Biological Sciences, 280, 20122820, https://doi.org/10.1098/rspb.2012.2820.
Jürgens, N., 1997, ‘Floristic biodiversity and history of African arid regions’, Biodiversity Conservation, 6, 495–514, https://doi.org/10.1023/A:1018325026863.
Kiers, E.T., Palmer, T.M., Ives, A.R., Bruno, J.F. & Bronstein, J.L., 2010, Mutualisms in a changing world: an evolutionary perspective’, Ecology Letters, 13, 1459–1474, https://doi.org/10.1111/j.1461-0248.2010.01538.x.
Krishnan, A., Pramanik, G.K., Revadi, S.V., Venkateswaran, V. & Borges, R.M., 2014, ‘High temperatures result in smaller nurseries which lower reproduction of pollinators and parasites in a brood site pollination mutualism’, PLoS One, 95, e115118, http://doi:10.1371/journal.pone.0115118.
Larcher, W., 2003, Physiological plant ecology: ecophysiology and stress physiology of functional groups, Springer Verlag, Berlin.
Lasky, J.R., Yang, J., Zhang, G., Cao, M., Tang, Y. & Keitt, T.H., 2014, ‘The role of functional traits and individual variation in the co-occurrence of Ficus species’, Ecology, 95, 978–990, https://doi.org/10.1890/13-0437.1.
Lehmann, C.E., Archibald, S.A., Hoffmann, W.A. & Bond, W.J., 2011, ‘Deciphering the distribution of the savanna biome’, New Phytologist, 191, 197–209, https://doi.org/10.1111/j.1469-8137.2011.03689.x.
Linder, H.P., 2014, ‘The evolution of African plant diversity’, Frontiers in Ecology and Evolution, 2, 38, https://doi.org/10.3389/fevo.2014.00038.
McLeish, M., Guo, D., Van Noort, S. & Midgley, G., 2011, ‘Life on the edge: rare and restricted episodes of a pan-tropical mutualism adapting to drier climates’, New Phytologist, 191, 210–222, https://doi.org/10.1111/j.1469-8137.2011.03683.x.
McLeish, M.J. & Van Noort, S., 2012, ‘Codivergence and multiple host species use by fig wasp populations of the Ficus pollination mutualism’, BMC Evolutionary Biology, 12, 1, https://doi.org/10.1186/1471-2148-12-1.
Mestre, A., Poulin, R. & Hortal, J., 2020, ‘A niche perspective on the range expansion of symbionts’, Biological Reviews, 95, 491–516, https://doi.org/10.1111/brv.12574.
Mucina, L. & Rutherford, M.C. (eds.), 2006, ‘The Vegetation of South Africa, Lesotho and Swaziland’, Strelitzia 19, South African National Biodiversity Institute, Pretoria.
Newman, E., Anderson, B. & Johnson, S.D., 2012, ‘Flower colour adaptation in a mimetic orchid’, Proceedings of the Royal Society London B: Biological Sciences, 279, 2309–2313, https://doi.org/10.1098/rspb.2011.2375.
Nieder, J., Prosperí, J., Michaloud, G., 2001, ‘Epiphytes and their contribution to canopy diversity’, in K.E. Linsenmair,, A.J. Davis,, B. Fiala & M.R. Speight (eds), Tropical Forest Canopies: Ecology and Management, Forestry Sciences, Vol 69, Springer, Dordrecht, https://doi.org/10.1007/978-94-017-3606-0_5.
Patiño, S., Herre, E.A. & Tyree, M.T., 1994, ‘Physiological determinants of Ficus fruit temperature and implications for the survival of pollinator wasp species: comparative physiology through an energy budget approach’, Oecologia, 100, 13–20, https://doi.org/10.1007/BF00317125.
Piedra-Malagón, E.M., Sosa, V. & Ibarra-Manríquez, G., 2011, ‘Clinal variation and species boundaries in the Ficus petiolaris complex (Moraceae)’, Systematic Botany, 36, 80–87, https://doi.org/10.1600/036364411X553153.
Pigliucci, M., 2003, ‘Phenotypic integration: studying the ecology and evolution of complex phenotypes’, Ecology letters, 6, 265–272, https://doi.org/10.1046/j.1461-0248.2003.00428.x.
Pyron, R.A., Costa, G.C., Patten, M.A. & Burbrink, F.T., 2015, ‘Phylogenetic niche conservatism and the evolutionary basis of ecological speciation’, Biological Reviews, 90, 1248–1262, https://doi.org/10.1111/brv.12154.
R Core Team, 2012, ‘R: A language and environment for statistical computing’, R Foundation for Statistical Computing, Vienna, Austria, from http://www.R-project.org/.
Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J., 2014, ‘Tracer v1.6.’, from http://beast.bio.ed.ac.uk/Tracer.
Renoult, J.P., Kjellberg, F., Grout, C., Santoni, S. & Khadari, B., 2009, ‘Cyto-nuclear discordance in the phylogeny of Ficus section Galoglychia and host shifts in plant-pollinator associations’, BMC Evolutionary Biology, 9, 1, https://doi.org/10.1186/1471-2148-9-248.
Rønsted, N., Salvo, G. & Savolainen, V., 2007, ‘Biogeographical and phylogenetic origins of African fig species (Ficus section Galoglychia)’, Molecular Phylogenetics and Evolution, 43, 190–201, https://doi.org/10.1016/j.ympev.2006.12.010.
Rowe, N. & Speck, T., 2005, ‘Plant growth forms: an ecological and evolutionary perspective’, New Phytologist, 166, 61–72, https://doi.org/10.1111/j.1469-8137.2004.01309.x.
Sachs, J.L. & Simms, E.L., 2006, ‘Pathways to mutualism breakdown’, Trends in Ecology and Evolution, 21, 585–592, https://doi.org/10.1016/j.tree.2006.06.018.
Salzmann, U. & Hoelzmann, P., 2005, ‘The Dahomey Gap: An abrupt climatically induced rain forest fragmentation in West Africa during the late Holocene’, Holocene, 15, 190–199, https://doi.org/10.1191/0959683605hl799rp.
Schulze, R.E., Maharaj, M., Warburton, M.L., Gers, C.J., Horan, M.J.C., Kunz, R.P. & Clark, D.J., 2007, South African atlas of climatology and agrohydrology, Water Research Commission, Pretoria, South Africa, WRC Report, 1489, 06.
Thébault, E. & Fontaine, C., 2010, ‘Stability of ecological communities and the architecture of mutualistic and trophic networks’, Science, 329, 853–856, https://doi.org/10.1126/science.1188321.
Van Noort, S. & Compton, S.G., 1996, ‘Convergent evolution of agaonine and sycoecine (Agaonidae, Chalcidoidea) head shape in response to the constraints of host fig morphology’, Journal of Biogeography, 23, 415–424, https://doi.org/10.1111/j.1365-2699.1996.tb00003.x.
Via, S. & Lande, R., 1985, ‘Genotype-environment interaction and the evolution of phenotypic plasticity’, Evolution, 39, 505–522, https://doi.org/10.1111/j.1558-5646.1985.tb00391.x.
Warren, M., Robertson, M.P. & Greeff, J.M., 2010, ‘A comparative approach to understanding factors limiting abundance patterns and distributions in a fig tree–fig wasp mutualism’, Ecography, 33, 148–158, https://doi.org/10.1111/j.1600-0587.2009.06041.x.
Werner, G.D., Cornelissen, J.H., Cornwell, W.K., Soudzilovskaia, N.A., Kattge, J., West, S. A. & Kiers, E.T., 2018, ‘Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown’, Proceeding of the National Academy of Sciences of the U.S.A., 115, 5229–5234, https://doi.org/10.1073/pnas.1721629115.
Zhang, L.S., Compton, S.G., Xiao, H., Lu, Q. & Chen, Y., 2014, ‘Living on the edge: Fig tree phenology at the northern range limit of monoecious Ficus in China’, Acta Oecologica, 57, 135–141, https://doi.org/10.1016/j.actao.2013.09.002.
Zotz, G. & Hietz, P., 2001, ‘The physiological ecology of vascular epiphytes: current knowledge, open questions’, Journal of Experimental Botany, 52, 2067–2078, https://doi.org/10.1093/jexbot/52.364.2067.
References (Supplementary material)
Hadfield, J., 2010, ‘MCMC methods for multi-response generalised linear mixed models: The MCMCglmm R package’, Journal of Statistical Software, 33, 1–22.
Schulze, R.E., 2007, ‘Soils: Agrohydrological Information Needs, Information Sources and Decision Support’, in R.E. Schulze (ed), South African Atlas of Climatology and Agrohydrology, Water Research Commission, Pretoria, RSA, WRC Report 1489/1/06, Section 4.1.
Schulze, R.E. & Horan, M.J.C., 2007, ‘Soils: Hydrological Attributes’, in R.E. Schulze (ed), South African Atlas of Climatology and Agrohydrology, Water Research Commission, Pretoria, RSA, WRC Report 1489/1/06, Section 4.2.
Schulze, R.E., Hull, P.J. & Maharaj, M., 2007, ‘Soil Water Stress’, in R.E. Schulze (ed), South African Atlas of Climatology and Agrohydrology, Water Research Commission, Pretoria, RSA, WRC Report 1489/1/06, Section 14.2.
Spiegelhalter, D.J., Best, N.G., Carlin, B.P. & Van Der Linde, A., 2002, ‘Bayesian measures of model complexity and fit’, Journal of the Royal Statistical Society: Series B, 64, 583–639, https://doi.org/10.1111/1467-9868.00353.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Michael McLeish, Danni Guo, Simon van Noort
This work is licensed under a Creative Commons Attribution 4.0 International License.
