WAS THE EVOLUTION OF ANGIOSPERM-FRUGIVORE INTERACTIONS DRIVEN BY RECIPROCAL COEVOLUTION BETWEEN THEM?
DOI:
https://doi.org/10.4257/oeco.2020.2401.02Palavras-chave:
coevolution, dispersal syndromes, fleshy fruits, mutualism, paleoecologyResumo
The evolution of fruits contributed to the dominance of angiosperms and provided new ecological opportunities for frugivore vertebrates to diversify. However, it is not yet clear whether reciprocal coevolution between plants and frugivores drove the evolution of their mutualistic interactions. This review aimed at discussing major events of the evolution of fleshy-fruited angiosperms and their major seed dispersers, in order to elucidate if and how they responded to mutual selective pressures. Angiosperms evolved between the Mid and Late Cretaceous and they experienced a large diversification until the early Eocene. However, all main lineages of extant frugivores originated from the Eocene onward: frugivorous birds evolved in the Eocene but diversified in the Oligocene; primates evolved in the early Eocene and frugivorous bats diversified in the Oligocene-Miocene. This divergence in the times of the origins of angiosperm and their modern seed dispersers suggest that other animals interacted with early angiosperms. The most likely candidates are the rodent-like multituberculates. Several studies investigated how plant-frugivore mutualistic interactions contribute to the diversification in both plants and animals and we draw two main hypotheses from them: the plant-frugivore coevolutionary hypothesis and the neutral hypothesis. There are consistent evidences supporting each of these hypotheses, which suggest that they may not be mutually exclusives. An integrative approach is that plant-frugivore coevolution happens in pulses. Times of high environmental disturbances promote significant changes in mutualistic interactions and release new ecological opportunities for emerging species, which in turn exert stronger selective pressures and adaptive changes on fruit and frugivores traits. As evolving frugivores occupies those niches, interactions become more stable and coevolution is weaker and diffuse. We are currently undergoing a new period of unstable plant-frugivore interactions and we need more information on plant-frugivore coevolution in order to predict how species will respond to a changing world.
Referências
Abello, M. A., Toledo, N., & Ortiz-Jaureguizar, E. 2018. Evolution of South American Paucituberculata (Metatheria: Marsupialia): adaptive radiation and climate changes at the Eocene- Oligocene boundary. Historical Biology, 00(00), 1–18. DOI: 10.1080/08912963.2018.1502286
Albert, A., Auffret, A. G., Cosyns, E., Cousins, S. A. O., D’Hondt, B., Eichberg, C., Eycott, A. E., Heinken, T., Hoffmann, M., Jaroszewicz, B., Malo, J. E., Mårell, A., Mouissie, M., Pakeman, R. J., Picard, M., Plue, J., Poschlod, P., Provoost, S., Schulze, K. A., & Baltzinger, C. 2015. Seed dispersal by ungulates as an ecological filter: A trait-based meta-analysis. Oikos, 124(9), 1109–1120. DOI: 10.1111/oik.02512
Althoff, D. M., Segraves, K. A., & Johnson, M. T. J. 2014. Testing for coevolutionary diversification: linking pattern with process. Trends in Ecology & Evolution, 29(2), 82–89. DOI: 10.1016/j.tree.2013.11.003
Bach, C. E., & Kelly, D. 2004. Effects of forest edges, fruit display size, and fruit colour on bird seed dispersal in a New Zealand mistletoe, Alepis flavida. New Zealand Journal of Ecology, 28(1), 93–103.
Baker, R. J., Bininda-Emonds, O. R. P., Mantilla-Meluk, H., Porter, C. A., & Van Den Bussche, R. A. 2012. Molecular time scale of diversification of feeding strategy and morphology in New World Leaf-Nosed Bats (Phyllostomidae): a phylogenetic perspective. In: G. F. Gunnell (Ed.), Evolutionary History of Bats: Fossils, Molecules and Morphology, pp. 385–409. Cambridge: Cambridge University Press.
Baker, R. J., Solari, S., Cirranello, A., & Simmons, N. B. 2016. Higher level classification of Phyllostomid bats with a summary of DNA synapomorphies. Acta Chiropterologica, 18(1), 1–38. DOI: 10.3161/15081109ACC2016.18.1.001
Bakker, R. T. 1978. Dinosaur feeding behaviour and the origin of flowering plants. Nature, 274(5672), 661–663. DOI: 10.1038/274661a0
Barnosky, A. D., Matzke, N., Tomiya, S., Wogan, G. O. U., Swartz, B., Quental, T. B., Marshall, C., McGuire, J. L., Lindsey, E. L. Kaitlin, Maguire, C., Mersey, B., & Ferrer, E. A. 2011. Has the Earth’s sixth mass extinction already arrived? Nature, 471(7336), 51–57. DOI: 10.1038/nature09678
Barrett, P. M. 2014. Paleobiology of herbivorous dinosaurs. Annual Review of Earth and Planetary Sciences, 42(1), 207–230. DOI: 10.1146/annurev-earth-042711-105515
Bascompte, J., & Jordano, P. 2007. Plant-animal mutualistic networks: the architecture of biodiversity. Annual Review of Ecology, Evolution, and Systematics, 38(2007), 567–593. DOI: 10.1146/annurev.ecolsys.38.091206.095818
Beddow, H. M., Liebrand, D., Sluijs, A., Wade, B. S., & Lourens, L. J. 2016. Global change across the Oligocene-Miocene transition: high-resolution stable isotope records from IODP Site U1334 (equatorial Pacific Ocean). Paleoceanography, 31(1), 81–97. DOI: 10.1002/2015PA002820
Bloch, J. I., Silcox, M. T., Boyer, D. M., & Sargis, E. J. 2007. New Paleocene skeletons and the relationship of plesiadapiforms to crown-clade primates. Proceedings of the National Academy of Sciences, 104(4), 1159–1164. DOI: 10.1073/pnas.0610579104
Bloch, Jonathan I, & Boyer, D. M. 2002. Grasping primate origins. Science, 298(5598), 1606–1610. DOI: 10.1126/science.1078249
Bolmgren, K., & Eriksson, O. 2010. Seed mass and the evolution of fleshy fruits in angiosperms. Oikos, 119(4), 707–718. DOI: 10.1111/j.1600-0706.2009.17944.x
Bowen, G. J. 2007. Palaeoclimate: when the world turned cold. Nature, 445(7128), 607–608. DOI: 10.1038/445607a
Boyer, D. M., Costeur, L., & Lipman, Y. 2012. Earliest record of Platychoerops (Primates, Plesiadapidae), a new species from Mouras Quarry, Mont de Berru, France. American Journal of Physical Anthropology, 149(3), 329–346. DOI: 10.1002/ajpa.22119
Boyer, D. M., Evans, A. R., & Jernvall, J. 2010. Evidence of dietary differentiation among late Paleocene-early Eocene plesiadapids (mammalia, primates). American Journal of Physical Anthropology, 142(2), 194–210. DOI: 10.1002/ajpa.21211
Brodie, J. F. 2017. Evolutionary cascades induced by large frugivores. Proceedings of the National Academy of Sciences, 114(45), 11998–12002. DOI: 10.1073/pnas.1710172114
Brodribb, T. J., & Feild, T. S. 2010. Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecology Letters, 13(2), 175–183. DOI: 10.1111/j.1461-0248.2009.01410.x
Brouat, C., Garcia, N., Andary, C., & McKey, D. 2001. Plant lock and ant key: Pairwise coevolution of an exclusion filter in an ant-plant mutualism. Proceedings of the Royal Society B: Biological Sciences, 268(1481), 2131–2141. DOI: 10.1098/rspb.2001.1763
Brown, S. A. E., Scott, A. C., Glasspool, I. J., & Collinson, M. E. 2012. Cretaceous wildfires and their impact on the Earth system. Cretaceous Research, 36, 162–190. DOI: 10.1016/j.cretres.2012.02.008
Buerki, S., Forest, F., Stadler, T., & Alvarez, N. 2013. The abrupt climate change at the Eocene-Oligocene boundary and the emergence of South-East Asia triggered the spread of sapindaceous lineages. Annals of Botany, 112(1), 151–160. DOI: 10.1093/aob/mct106
Bunney, K., Bond, W. J., & Henley, M. 2017. Seed dispersal kernel of the largest surviving megaherbivore—the African savanna elephant. Biotropica, 49(3), 395–401. DOI: 10.1111/btp.12423
Burns, K. C. 2013. What causes size coupling in fruit-frugivore interaction webs? Ecology, 94(2), 295–300. DOI: 10.1890/12-1161.1
Butler, R. J., Barrett, P. M., Kenrick, P., & Penn, M. G. 2009. Diversity patterns amongst herbivorous dinosaurs and plants during the Cretaceous: implications for hypotheses of dinosaur/angiosperm co-evolution. Journal of Evolutionary Biology, 22(3), 446–459. DOI: 10.1111/j.1420-9101.2008.01680.x
Chapman, C. A., & Dunham, A. E. 2018. Primate Seed dispersal and forest restoration: an african perspective for a brighter future. International Journal of Primatology, 39(3), 427–442. DOI: 10.1007/s10764-018-0049-3
Chaves, Ó. M., Bicca-Marques, J. C., & Chapman, C. A. 2018. Quantity and quality of seed dispersal by a large arboreal frugivore in small and large Atlantic forest fragments. PLoS ONE, 13(3), 4–6. DOI: 10.1371/journal.pone.0193660
Chester, S. G. B., & Beard, K. C. 2012. New micromomyid plesiadapiforms (Mammalia, Euarchonta) from the Late Paleocene of Big Multi Quarry, Washakie Basin, Wyoming. Annals of Carnegie Museum, 80(2), 159–172. DOI: 10.2992/007.080.0204
Colinvaux, P. A., & Oliveira, P. E. 2001. Amazon plant diversity and climate through the Cenozoic. Palaeogeography, Palaeoclimatology, Palaeoecology, 166(1–2), 51–63. DOI: 10.1016/S0031-0182(00)00201-7
Connell, J. H. 1980. Diversity and the coevolution of competitors, or the ghost of competition past. Oikos, 35(2), 131. DOI: 10.2307/3544421
Corlett, R. T. 2017. Frugivory and seed dispersal by vertebrates in tropical and subtropical Asia: an update. Global Ecology and Conservation, 11, 1–22. DOI: 10.1016/j.gecco.2017.04.007
Correa, D. F., Álvarez, E., & Stevenson, P. R. 2015. Plant dispersal systems in Neotropical forests: availability of dispersal agents or availability of resources for constructing zoochorous fruits? Global Ecology and Biogeography, 24(2), 203–214. DOI: 10.1111/geb.12248
Correa, S. B., Costa-Pereira, R., Fleming, T., Goulding, M., & Anderson, J. T. 2015. Neotropical fish-fruit interactions: eco-evolutionary dynamics and conservation. Biological Reviews, 90(4), 1263–1278. DOI: 10.1111/brv.12153
Correa, S. B., Oliveira, P. C., Nunes da Cunha, C., Penha, J., & Anderson, J. T. 2018. Water and fish select for fleshy fruits in tropical wetland forests. Biotropica, 50(2), 312–318. DOI: 10.1111/btp.12524
Costa, J. M., Ramos, J. A., Timóteo, S., Silva, L. P., Ceia, R. S., & Heleno, R. H. 2018. Species activity promote the stability of fruit-frugivore interactions across a five-year multilayer network. BioRxiv, 421941. DOI: 10.1101/421941
Cracraft, J., Barker, F., & Cibois, A. 2003. Avian higher-level phylogenetics and the Howard and Moore checklist of birds. Complete Checklist of the Birds of the World, 2001(2947), 16–21.
Day, E., & Kokko, H. 2015. Relaxed selection when you least expect it: why declining bird populations might fail to respond to phenological mismatches. Oikos, 124(1), 62–68. DOI: 10.1111/oik.01340
Dumont, E. R. 2003. Bats and fruit: an ecomorphological approach. In: T. Kunz & M. B. Fenton (Eds.), Bat ecology. pp. 398–429. Chicago: University of Chicago Press.
Dumont, E. R., Dávalos, L. M., Goldberg, A., Santana, S. E., Rex, K., & Voigt, C. C. 2012. Morphological innovation, diversification and invasion of a new adaptive zone. Proceedings of the Royal Society B: Biological Sciences, 279(1734), 1797–1805. DOI: 10.1098/rspb.2011.2005
Ericson, P. G. P., Irestedt, M., & Johansson, U. S. 2003. Evolution, biogeography, and patterns of diversification in passerine birds. Journal of Avian Biology, 34(1), 3–15. DOI: 10.1034/j.1600-048X.2003.03121.x
Eriksson, O. 2008. Evolution of seed size and biotic seed dispersal in angiosperms: paleoecological and neoecological evidence. International Journal of Plant Sciences, 169(7), 863–870. DOI: 10.1086/589888
Eriksson, O. 2014. Evolution of angiosperm seed disperser mutualisms: the timing of origins and their consequences for coevolutionary interactions between angiosperms and frugivores. Biological Reviews, 91(1), 168–186. DOI: 10.1111/brv.12164
Fleming, T. H., & Kress, W. J. 2011. A brief history of fruits and frugivores. Acta Oecologica, 37(6), 521–530. DOI: 10.1016/j.actao.2011.01.016
Fleming, T. H., & Kress, W. J. 2013. The ornaments of life. Chicago: University of Chicago Press: p. 616. DOI: 10.7208/chicago/9780226023328.001.0001
Fort, H., Vázquez, D. P., & Lan, B. L. 2016. Abundance and generalisation in mutualistic networks: solving the chicken-and-egg dilemma. Ecology Letters, 19(1), 4–11. DOI: 10.1111/ele.12535
Galetti, M., Guevara, R., Côrtes, M. C., Fadini, R., Von Matter, S., Leite, A. B., Labecca, F., Ribeiro, T., Carvalho, C. S., Collevatti, R. G., Pires, M. M., Guimarães, P. R., Brancalion, P. H., Ribeiro, M. C., & Jordano, P. 2013. Functional extinction of birds drives rapid evolutionary changes in seed size. Science, 340(6136), 1086–1090. DOI: 10.1126/science.1233774
Gautier-Hion, A., Duplantier, J.-M., Quris, R., Feer, F., Sourd, C., Decoux, J.-P., Dubost, G., Emmons, L., Erard, C., Hecketsweiler, P., Moungazi, A., Roussilhon, C., & Thiollay, J.-M. 1985. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia, 65(3), 324–337. DOI: 10.1007/BF00378906
Gómez, J. M., & Verdú, M. 2012. Mutualism with plants drives primate diversification. Systematic Biology, 61(4), 567–577. DOI: 10.1093/sysbio/syr127
Hampe, A. 2003. Large-scale geographical trends in fruit traits of vertebrate-dispersed temperate plants. Journal of Biogeography, 30(4), 487–496. DOI: 10.1046/j.1365-2699.2003.00852.x
Hembry, D. H., Yoder, J. B., & Goodman, K. R. 2014. Coevolution and the diversification of life. The American Naturalist, 184(4), 425–438. DOI: 10.1086/677928
Herrera, C. M. 1985. Determinants of plant-animal coevolution: the case of mutualistic dispersal of seeds by vertebrates. Oikos, 44(1), 132–141. DOI: 10.2307/3544054
Herrera, C. M. 1998. Long-term dynamics of mediterranean frugivorous birds and fleshy fruits: a 12-year study. Ecological Monographs, 68(4), 511–538. DOI: 10.2307/2657152
Hubbell, S. P. 2001. The unified neutral theory of biodiversity and biogeography. Princeton: University Press: p. 448.
Jaramillo, C., Rueda, M. J., & Mora, G. 2006. Cenozoic plant diversity in the neotropics. Science, 311(5769), 1893–1896. DOI: 10.1126/science.1121380
Jarvis, E. D. et al. 2014. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science, 346(6215), 1320–1331. DOI: 10.1126/science.1253451
Jones, K. E., Bininda-Emonds, O. R. P., & Gittleman, J. L. 2005. Bats, clocks, and rocks: diversification patterns in Chiroptera. Evolution; International Journal of Organic Evolution, 59(10), 2243–2255. DOI: 10.1554/04-635.1
Jordano, P. 2017. Fruits and frugivory. In: M. Fenner (Ed.), Seeds: the ecology of regeneration in plant communities, pp. 125–165. Oxford: Oxford University Press. DOI: 10.1079/9780851994321.0125
Kainulainen, K., Persson, C., Eriksson, T., & Bremer, B. 2010. Molecular systematics and morphological character evolution of the Condamineeae (Rubiaceae). American Journal of Botany, 97(12), 1961–1981. DOI: 10.3732/ajb.1000090
Kissling, W. D., Böhning-Gaese, K., & Jetz, W. 2009. The global distribution of frugivory in birds. Global Ecology and Biogeography, 18(2), 150–162. DOI: 10.1111/j.1466-8238.2008.00431.x
Kristoffersen, A. V. 2002. An early Paleogene trogon (Aves: Trogoniformes) from the Fur Formation, Denmark. Journal of Vertebrate Paleontology, 22(3), 661–666.
Lambert, J. E. 2011. Primate nutritional ecology: feeding biology and diet at ecological and evolutionary scales. In: C. J., Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective. pp. 512–522. Oxford: Oxford University Press.
Lindow, B. E. K., & Dyke, G. J. 2006. Bird evolution in the Eocene: Climate change in Europe and a Danish fossil fauna. Biological Reviews of the Cambridge Philosophical Society, 81(4), 483–499. DOI: 10.1017/S146479310600707X
Lomáscolo, S. B., & Schaefer, H. M. 2010. Signal convergence in fruits: a result of selection by frugivores? Journal of Evolutionary Biology, 23(3), 614–624. DOI: 10.1111/j.1420-9101.2010.01931.x
Lomáscolo, S. B., Speranza, P., & Kimball, R. T. 2008. Correlated evolution of fig size and color supports the dispersal syndromes hypothesis. Oecologia, 156(4), 783–796. DOI: 10.1007/s00442-008-1023-0
Lord, J. 2004. Frugivore gape size and the evolution of fruit size and shape in southern hemisphere floras. Austral Ecology, 29(4), 430–436. DOI: 10.1111/j.1442-9993.2004.01382.x
Lorenzen, E. D. et al. 2011. Species-specific responses of Late Quaternary megafauna to climate and humans. Nature, 479(7373), 359–364. DOI: 10.1038/nature10574
Lotan, A., & Izhaki, I. 2013. Could abiotic environment shape fleshy fruit traits? A field study of the desert shrub Ochradenus baccatus. Journal of Arid Environments, 92, 34–41. DOI: 10.1016/j.jaridenv.2012.12.013
Mack, A. L. 2000. Did fleshy fruit pulp evolve as a defence against seed loss rather than as a dispersal mechanism? Journal of Biosciences, 25(1), 93–97. DOI: 10.1007/BF02985186
McLoughlin, S., & Pott, C. 2018. Plant mobility in the Mesozoic: Disseminule dispersal strategies of Chinese and Australian Middle Jurassic to Early Cretaceous plants. Palaeogeography, Palaeoclimatology, Palaeoecology, 515, 47–69. DOI: 10.1016/j.palaeo.2017.12.036
Miranda, E. B. P. 2017. The plight of reptiles as ecological actors in the tropics. Frontiers in Ecology and Evolution, 5, 159. DOI: 10.3389/fevo.2017.00159
Moles, A. T. 2005. A brief history of seed size. Science, 307(5709), 576–580. DOI: 10.1126/science.1104863
Nevo, O., & Valenta, K. 2018. The ecology and evolution of fruit odor: implications for primate seed dispersal. International Journal of Primatology, 39(3), 338–355. DOI: 10.1007/s10764-018-0021-2
Nevo, O., Valenta, K., Razafimandimby, D., Melin, A. D., Ayasse, M., & Chapman, C. A. 2018. Frugivores and the evolution of fruit colour. Biology Letters, 14(9). DOI: 10.1098/rsbl.2018.0377
Olesen, J. M., & Valido, A. 2003. Lizards as pollinators and seed dispersers: an island phenomenon. Trends in Ecology and Evolution, 18(4), 177–181. DOI: 10.1016/S0169-5347(03)00004-1
Omeja, P. A., Jacob, A. L., Lawes, M. J., Lwanga, J. S., Rothman, J. M., Tumwesigye, C., & Chapman, C. A. 2014. Changes in elephant abundance affect forest composition or regeneration? Biotropica, 46(6), 704–711. DOI: 10.1111/btp.12154
Pellmyr, O., & Leebens-Mack, J. 1999. Forty million years of mutualism: evidence for Eocene origin of the yucca-yucca moth association. Proceedings of the National Academy of Sciences, 96(16), 9178–9183. DOI: 10.1073/pnas.96.16.9178
Pontarp, M., & Petchey, O. L. 2018. Ecological opportunity and predator-prey interactions: linking eco-evolutionary processes and diversification in adaptive radiations. Proceedings of the Royal Society B: Biological Sciences, 285(1874). DOI: 10.1098/rspb.2017.2550
Pound, M. J., & Salzmann, U. 2017. Heterogeneity in global vegetation and terrestrial climate change during the late Eocene to early Oligocene transition. Scientific Reports, 7(1), 43386. DOI: 10.1038/srep43386
Price, S. L., Etienne, R. S., & Powell, S. 2016. Tightly congruent bursts of lineage and phenotypic diversification identified in a continental ant radiation. Evolution, 70(4), 903–912. DOI: 10.1111/evo.12894
Ramos-Robles, M., Dáttilo, W., Díaz-Castelazo, C., & Andresen, E. 2018. Fruit traits and temporal abundance shape plant-frugivore interaction networks in a seasonal tropical forest. Science of Nature, 105(3–4), 29. DOI: 10.1007/s00114-018-1556-y
Renoult, J. P., Valido, A., Jordano, P., & Schaefer, H. M. 2014. Adaptation of flower and fruit colours to multiple, distinct mutualists. New Phytologist, 201(2), 678–686. DOI: 10.1111/nph.12539
Rojas, D., Vale, Á., Ferrero, V., & Navarro, L. 2012. The role of frugivory in the diversification of bats in the Neotropics. Journal of Biogeography, 39(11), 1948–1960. DOI: 10.1111/j.1365-2699.2012.02709.x
Rojas, D., Warsi, O. M., & Dávalos, L. M. 2016. Bats (Chiroptera: Noctilionoidea) challenge a recent origin of extant Neotropical diversity. Systematic Biology, 65(3), 432–448. DOI: 10.1093/sysbio/syw011
Rother, D. C., Pizo, M. A., & Jordano, P. 2015. Variation in seed dispersal effectiveness: the redundancy of consequences in diversified tropical frugivore assemblages. Oikos, 125(3), 336–342. DOI: 10.1111/oik.02629
Sánchez, M. S., & Giannini, N. P. 2018. Trophic structure of frugivorous bats in the Neotropics: emergent patterns in evolutionary history. Mammal Review, 48(2), 90–107. DOI: 10.1111/mam.12116
Särkinen, T., Bohs, L., Olmstead, R. G., & Knapp, S. 2013. A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Evolutionary Biology, 13(1), 214. DOI: 10.1186/1471-2148-13-214
Schaefer, H. M., Schaefer, V., & Vorobyev, M. 2007. Are fruit colors adapted to consumer vision and birds equally efficient in detecting colorful signals? American Naturalist, 169(1), S159–S169. DOI: 10.1086/510097
Schluter, D. 2010. Resource competition and coevolution in sticklebacks. Evolution: Education and Outreach, 3(1), 54–61. DOI: 10.1007/s12052-009-0204-6
Seymour, G. B., Østergaard, L., Chapman, N. H., Knapp, S., & Martin, C. 2013. Fruit development and ripening. Annual Review of Plant Biology, 64(1), 219–241. DOI: 10.1146/annurev-arplant-050312-120057
Shanahan, M., So, S., Compton, S. G., & Corlett, R. 2001. Fig-eating by vertebrate frugivores: a global review. Biological Reviews, 76(4), 529–572. DOI: 10.1017/S1464793101005760
Shi, J. J., & Rabosky, D. L. 2015. Speciation dynamics during the global radiation of extant bats. Evolution, 69, 1528–1545. DOI: 10.1111/evo.12681
Simmons, N. B. 2005. An Eocene big bang for bats. Science, 307(5709), 527–528. DOI: 10.1126/science.1108871
Simmons, N. B., & Geisler, J. H. 1998. Phylogenetic relationships of Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx to extant bat lineages, with comments on the evolution of echolocation and foraging strategies in Microchiroptera. Bulletin of the American Museum of Natural History, 235, 4–182.
Simmons, N., & Conway, T. 2003. Evolution of ecological diversity in bats. In: T. H. Kunz & M. B. Fenton (Eds.), Bat ecology. pp. 493–535. Chicago: University of Chicago Press.
Smith, T., Habersetzer, J., Simmons, N. B., & Gunnell, G. F. 2012. Systematics and paleobiogeography of early bats. Evolutionary History of Bats: Fossils, Molecules and Morphology, January, 23–66. DOI: 10.1017/CBO9781139045599.003
Soltis, P. S., & Soltis, D. E. 2004. The origin and diversification of angiosperms. American Journal of Botany, 91(10), 1614–1626. DOI: 10.2307/4123855
Stournaras, K. E., & Schaefer, H. M. 2017. Does flower and fruit conspicuousness affect plant fitness? contrast, color coupling and the interplay of pollination and seed dispersal in two Vaccinium species. Evolutionary Ecology, 31(2), 229–247. DOI: 10.1007/s10682-016-9864-1
Sunyer, P., Muñoz, A., Bonal, R., & Espelta, J. M. 2013. The ecology of seed dispersal by small rodents: a role for predator and conspecific scents. Functional Ecology, 27(6), 1313–1321. DOI: 10.1111/1365-2435.12143
Sussman, R. W., Rasmussen, D. T., & Raven, P. H. 2013. Rethinking primate origins again. American Journal of Primatology, 75(2), 95–106. DOI: 10.1002/ajp.22096
Teeling, E. C. 2005. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science, 307(5709), 580–584. DOI: 10.1126/science.1105113
Tewksbury, J. J. 2002. Fruits, frugivores and the evolutionary arms race. New Phytologist, 156(2), 137–139. DOI: 10.1046/j.1469-8137.2002.00522.x
Thompson, J. N. 1999. The evolution of species interactions. Science, 284(5423), 2116–2118. DOI: 10.1126/science.284.5423.2116
Tiffney, B. H. 2004. Vertebrate dispersal of seed plants through time. Annual Review of Ecology, Evolution, and Systematics, 35(1), 1–29. DOI: 10.1146/annurev.ecolsys.34.011802.132535
Townsend, K. E. B., Rasmussen, D. T., Murphey, P. C., & Evanoff, E. 2010. Middle Eocene habitat shifts in the North American western interior: a case study. Palaeogeography, Palaeoclimatology, Palaeoecology, 297(1), 144–158. DOI: 10.1016/j.palaeo.2010.07.024
Valenta, K., Burke, R. J., Styler, S. A., Jackson, D. A., Melin, A. D., & Lehman, S. M. 2013. Colour and odour drive fruit selection and seed dispersal by mouse lemurs. Scientific Reports, 3, 2424. DOI: 10.1038/srep02424
Valenta, K., & Chapman, C. A. 2018. Primate-plant mutualisms: Is there evidence for primate fruit syndromes?. In: U. Kalbitzer & K. Jack (Eds.), Primate life histories, sex roles, and adaptability. pp. 245–255. Springer, Cham. DOI: 10.1007/978-3-319-98285-4_12
Valenta, K., Kalbitzer, U., Razafimandimby, D., Omeja, P., Ayasse, M., Chapman, C. A., & Nevo, O. 2018. The evolution of fruit colour: phylogeny, abiotic factors and the role of mutualists. Scientific Reports, 1–8. DOI: 10.1038/s41598-018-32604-x
van der Pijl, L. 1969. Principles of dispersal in higher plants. Berlin, Heidelberg: Springer Berlin Heidelberg. DOI: 10.1007/978-3-662-00799-0
Wheelwright, N. T. 1985. Fruit size, gape width, and the diets of fruit-eating birds. Ecology, 66(3), 808–818. DOI: 10.2307/1940542
Wiebes, J. T. 1979. Co-evolution of figs and their insect pollinators. Annual Review of Ecology and Systematics, 10(1), 1–12. DOI: 10.1146/annurev.es.10.110179.000245
Wilson, G. P., Evans, A. R., Corfe, I. J., Smits, P. D., Fortelius, M., & Jernvall, J. 2012. Adaptive radiation of multituberculate mammals before the extinction of dinosaurs. Nature, 483(7390), 457–460. DOI: 10.1038/nature10880
Xu, X., Zhou, Z., Dudley, R., Mackem, S., Chuong, C.-M., Erickson, G. M., & Varricchio, D. J. 2014. An integrative approach to understanding bird origins. Science, 346(6215), 1253293–1253293. DOI: 10.1126/science.1253293
Yoder, J. B., & Nuismer, S. L. 2010. When does coevolution promote diversification? The American Naturalist, 176(6), 802–817. DOI: 10.1086/657048
Yuan, C. X., Ji, Q., Meng, Q. J., Tabrum, A. R., & Luo, Z. X. 2013. Earliest evolution of multituberculate mammals revealed by a new Jurassic fossil. Science, 341(6147), 779–783. DOI: 10.1126/science.1237970
Zu, J., Wang, J., & Huang, G. 2016. Evolutionary diversification of prey and predator species facilitated by asymmetric interactions. PLoS ONE, 11(9), e0163753. DOI: 10.1371/journal.pone.0163753
